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NCI Program Project in Esophageal Carcinogenesis

Publications

The following is a list of publications by faculty member and is available for download in pdf format.


Anil Rustgi Publications:

Nakagawa H, Wang TC, Zukerberg L, Odze R, Togawa K, May GHW, Wilson J, Rustgi AK.  The targeting of the cyclin D1 oncogene by an Epstein-Barr virus promoter in transgenic mice causes dysplasia in the tongue, esophagus and forestomach.  Oncogene 1997; 14:1185-1190. [PMC3266546]

Nakagawa H, Inomoto T, Rustgi AK.  A CACCC box like cis-regulatory element of the Epstein-Barr virus ED-L2 promoter interacts with a nuclear transcriptional factor in tissue-specific squamous epithelia.  J Biol Chem 272 1997;16688-16699. [pdf]

Jenkins TD, Nakagawa H, Rustgi AK.  The keratinocyte specific Epstein-Barr virus ED-L2 promoter is regulated by phorbol 12-myristate 13-Acetate through two cis-regulatory elements containing e-box and Krüppel-like factor motifs. J Biol Chem 1997; 272:24433-24442. [pdf]

Yan YX, Nakagawa H, Lee MH, Rustgi AK.  TGFa enhances cyclin D1 transcription through the binding of early-growth response protein to a cis-regulatory element in the cyclin D1 promoter. J Biol Chem  1997; 272:33181-33190. [pdf]

Mueller A, Odze R, Jenkins TD, Shahsesfaei A, Nakagawa H, Inomoto T, Rustgi AK.  A transgenic mouse model with cyclin D1 overexpression results in cell cycle, epidermal growth factor receptor and p53 abnormalities.  Cancer Research 1997; 57:5542-5549. [pdf]

Jenkins TD, Opitz OG, Okano J-I, Rustgi AK. Transactivation of the Human Keratin 4 and Epstein-Barr virus ED-L2 promoters by Gut-enriched Krüppel-like factor.  J Biol Chem 1998; 273: 17, 10747-10754. [pdf]

Compton CC, Warland G, Nakagawa H, Opitz OG, Rustgi AK.  Cellular characterization and successful transfection of serially subcultured normal human esophageal keratinocytes.  J Cellular Phys 1998;177: 274-281. [pdf]

Ness S, Edelmann W, Jenkins TD, Liedtke W, Rustgi AK, Kucherlapati R.  Mouse keratin 4 is necessary for internal epithelial integrity.  J Biol Chem 1998; 273: 23904-23911. [pdf]

Opitz OG, Jenkins TD, Rustgi AK.  Transcriptional regulation of the differentiation-linked human keratin 4 promoter is dependent upon esophageal-specific nuclear factors.  J Biol Chem 1998; 73: 3912-23921. [pdf]

Jenkins TD, Mueller A, Odze R, Shahsafaei A, Zukerberg LR, Kent R, Stoner GD, Rustgi AK. Cyclin D1 overexpression combined with N-nitrosomethylbenzylamine increases dysplasia and cellular proliferation in murine esophageal squamous epithelium.  Oncogene 1999; 18: 59-66. [pdf]

Brembeck FH, Opitz OG, Liebermann TA, Rustgi AK. Dual function of the epithelial specific ets transcription factor, ELF3, in modulating epithelial differentiation.  Oncogene 2000; 19:1941-1949. [pdf]

Okano J, Opitz OG, Nakagawa H, Jenkins TD, Friedman S, Rustgi AK. The Kruppel-like transcriptional factors Zf9 and GKLF coactivate the human keratin 4 promoter and physically interact.  FEBS letters 2000; 473: 95-100. [pdf]

Opitz OG, Rustgi AK.  Interaction between Sp1 and cell cycle regulatory proteins is important in transactivation of a differentiation-linked gene. Cancer Research 2000; 60: 2825-2830. [pdf]

Okano JI, Gaslightwala I,  Birnbaum MJ,  Rustgi AK, Hiroshi Nakagawa. Akt/Protein Kinase B isoforms are differentially regulated by epidermal growth factor stimulation. J Biol Chem 2000 Oct 6; 275(40): 30934-30942. [pdf]

Okano JI, Rustgi AK. Paclitaxel induces prolonged activation of the Ras/MEK/ERK pathway independently of activating the programmed cell-death machinery. J Biol Chem  2001; Jun 1; 276(22): 19555-19564. [pdf]

Opitz OG, Suliman Y, Hahn WC, Harada H, Blum HE, Rustgi AK. Cyclin D1 overexpression and p53 inactivation immortalize primary oral keratinocytes by a telomerase independent mechanism. Journal of Clinical Investigation. 2001;108:725-732. (Commentary in Journal of Clinical Investigation and Nature Cancer Reviews). [PMC209376]

Suliman Y, Opitz OG, Avadhani A, Burns TF, El-Deiry WS, Wong D, Rustgi AK.  p63 expression is associated with p53 loss in oral-esophageal epithelia of p53 deficient mice. Cancer Research 2001; 61: 6467-6473. [pdf]

O'Shaughnessy JA, Kelloff GJ, Gordon GB, Dannenberg AJ, Hong WK, Fabian CJ, Sigman CC, Bertagnolli MM, Stratton SP, Lam S, Nelson WG, Meyskens FL, Alberts DS, Follen M, Rustgi AK, Papadimitrakopoulou V, Scardino PT, Gazdar AF, Wattenberg LW, Sporn MB, Sakr WA, Lippman SM, Von Hoff DD. Treatment and prevention of intraepithelial neoplasia: an important target for accelerated new agent development : recommendations of the american association for cancer research task force on the treatment and prevention of intraepithelial neoplasia. Clin Cancer Res 2002; 8(2): 314-346. [pdf]

Opitz OG, Harada H, Suliman Y, Rhoades B, Sharpless NE, Kent R, Kopelovich L, Nakagawa H, Rustgi AK.  A mouse genetic model of human oral-esophageal cancer.  Journal of Clinical Investigation 2002: 110:761-769. [PMC151126]

Andl CD, Mizushima T, Nakagawa H, Oyama K, Harada H, Chruma K, Herlyn M, Rustgi AK. Epidermal growth factor receptor mediates increased cell proliferation, migration, and aggregation in esophageal keratinocytes in vitro and in vivo.  J Biol Chem 2003; 278(3):1824-1830.* [pdf]

Mizushima T, Nakagawa H, Rustgi AK. Wnt-1 but not EGF is required for b-Catenin-T cell factor dependent transcription in esophageal cancer. Cancer Research  2002; 62: 277-282. [pdf]

Okano J, Snyder L, Rustgi AK.  Genetic alterations in esophageal cancer. Methods Mol Biol  2003; 222:131-145.

Harada H, Nakagawa N, Oyama K, Takaoka T, Andl C, Jacobmeier B, Enders GH, Opitz OG, Rustgi AK. Telomerase induces immortalization of human esophageal keratinocytes without p16INK4a inactivation.  Molecular Cancer Research 2003; 1:729-738. [pdf]

Fong LY, Mancini R, Nakagawa H, Rustgi AK, Huebner K. Combined cyclin D1 overexpression and zinc deficiency disrupts cell cycle and accelerates mouse forestomach carcinogenesis. Cancer Res 2003; 63: 4244-4252. [pdf]

Andl CD, Mizushima T, Oyama K, Bowser M, Nakagawa H, Rustgi AK.  EGFR induced cell migration is mediated predominantly by the JAK/Stat pathway in primary esophageal keratinocytes. Am J Physiol Gastrointest Liver Physiol. 2004 Jul 29 (epub on-line) [pdf]

Kim SH, Kim K, Kwagh JG, Dicker DT, Herlyn M, Rustgi AK, Chen Y, El-Deiry WS.  Death induction by recombinant native TRAIL and its prevention by a caspase 9 inhibitor in primary human esophageal epithelial cells. J Biol Chem 2004; Jun 28. [pdf]

Benzeno S, Lu F, Guo M, Herman JG, Barbash O, Zhang F, Klein PS, Rustgi AK, Diehl JA. Identification of mutations that disrupt phosphoryltaion-dependent nuclear export of cyclin D1. Oncogene 2006 May 29. Epub. [pdf]

Oyama K, Okawa T., Nakagawa H, Takaoka M, Andl CD, Kim SH, Klein-Szanto A, Diehl JA, Herlyn M, El-Deiry W, Rustgi AK. AKT induces senescence in primary esophageal epithelial cells but is permissive for differentiation as revealed in organotypic culture. Oncogene 2006 October 9, Epub. [PMC2996093]

Andl CD , Fargnoli B, Okawa T, Bowser M, Takaoka M, Nakagawa H, Klein-Szanto A, Hua X, Herlyn M, Rustgi AK. Coordinated functions of E-cadherin and TGF¾ receptor II in vitro and in vivo. Cancer Research  2006; 66(20) on-line. [PMC2996096]

Lin D, Barbash O, Kumar S, Weber J, Harper W, Klein-Szanto A, Rustgi AK, Fuchs S, Diehl JA. Phosphorylation-dependent ubiquitination of cyclin D1 by the SCFFBX4-alphaBcrystallin complex. Molecular Cell  2006; 24(3): 355-366. [PMC1702390]

Grandis JR, Carbone DP, Rustgi AK. Advances and challenges in aerodigestive epithelial cancer: meeting summary and research opportunities. Cancer Research  2007; 67(16):7556-7558. [pdf]

Okawa T, Michaylira CZ, Nakagawa H, Andl CD, Stairs DB, Johnstone CN, Klein-Szanto AJP, El-Deiry WS, Cukierman E, Herlyn M, Rustgi AK.  The functional interplay between EGFR overexpression, hTER activation and p53 mutation in esophageal epithelial cells with activation of stromal fibroblasts induce tumor development, invasion and differentiation.  Genes & Development  2007; 21: 2788-2083.  [PMC2045132]

Harada H, Nakagawa H, Takaoka M, Lee J, Gimotty P, Herlyn M, Diehl AJ, Rustgi AK.  Cleavage of MCM2 licensing proteins fosters senescence in human keratinocytes.  Cell Cycle 2008; 7(22): 3534-3538. [PMC2736109]

Barbash O, Zamfirova P, Lin DI, Chen LX, Yang K, Nakagawa H, Lu F, Rustgi AK, Diehl JA.  Mutations in Fbx4 inhibit phosphorylation-dependent dimerization of the SCF-Fbx4 ligase and contribute to cyclin D1overexpression in human cancer. Cancer Cell 2008; 14(1):68-78. [PMC2597358]

Stairs D, Nakagawa H, Klein-Szanto A, Mitchell S, Silberg D, Gimotty P, Tobias J, Lynch J, Rustgi AK.  Cdx1 and c-myc Foster the Initiation of Transdifferentiation of the Normal Esophageal Squamous Epithelium towards Barrett's Esophagus. PLoS Once 2008; 3(10):e3534. [PMC2568822]

Lioni M, Noma K, Snyder A, Klein-Szanto A, Diehl JA, Rustgi AK, Herlyn M, Smalley KS. Bortezomib induces apoptosis in esophageal squamous cell carcinoma cells through activation of the p38 mitogen-activated protein kinase pathway.  Mol Cancer Ther. 2008 Sep;7(9):2866-75. [PMC2903039]

Harada H, Nakagawa H, Takaoka M, Lee J, Gimotty P, Herlyn M, Diehl AJ, Rustgi AK.  Cleavage of MCM2 licensing proteins fosters senescence in human keratinocytes.  Cell Cycle 2008 Nov 15; 7(22):3534-3538. Epub 2008 Nov. 18 [PMC2736109]

Kalabis J, Oyama K, Okawa T, Nakagawa H, Michaylira CZ, Stairs DB, Figueiredo JL, Mahmood U, Diehl JA, Herlyn M, Rustgi AK. A subpopulation of mouse esophageal basal cells has properties of stem cells with the capacity for self-renewal and lineage specification. J Clin Invest 2008 Dec; 118(12):38360-3869. [PMC2579884]

Kalabis J, Li G, Fukunaga-Kalabis M, Rustgi AK, Herlyn M. Endothelin-3 stimulates survival of goblet cells in organotypic cultures of fetal human colonic epithelium. Am J Physiol Gastrointest Liver Physiol 2009 Dec; 295(6):1182-1189. [PMC2604801]

Kong J, Nakagawa H, Isariyawongse B, Funakoshi S, Silberg D, Rustgi AK, Lynch JP.  Induction of intestinalizatioin in human esophageal keratinocytes is a multi-step process. Carcinogenesis 2009 Jan; 30(1):122-30. [PMC2722140]

Wilkey JF, Buchberger G, Saucier K, Patel SM, Eisenberg E, Nakawawa H, Michaylira CZ, Rustgi AK, Mallya SM. Cyclin D1 overexpression increases susceptibility to 4-nitroquinoline-1-oxide-induced dysplasia and neoplasia in murine squamous oral epithelium. Mol Carcinog 2009 Sep; 48(9):853-861. [PMC2736315]

Bass AJ, Watanabe H, Mermel CH, Yu S, Perner S, Verhaak RG, Kim Sy, Wardwell L, Tamayo P, Gat-Viks I, Ramos AH, Woo MS, Weir BA, Getz G, Beroukhim R, O'Kelly M, Dutt A, Rozenblatt-Rosen O, Dziunycz P, Komisarof J, Chirieac LR, Lafargue CJ, Scheble V, Wilbertz T, Ma C, Rao S, Nakagawa H, Stairs DB, Lin L, Giordano TJ, Wagner P, Minna JD, Gazdar AF, Zhu CQ, Brose MS, Cecconello I, Jr UR, Marie SK, Dahl O, Shivdasani RA, Tsao MS, Rubin MA, Wong KK, Regev A, Hahn WC, Beer DG, Rustgi AK, Meyerson M. SOX2 is an amplified lineage-survival oncogene in lung and esophageal squamous cell carcinomas. Nat Genet. 2009 Nov; 41(11):1238-42. [PMC2783775]

Okumura T, Wang S, Takaishi S, Tu S, Ng V, Ericksen R, Rustgi AK, and Wang T. Identification of a bone marrow-derived mesenchymal progenitor cell subset that can contribute to the gastric epithelium. Lab Invest 2009 Dec; 89(12):1410-22. [PMC2917339]

Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J, Barretina J, Boehm JS, Dobson J, Urashima M, McHenry KT, Pinchback RM, Ligon AH, Cho YJ, Haery L, Greulich H, Reich M, Winckler W, Lawrence MS, Weir BA, Tanaka KE, Chiang DY, Bass AJ, Loo A, Hoffman C, Prensner J, Liefeld T, Gao Q, Yecies D, Signoretti S, Maher E, Kaye FJ, Sasaki H, Tepper JE, Fletcher JA, Tabernero J, Baselga J, Tsao MS, Demichelis F, Rubin MA, Janne PA, Daly MJ, Nucera C, Levine RL, Ebert BL, Gabriel S, Rustgi AK, Antonescu CR, Ladanyi M, Letai A, Garraway LA, Loda M, Beer DG, True LD, Okamoto A, Pomeroy SL, Singer S, Golub TR, Lander ES, Getz G, Sellers WR, Meyerson M. The landscape of somativ copy-number alteration across human cancers. Nature 2010 Feb; 463(7283):899-905. PMID: 20164920 [PMC2826709]

Andl CS, McCowan KM, Allison GL, Rustgi AK. Cathepsin B is the driving force of esophageal cell invasion in a fibroblast-dependent manner. Neoplasia 2010; 12(6):485-498 [PMC2887089]

Grugan K, Miller CG, Yao Y, Michaylira C, Ohashi S, Klein-Szanto AJ, Diehl JA, Herlyn M, Han M, Nakagawa H, Rustgi AK. Fibroblasts secreted hepatocyte growth factor is essential for esophageal squamous cell carcinoma invasion. Proceedings of the National Academy of Sciences. 2010; 107(24):11026-11031 [PMC2890722]

Michaylira C, Wong GS, Miller CG, Gutierrez CM, Nakagawa H, Hammond R, Klein-Szanto AJ, Lee JS, Herlyn M, Diehl JA, Gimotty P, Rustgi AK. Periostin, a cell adhesion molecule, facilitates invasion in the tumor microenvironment and annotes a novel tumor invasive signature in esophageal cancer. Cancer Research 2010; 70(13):5281-5292 [PMC3274349]

Ohasi S, Natsuizaka M, Wong G, Michaylira C, Grugan K, Stairs DB, Kalabis J, Vega ME, Kalman R, Nakagawa M, Klein-Szanto AJ, Herlyn M, Diehl JA, Rustgi AK, Nakagawa H.  EGFR and mutant p53 expand esophageal cellular subpopulation capable of epithelial-to-mesenchymal transition through ZEB transcription factors.  Cancer Research  2010; 116(23): 4948-4957.  [PMC3007622]

Aggarwal P, Vaites LP, Kim JK, Mellert H, Nakagawa H, Herlyn M, Rustgi A, McMahon SB, Diehl JA. Nuclear Cyclin D1/CDK4 minase regulates CUL4 expression and triggers neoplastic growth via activation of the PRMT5 methyltransferase.  Cancer Cell  2010; 18(4): 329-340. [PMC295747]

Kashyap MK, Harsha HC, Renuse S, Pawar H, Patankar N, Kim M-S, Marimuthu A, Keerthikumar S, Muthusamy B, Kandasamy K, Subbannayya Y, Prasad TSK, Rajagopalan S, Waddell K, Mahmood R, Chaerkady R, Meltzer SJ, Kumar RV, Rustgi AK, Pandey A.  SILAC based quantitative proteomic approach for identification of potential biomarkers from esophageal.  [PMC3093916]

Stairs DB, Bayne LJ, Rhoades B, Vega ME, Kalabis J, Klein-Szanto JA, Lee J-S, Katz JP, Diehl JA, Vonderheide RH, Reynolds AB, Rustgi AK.  Deletion of p120-catenin results in a tumor microenvironment with inflammation and cancer that establishes it as a bone fide tumor suppressor.  Cancer Cell  2011; 19(4): 470-483.  [PMC3077713]

Basu D, Nguyen T-T, Montone KT, Zhang G, Wang L-P, Diehl JA, Rustgi AK, Lee JT, Weinstein GS, Herlyn M. Evidence for mesenchymal sub-populations within squamous cell carcinomas exhibiting chemoresistance and phenotypic plasticity. Oncogene 2010; 29(29): 4170-4182.  [PMC3039880]

Quante M, Bhagat G, Abrams JA, Marache F, Good P, Lee MD, Lee Y, Friedman R, Asfaha S, Dubeykovskaya Z, Mahmood U, Figueiredo JL, Kitajewski J, Shawber C, Lightdale CJ, Rustgi AK, Wang TC.  Bile acid and inflammation activate gastric cardia stem cells in a mouse model of Barrett-like metaplasia. Cancer Cell. 2012; 21(1):36-51. [PMC3266546]

Kalabis J, Wong GS, Vega ME, Natsuizaka M, Robertson ES, Herlyn M, Nakagawa H, Rustgi AK. Isolation and characterization of mouse and human esophageal epithelial cells in 3D organotypic culture. Nat Protoc. 2012; 7(2):235-46. doi: 10.1038/nprot.2011.437. [PMC3505594]

Patel ZS, Grugan KD, Rustgi AK, Cucinotta FA, Huff JL. Ionizing radiation enhances esophageal epithelial cell migration and invasion through a paracrine mechanism involving stromal-derived hepatocyte growth factor. Radiat Res. 2012; 177(2):200-8. Epub 2011 Nov 11. [PMID: 22077339]

Kosoff RE, Gardiner KL, Merlo LM, Pavlov K, Rustgi AK, Maley CC. Development and characterization of an organotypic model of Barrett's esophagus. J Cell Physiol. 2012; 227(6):2654-9. doi: 10.1002/jcp.23007.  [PMC3352665]

Predina JD, Judy B, Aliperti LA, Fridlender ZG, Blouin A, Kapoor V, Laguna B, Nakagawa H, Rustgi AK, Aguilar L, Aguilar-Cordova E, Albelda SM, Singhal S. Neoadjuvant in situ gene-mediated cytotoxic immunotherapy improves postoperative outcomes in novel syngeneic esophageal carcinoma models.  Cancer Gene Ther. 2011; 18(12):871-83. doi: 10.1038/cgt.2011.56. Epub 2011 Aug 26. [PMC3215998]

Weber SM, Bornstein S, Li Y, Malkoski SP, Wang D, Rustgi AK, Kulesz-Martin MF, Wang XJ, Lu SL. Tobacco-specific carcinogen nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone induces AKT activation in head and neck epithelia. Int J Oncol. 2011; 39(5):1193-8. doi: 10.3892/ijo.2011.1149. Epub 2011 Aug 5. [PMC3249931]

Matkar SS, Durham A, Brice A, Wang TC, Rustgi AK, Hua X. Systemic activation of K-ras rapidly induces gastric hyperplasia and metaplasia in mice. Am J Cancer Res. 2011; 1(4):432-445. [PMC3134228]

Basu D, Montone KT, Wang LP, Gimotty PA, Hammond R, Diehl JA, Rustgi AK, Lee JT, Rasanen K, Weinstein GS, Herlyn M. Detecting and targeting mesenchymal-like subpopulations within squamous cell carcinomas. Cell Cycle. 2011; 10(12):2008-16.  [PMC3154419]

Vaites LP, Lee EK, Lian Z, Barbash O, Roy D, Wasik M, Klein-Szanto AJ, Rustgi AK, Diehl JA. The Fbx4 tumor suppressor regulates cyclin D1 accumulation and prevents neoplastic transformation.  Mol Cell Biol. 2011; 31(22):4513-23. Epub 2011 Sep 12. [PMC3209253]

Basu D, Montone KT, Wang LP, Gimotty PA, Hammond R, Diehl JA, Rustgi AK, Lee JT, Rasanen K, Weinstein GS, Herlyn M. Detecting and targeting mesenchymal-like subpopulations within squamous cell carcinomas. Cell Cycle  2011; 10(12):2008-2016.  [PMC3154419]

Matkar SS, Durham A, Brice A, Wang TC, Rustgi AK, Hua X. Systemic activation of K-ras rapidly induces gastric hyperplasia and metaplasia in mice. Am J Cancer Res  2011; 1(4):432-445. [PMC3134228]

Stairs DB, Bayne LJ, Rhoades B, Vega ME, Kalabis J, Klein-Szanto JA, Lee J-S, Katz JP, Diehl JA, Vonderheide RH, Reynolds AB, Rustgi AK.  Deletion of p120-catenin results in a tumor microenvironment with inflammation and cancer that establishes it as a bone fide tumor suppressor.  Cancer Cell  2011; 19(4): 470-483.  [PMC3077713]

Weber SM, Bornstein S, Li Y, Malkoski SP, Wang D, Rustgi AK, Kulesz-Martin MF, Wang XJ, Lu SL. Tobacco-specific carcinogen nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone induces AKT activation in head and neck epithelia. Int J Oncol. 2011; 39(5):1193-1198. doi: 10.3892/ijo.2011.1149. Epub 2011 Aug 5. [PMC3249931]

Predina JD, Judy B, Aliperti LA, Fridlender ZG, Blouin A, Kapoor V, Laguna B, Nakagawa H, Rustgi AK, Aguilar L, Aguilar-Cordova E, Albelda SM, Singhal S. Neoadjuvant in situ gene-mediated cytotoxic immunotherapy improves postoperative outcomes in novel syngeneic esophageal carcinoma models.  Cancer Gene Ther  2011; 18(12):871-883. doi: 10.1038/cgt.2011.56. Epub 2011 Aug 26. [PMC3215998]

Kosoff RE, Gardiner KL, Merlo LM, Pavlov K, Rustgi AK, Maley CC. Development and characterization of an organotypic model of Barrett's esophagus. J Cell Physiol  2012; 227(6):2654-2659. [PMC3352665]

Masterson JC, McNamee EN, Hosford L, Capocelli KE, Ruybal J, Fillon SA, Doyle AD, Eltzschig HK, Rustgi AK, Protheroe CA, Lee NA, Lee JJ, Furuta GT.  Local hypersensitivity reaction in transgenic mice with squamous epithelial IL-5 overexpression provides a novel model of eosinophilic oesophagitis.  Gut. 2012 Nov 17. [PMID: 23161496]

Quante M, Bhagat G, Abrams JA, Marache F, Good P, Lee MD, Lee Y, Friedman R, Asfaha S, Dubeykovskaya Z, Mahmood U, Figueiredo JL, Kitajewski J, Shawber C, Lightdale CJ, Rustgi AK, Wang TC. Bile acid and inflammation activate gastric cardia stem cells in a mouse model of Barrett-like metaplasia. Cancer Cell  2012; 21(1):36-51. [PMC3266546]

Kalabis J, Wong GS, Vega ME, Natsuizaka M, Robertson ES, Herlyn M, Nakagawa H, Rustgi AK. Isolation and characterization of mouse and human esophageal epithelial cells in 3D organotypic culture. Nat Protoc  2012; 7:235-246.  [PMC3505594]

Wong GS, Rustgi AK. Matricellular proteins: priming the tumour microenvironment for cancer development and metastasis. Br J Cancer. 2013 Mar 5;108(4):755-61. [PMC3590656]

Wong GS, Habibollahi P, Heidari P, Lee JS, Klein-Szanto AJ, Waldron TJ, Gimotty PA, Nakagawa H, Taylor PR, Wang TC, Mahmood U, Rustgi AK.  Optical imaging of periostin enables early endoscopic detection and characterization of esophageal cancer in mice. Gastroenterology. 2013 Feb;144(2):294-7. [PMC3624041]

Kadaba R, Birke H, Wang J, Hooper S, Andl CD, Di Maggio F, Soylu E, Ghallab M, Bor D, Froeling FE, Bhattacharya S, Rustgi AK, Sahai E, Chelala C, Sasieni P, Kocher HM.  Imbalance of desmoplastic stromal cell numbers drives aggressive cancer processes. J Pathol. 2013 May;230(1):107-17. [PMID: 23359139]

Gupta M, Iyer PG, Lutzke L, Gorospe EC, Abrams JA, Falk GW, Ginsberg GG, Rustgi AK, Lightdale CJ, Wang TC, Fudman DI, Poneros JM, Wang KK. Recurrence of esophageal intestinal metaplasia after endoscopic mucosal resection and radiofrequency ablation of Barrett's esophagus: results from a US Multicenter Consortium.  Gastroenterology  2013 Jul; 145(1):79-86. [PMC3696438]

Li, K, Jiang M,  Lu, Y, Chen H, Sun J,  Wu S, Ku WY, Nakagawa H, Kita Y, Natsugoe S, Peters JH, Rustgi AK, Onaitis MW, Kiernan A, Chen X, Que J: Sox2 Cooperates with Inflammation-Mediated Stat3 Activation in the Malignant Transformation of Foregut Basal Progenitor Cells. Cell Stem Cell 2013 Mar 7; 12(3):304-315. [PMC3594795]

Wong GS, Lee JS, Park YY, Klein-Szanto AJ, Waldron TJ, Cukierman E, Herlyn M, Gimotty PA, Nakagawa H, Rustgi AK. Periostin cooperates with mutant p53 to mediate invasion through the induction of STAT1 signaling in the esophageal tumor microenvironment.  Oncogenesis. 2013 Aug 5; 2:e59. [PMC3759121]

Basu D, Bewley AF, Sperry SM, Montone KT, Gimotty PA, Rasanen K, Facompre ND, Weinstein GS, Nakagawa H, Diehl JA, Rustgi AK, Herlyn M.  EGFR Inhibition Promotes an Aggressive Invasion Pattern Mediated by Mesenchymal-like Tumor Cells within Squamous Cell Carcinomas.  Molecular Cancer Therapeutics 2013 Aug 12. [PMC3796003]

Waldron TJ, Quatromoni JG, Karakasheva TA, Singhal S, Rustgi AK.  Myeloid derived suppressor cells: Targets for therapy.  Oncoimmunology. 2013 Apr 1;2(4):e24117. [PMC3654606]

Grugan KD, Vega ME, Wong GS, Diehl JA, Bass AJ, Wong KK, Nakagawa H, Rustgi AK.  A common p53 mutation (R175H) activates c-Met receptor tyrosine kinase to enhance tumor cell invasion. Cancer Biol Ther. 2013;14(9). [PMID: 23792586]

Rasanen K, Sriswasdi S, Valiga A, Tang HY, Zhang G, Perego M, Somasundaram R, Li L, Speicher K, Klein-Szanto A, Basu D, Rustgi AK, Speicher DW, Herlyn M. Comparative secretome analysis of epithelial and mesenchymal subpopulations of head and neck squamous cell carcinoma identifies S100A4 as a potential therapeutic target. Molecular and Cellular Proteomics. Mol Cell Proteomics 2013 Dec;12(12):3778-92. [PMC3861723] 

Watanabe H, Ma Q, Peng S, Adelmant G, Swain D, Song W, Fox C, Francis JM, Pedamallu CS, DeLuca DS, Brooks AN, Wang S, Que J, Rustgi AK, Wong KK, Ligon KL, Liu XS, Marto JA, Meyerson M, Bass AJ. SOX2-p63 interaction and genomic co-localization in squamous cell carcinomas. Under re-review in Journal of Clinical Investigation. 2013.

Waldron T, Karakasheva T, Eruslanov E, Lee JS, Basu D, Malavasi F, Singhal S, Rustgi AK. CD38 enhances the immunosuppressive properties of myeloid-derived suppressor cells. Manuscript under review.


Adam Bass Publications:

Bass AJ, Watanabe H, Mermel CH, Yu S, Perner S, Verhaak RG, Kim SY, Wardwell L, Tamayo P, Gat-Viks I, Ramos AH, Woo MS, Weir BA, Getz G, Beroukhim R, O'Kelly M, Dutt A, Rozenblatt-Rosen O, Dziunycz P, Komisarof J, Chirieac LR, Lafargue CJ, Scheble V, Wilbertz T, Ma C, Rao S, Nakagawa H, Stairs DB, Lin L, Giordano TJ, Wagner P, Minna JD, Gazdar AF, Zhu CQ, Brose MS, Cecconello I, Jr UR, Marie SK, Dahl O, Shivdasani RA, Tsao MS, Rubin MA, Wong KK, Regev A, Hahn WC, Beer DG, Rustgi AK, Meyerson M.  SOX2 is an amplified lineage-survival oncogene in lung and esophageal squamous cell carcinomas. Nat Genet  2009; 41(11):1238-1242. [PMC2783775]

Watanabe H, Ma Q, Peng S, Adelmant G, Swain D, Song W, Fox C, Francis JM, Pedamallu CS, DeLuca DS, Brooks AN, Wang S, Que J, Rustgi AK, Wong KK, Ligon KL, Liu XS, Marto JA, Meyerson M, Bass AJ. SOX2-p63 interaction and genomic co-localization in squamous cell carcinomas. Under re-review in Journal of Clinical Investigation. 2013.


J. Alan Diehl Publications:

Rimerman RA, Gellert-Randleman A, Diehl JA.  Wnt1 and MEK1 cooperate to promote cyclin D1 accumulation and cellular transformation. J Biol Chem  2000; 275:14736-14742.  [pdf]

Alt JR, Cleveland JL, Hannink M, Diehl JA. Phosphorylation-dependent regulation of cyclin D1 nuclear export and cyclin D1-dependent cellular transformation. Genes & Dev  2000;  14:3102-3114.  [PMC317128]

Alt JR, Gladden AB, Diehl JA. p21(Cip1) promotes cyclin D1 nuclear accumulation via direct inhibition of nuclear export. J Biol Chem  2002;  277:8517-8523. [pdf]

Diehl JA, Yang W, Rimerman RA, Xiao H, Emili A. Hsc70 Regulates Accumulation of Cyclin D1 and the Cyclin D1-Dependent Protein Kinase. Mol Cell Biol  2003; 23:1764-1774. [PMC151693]

Gladden AB, Diehl JA. The Cyclin D1-dependent kinase associates with the pre-replication complex and modulates RB.MCM7 binding. J Biol Chem 2003; 278:9754-9760. [pdf]

Lu F, Gladden AB, Diehl JA. An alternatively spliced cyclin D1 isoform, cyclin D1b, is a nuclear oncogene. Cancer Research 2003; 63:7056-7061. [pdf]

Benzeno S, Lu F, Guo M, Barbash O, Zhang F, Herman JG, Klein PS, Rustgi AK, Diehl JA.  Identification of mutations that disrupt phosphorylation-dependent nuclear export of cyclin D1. Oncogene  2006; Oct 12: 25(47):  6291-6303.  [pdf]

Lin DI, Barbash O, Kumar KG, Weber JD, Harper JW, Klein-Szanto AJ, Rustgi AK, Fuchs Sy, Diehl JA. Phosphorylation-dependent ubiquitination of cyclin D1 by the SCF(FBX4-alphaB crystallin) complex.  Mol Cell 2006 Nov 3;24(3):355-366. [PMC1702390]

Barbash O, Lin DI, Diehl JA. SCF Fbx4/alphaB-crystallin cyclin D1 ubiquitin ligase: a license to destroy. Cell Div  2007; Jan 15;2:2. [PMC1790704]

Lin DI, Lessie MD, Gladden AB, Bassing CH, Wagner KU, Diehl JA. Disruption of cyclin D1 nuclear export and proteolysis accelerates mammary carcinogenesis. Oncogene  2008; 27:1231-1242. [PMC3733559]

Aggarwal P, Lessie M, Lin DI, Gladden AD, Nuskey B, Goradia A, Wasik M, Klein-Szanto A, Rustgi A, Bassing C, Diehl JA. Nuclear Accumulation of Cyclin D1 During S-phase Inhibits Cul4-dependent Cdt1 Proteolysis and Triggers p53-dependent DNA Re-replication. Genes & Dev  2007; 21: 2908-2922. [PMC2049193]

Barbash O, Zamfirova P, Lin DI, Chen LX, Yang K, Nakagawa H, Lu F, Rustgi AK, Diehl JA.  Mutations in Fbx4 inhibit phosphorylation-dependent dimerization of the SCF-Fbx4 ligase and contribute to cyclin D1overexpression in human cancer. Cancer Cell 2008; 14(1):68-78. [PMC2597358]

Barbash O, Diehl JA.  SCF(Fbx4/alpha beta-crystallin) E3 ligase: when one is not enough. Cell Cycle. 2008 Oct;7(19):2983-6. Epub 2008 Oct 12. [PMID: 18818515]

Lioni M, Noma K, Snyder A, Klein-Szanto A, Diehl JA, Rustgi AK, Herlyn M, Smalley KS. Bortezomib induces apoptosis in esophageal squamous cell carcinoma cells through activation of the p38 mitogen-activated protein kinase pathway.  Mol Cancer Ther. 2008 Sep;7(9):2866-75. [PMC2903039]

Harada H, Nakagawa H, Takaoka M, Lee J, Gimotty P, Herlyn M, Diehl JA, Rustgi AK.  Cleavage of MCM2 licensing proteins fosters senescence in human keratinocytes.  Cell Cycle 2008 Nov 15; 7(22):3534-3538. Epub 2008 Nov. 18. [PMC2736109]

Kalabis J, Oyama K, Okawa T, Nakagawa H, Michaylira CZ, Stairs DB, Figueiredo JL, Mahmood U, Diehl JA, Herlyn M, Rustgi AK. A subpopulation of mouse esophageal basal cells has properties of stem cells with the capacity for self-renewal and lineage specification. J Clin Invest 2008 Dec; 118(12):38360-3869. [PMC2579884]

Pontano LL, Aggarwal P, Babrbash O, Brown E, Bassing CH, Diehl JA. Genotoxic Stress-Induced Cyclin D1 Phosphorylation and Proteolysis Are Required for Genomic Stability. Mol Cell Biol 2008; 278: 7245-7258. [PMC2593367]

Barbash O, Egan E, Pontano LL, Kosak J, Diehl JA. Lysine 269 is essential for cyclin D1 ubiquitylation by the SCF Fbx4/aB-crystallin ligase and subsequent proteasome-dependent degradation. Oncogene 2009; 28:4317-4322. [PMC2794935]

Grugan K, Miller CG, Yao Y, Michaylira C, Ohashi S, Klein-Szanto AJ, Diehl JA, Herlyn M, Han M, Nakagawa H, Rustgi AK. Fibroblasts secreted hepatocyte growth factor is essential for esophageal squamous cell carcinoma invasion. Proceedings of the National Academy of Sciences. 2010; 107(24):11026-11031 [PMC2890722]

Michaylira C, Wong GS, Miller CG, Gutierrez CM, Nakagawa H, Hammond R, Klein-Szanto AJ, Lee JS, Herlyn M, Diehl JA, Gimotty P, Rustgi AK. Periostin, a cell adhesion molecule, facilitates invasion in the tumor microenvironment and annotes a novel tumor invasive signature in esophageal cancer. Cancer Research 2010; 70(13):5281-5292 [PMC3274349]

Ohasi S, Natsuizaka M, Wong G, Michaylira C, Grugan K, Stairs DB, Kalabis J, Vega ME, Kalman R, Nakagawa M, Klein-Szanto AJ, Herlyn M, Diehl JA, Rustgi AK, Nakagawa H.  EGFR and mutant p53 expand esophageal cellular subpopulation capable of epithelial-to-mesenchymal transition through ZEB transcription factors.  Cancer Research  2010; 116(23): 4948-4957.  [PMC3007622]

Natsuizaka M, Ohashi S, Wong G, Ahmadi A, Kalman R, Budo D, Klein-Szanto A, Herlyn M, Diehl JA, Nakagawa H. Insulin-like growth factor binding protein-3 promotes transforming growth factor-ß1-mediated epithelial-to-mesenchymal transition and motility in transformed human esophageal cells. Carcinogenesis  2010; 31(8): 1344-1353.  [PMC2915630]

Ohashi S, Natsuizaka M, Yashiro-Ohtani Y, Kalman RA, Nakagawa M, Wu L, Klein-Szanto AJ, Herlyn M, Diehl JA, Katz JP, Pear WS, Seykora JT, Nakagawa H. NOTCH1 and NOTCH3 coordinate esophageal squamous differentiation through a CSL-dependent transcriptional network. Gastroenterology 2010; 139(6): 2113-2123.  [PMC2997138]

Aggarwal P, Vaites LP, Kim JK, Mellert H, Nakagawa H, Herlyn M, Rustgi A, McMahon SB, Diehl JA. Nuclear Cyclin D1/CDK4 minase regulates CUL4 expression and triggers neoplastic growth via activation of the PRMT5 methyltransferase.  Cancer Cell  2010; 18(4): 329-340. [PMC295747]

Stairs DB, Bayne LJ, Rhoades B, Vega ME, Kalabis J, Klein-Szanto JA, Lee J-S, Katz JP, Diehl JA, Vonderheide RH, Reynolds AB, Rustgi AK.  Deletion of p120-catenin results in a tumor microenvironment with inflammation and cancer that establishes it as a bone fide tumor suppressor.  Cancer Cell  2011; 19(4): 470-483.  [PMC3077713]

Basu D, Nguyen T-T, Montone KT, Zhang G, Wang L-P, Diehl JA, Rustgi AK, Lee JT, Weinstein GS, Herlyn M. Evidence for mesenchymal sub-populations within squamous cell carcinomas exhibiting chemoresistance and phenotypic plasticity. Oncogene 2010; 29(29): 4170-4182.  [PMC3039880]

Barbash O, Lee EK, Diehl JA.  Phosphorylation-dependent regulation of SCF (Fbx4) dimerization and activity involves a novel component, 14-3-3ε.  Oncogene  2011, Jan 17.   (Epub ahead of print).  [PMC3084329]

Basu D, Montone KT, Wang LP, Gimotty PA, Hammond R, Diehl JA, Rustgi AK, Lee JT, Rasanen K, Weinstein GS, Herlyn M. Detecting and targeting mesenchymal-like subpopulations within squamous cell carcinomas. Cell Cycle. 2011; 10(12):2008-16.  [PMC3154419]

Ohashi S, Natsuizaka M, Naganuma S, Kagawa S, Kimura S, Itoh H, Kalman RA, Nakagawa M, Darling DS, Basu D, Gimotty PA, Klein-Szanto AJ, Diehl JA, Herlyn M, Nakagawa H. A NOTCH3-mediated squamous cell differentiation program limits expansion of EMT-competent cells that express the ZEB transcription factors.Cancer Res. 2011; 71(21):6836-47. Epub 2011 Sep 2. [PMC3206139]

Vaites LP, Lee EK, Lian Z, Barbash O, Roy D, Wasik M, Klein-Szanto AJ, Rustgi AK, Diehl JA. The Fbx4 tumor suppressor regulates cyclin D1 accumulation and prevents neoplastic transformation. Mol Cell Biol  2011; 31(22):4513-4523. Epub 2011 Sep 12. [PMC3209253]

Naganuma S, Whelan KA, Natsuizaka M, Kagawa S, Kinugasa H, Chang S, Subramanian H, Rhoades B, Ohashi S, Itoh H, Herlyn M, Diehl JA, Gimotty PA, Klein-Szanto AJ, Nakagawa H. Genetic Notch inhibition reveals cyclin D1 and Wnt signaling in invasive esophageal squamous cell carcinoma.  Am J Cancer Res  2012; 2(4):459-475.  [PMC3410579]

Basu D, Bewley AF, Sperry SM, Montone KT, Gimotty PA, Rasanen K, Facompre ND, Weinstein GS, Nakagawa H, Diehl JA, Rustgi AK, Herlyn M.  EGFR Inhibition Promotes an Aggressive Invasion Pattern Mediated by Mesenchymal-like Tumor Cells within Squamous Cell Carcinomas. Mol Cancer Ther. 2013 Oct;12(10):2176-86. [PMC3796003]


Phyllis Gimotty Publications:

Stairs D, Nakagawa H, Klein-Szanto A, Mitchell S, Silberg D, Gimotty P, Tobias J, Lynch J, Rustgi AK.  Cdx1 and c-myc Foster the Initiation of Transdifferentiation of the Normal Esophageal Squamous Epithelium towards Barrett’s Esophagus.  PLoS One  2008; 3(10):e3534. [PMC2568822]

Michaylira C, Wong GS, Miller CG, Gutierrez CM, Nakagawa H, Hammond R, Klein-Szanto AJ, Lee, J-S, Herlyn M, Diehl JA, Gimotty P, Rustgi AK.  Periostin, a cell adhesion molecule, facilitates invasion in the tumor microenvironment and annotates a novel tumor invasive signature in esophageal cancer.  Cancer Research  2010; 70(13):5281-5292.  [PMC3274349]

Ohashi S, Natsuizaka M, Naganuma S, Kagawa S, Kimura S, Itoh H, Kalman RA, Nakagawa M, Darling DS, Basu D, Gimotty PA, Klein-Szanto AJ, Diehl JA, Herlyn M, Nakagawa H. A NOTCH3-mediated squamous cell differentiation program limits expansion of EMT-competent cells that express the ZEB transcription factors. Cancer Res  2011; 71(21):6836-6847. Epub 2011 Sep 2. [PMC3206139]

Basu D, Montone KT, Wang LP, Gimotty PA, Hammond R, Diehl JA, Rustgi AK, Lee JT, Rasanen K, Weinstein GS, Herlyn M. Detecting and targeting mesenchymal-like subpopulations within squamous cell carcinomas. Cell Cycle  2011; 10(12):2008-2016.  [PMC3154419]

Naganuma S, Whelan KA, Natsuizaka M, Kagawa S, Kinugasa H, Chang S, Subramanian H, Rhoades B, Ohashi S, Itoh H, Herlyn M, Diehl JA, Gimotty PA, Klein-Szanto AJ, Nakagawa H. Genetic Notch inhibition reveals cyclin D1 and Wnt signaling in invasive esophageal squamous cell carcinoma.  Am J Cancer Res  2012; 2(4):459-475.  [PMC3410579]

Wong GS, Habibollahi P, Heidari P, Lee JS, Klein-Szanto AJ, Waldron TJ, Gimotty PA, Nakagawa H, Taylor PR, Wang TC, Mahmood U, Rustgi AK.  Optical imaging of periostin enables early endoscopic detection and characterization of esophageal cancer in mice. Gastroenterology. 2013 Feb;144(2):294-7. [PMC3624041]

Wong GS, Lee JS, Park YY, Klein-Szanto AJ, Waldron TJ, Cukierman E, Herlyn M, Gimotty PA, Nakagawa H, Rustgi AK. Periostin cooperates with mutant p53 to mediate invasion through the induction of STAT1 signaling in the esophageal tumor microenvironment.  Oncogenesis. 2013 Aug 5; 2:e59. [PMC3759121]

Basu D, Bewley AF, Sperry SM, Montone KT, Gimotty PA, Rasanen K, Facompre ND, Weinstein GS, Nakagawa H, Diehl JA, Rustgi AK, Herlyn M.  EGFR Inhibition Promotes an Aggressive Invasion Pattern Mediated by Mesenchymal-like Tumor Cells within Squamous Cell Carcinomas. Mol Cancer Ther. 2013 Oct;12(10):2176-86. [PMC3796003]


Meenhard Herlyn Publications:

Yang L, Dan HC, Sun M, Liu Q, Sun XM, Feldman RI, Hamilton AD, Polokoff M, Nicosia SV, Herlyn M, Sebti SM, Cheng JQ. Akt/protein kinase B signaling inhibitor-2, a selective small molecule inhibitor of Akt signaling with antitumor activity in cancer cells overexpressing Akt. Cancer Res  2004; 64:4394-4399. [pdf]

Gorgoulis VG, Vassiliou LV, Karakaidos P, Zacharatos P, Kotsinas A, Liloglou T, Venere M, Ditullio RA, Jr, Kastrinakis NG, Levy B, Kletsas D, Yoneta A, Herlyn M, Kittas C, Halazonetis TD. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature   2005; 434:907-913. [pdf]

Liu Z-J, Xiao M, Balint K, Soma A, Pinnix CC, Capobianco AJ, Herlyn M. Inhibiton of endothelial cells growth by Notch1 signaling is mediated by repressing MAPK and PI3K/Akt pathways and requirtes MAML1. FASEB J  2006; 20(7): 1009-1011. [pdf]

Lioni M, Brafford P, Andl A, Rustgi A, El-Deiry W, Herlyn M, Smalley KSM. Dysregulation of Claudin-7 leads to loss of E-cadherin expression and the increased invasion of esophageal squamous cell carcinoma cells. Am. J. Pathol.  2007; 170: 709-721. [PMC1851859]

Noma K, Smalley KS, Lioni M, Naomoto Y, Tankaka N, El-Deiry W, King AJ, Nakagawa H, Herlyn M.  The Essential Role of Fibroblasts in Esophageal Squamous Cell Carcinoma-Induced Angiogenesis.  Gastroenterology  2008; 134(7): 1981-1983. [PMC2562524]

Lioni M, Noma K, Snyder A, Klein-Szanto A, Diehl JA, Rustgi AK, Herlyn M, Smalley KS. Bortezomib-Induces Apoptosis in Esophageal Squamous Cell Carcionma Cells through Activation of the p38 MAPK Pathway.  Molecular Cancer Therapy  2008; 7(9); 2866-2875.  [PMC2903039]

Basu D, Herlyn M. Salmonella Typhimurium and a novel RNA interference vector for cancer gene therapy. Cancer Biol Therapy 2008; 1:151-152. [pdf]

Harada H, Nakagawa H, Takaoka M, Lee J, Gimotty P, Herlyn M, Diehl AJ, Rustgi AK.  Cleavage of MCM2 licensing proteins fosters senescence in human keratinocytes.  Cell Cycle 2008 Nov 15; 7(22):3534-3538. Epub 2008 Nov. 18 PMC: 2736109. [PMC2736109]

Kalabis J, Oyama K, Okawa T, Nakagawa H, Michaylira CZ, Stairs DB, Figueiredo JL, Mahmood U, Diehl JA, Herlyn M, Rustgi AK. A subpopulation of mouse esophageal basal cells has properties of stem cells with the capacity for self-renewal and lineage specification. J Clin Invest 2008 Dec; 118(12):38360-3869. [PMC2579884]

Basu D, Herlyn M. Defining microenvironments within mouse models that enhance tumor aggressiveness. Cancer Biol Ther 2009; 8(4) 380-381. PMID: 19182538 [pdf]

Kalabis J, Li G, Fukunaga-Kalabis M, Rustgi AK, Herlyn M. Endothelin-3 stimulates survival of goblet cells in organotypic cultures of fetal human colonic epithelium. Am J Physiol Gastrointest Liver Physiol 2009 Dec; 295(6):1182-1189. PMC:2604801. [PMC2604801]

Grugan K, Miller CG, Yao Y, Michaylira C, Ohashi S, Klein-Szanto AJ, Diehl JA, Herlyn M, Han M, Nakagawa H, Rustgi AK. Fibroblasts secreted hepatocyte growth factor is essential for esophageal squamous cell carcinoma invasion. Proceedings of the National Academy of Sciences. 2010; 107(24):11026-11031 [PMC2890722]

Michaylira C, Wong GS, Miller CG, Gutierrez CM, Nakagawa H, Hammond R, Klein-Szanto AJ, Lee JS, Herlyn M, Diehl JA, Gimotty P, Rustgi AK. Periostin, a cell adhesion molecule, facilitates invasion in the tumor microenvironment and annotes a novel tumor invasive signature in esophageal cancer. Cancer Research 2010; 70(13):5281-5292 [PMC3274349]

Ohasi S, Natsuizaka M, Wong G, Michaylira C, Grugan K, Stairs DB, Kalabis J, Vega ME, Kalman R, Nakagawa M, Klein-Szanto AJ, Herlyn M, Diehl JA, Rustgi AK, Nakagawa H.  EGFR and mutant p53 expand esophageal cellular subpopulation capable of epithelial-to-mesenchymal transition through ZEB transcription factors.  Cancer Research  2010; 116(23): 4948-4957.  [PMC3007622]

Natsuizaka M, Ohashi S, Wong G, Ahmadi A, Kalman R, Budo D, Klein-Szanto A, Herlyn M, Diehl JA, Nakagawa H. Insulin-like growth factor binding protein-3 promotes transforming growth factor-ß1-mediated epithelial-to-mesenchymal transition and motility in transformed human esophageal cells. Carcinogenesis  2010; 31(8): 1344-1353.  [PMC2915630]

Ohashi S, Natsuizaka M, Yashiro-Ohtani Y, Kalman RA, Nakagawa M, Wu L, Klein-Szanto AJ, Herlyn M, Diehl JA, Katz JP, Pear WS, Seykora JT, Nakagawa H. NOTCH1 and NOTCH3 coordinate esophageal squamous differentiation through a CSL-dependent transcriptional network. Gastroenterology 2010; 139(6): 2113-2123.  [PMC2997138]

Aggarwal P, Vaites LP, Kim JK, Mellert H, Nakagawa H, Herlyn M, Rustgi A, McMahon SB, Diehl JA. Nuclear Cyclin D1/CDK4 minase regulates CUL4 expression and triggers neoplastic growth via activation of the PRMT5 methyltransferase.  Cancer Cell  2010; 18(4): 329-340. [PMC295747]

Basu D, Nguyen T-T, Montone KT, Zhang G, Wang L-P, Diehl JA, Rustgi AK, Lee JT, Weinstein GS, Herlyn M. Evidence for mesenchymal sub-populations within squamous cell carcinomas exhibiting chemoresistance and phenotypic plasticity. Oncogene 2010; 29(29): 4170-4182.  [PMC3039880]

Kalabis J, Wong GS, Vega ME, Natsuizaka M, Robertson ES, Herlyn M, Nakagawa H, Rustgi AK. Isolation and characterization of mouse and human esophageal epithelial cells in 3D organotypic culture. Nat Protoc. 2012; 7(2):235-46. doi: 10.1038/nprot.2011.437. [PMC3505594]

Basu D, Montone KT, Wang LP, Gimotty PA, Hammond R, Diehl JA, Rustgi AK, Lee JT, Rasanen K, Weinstein GS, Herlyn M. Detecting and targeting mesenchymal-like subpopulations within squamous cell carcinomas. Cell Cycle. 2011; 10(12):2008-16. [PMC3154419]

Ohashi S, Natsuizaka M, Naganuma S, Kagawa S, Kimura S, Itoh H, Kalman RA, Nakagawa M, Darling DS, Basu D, Gimotty PA, Klein-Szanto AJ, Diehl JA, Herlyn M, Nakagawa H. A NOTCH3-mediated squamous cell differentiation program limits expansion of EMT-competent cells that express the ZEB transcription factors.Cancer Res. 2011; 71(21):6836-47. Epub 2011 Sep 2. [PMC3206139]

Facompre N, Nakagawa H, Herlyn M, Basu D. Stem-like cells and therapy resistance in squamous cell carcinomas. Advances in Pharmacology  2012; 65:235-265.  [PMC3595160]

Kalabis J, Wong GS, Vega ME, Natsuizaka M, Robertson ES, Herlyn M, Nakagawa H, Rustgi AK. Isolation and characterization of mouse and human esophageal epithelial cells in 3D organotypic culture. Nat Protoc  2012; 7:235-246. [PMC3505594]

Naganuma S, Whelan KA, Natsuizaka M, Kagawa S, Kinugasa H, Chang S, Subramanian H, Rhoades B, Ohashi S, Itoh H, Herlyn M, Diehl JA, Gimotty PA, Klein-Szanto AJ, Nakagawa H. Genetic Notch inhibition reveals cyclin D1 and Wnt signaling in invasive esophageal squamous cell carcinoma.  Am J Cancer Res  2012; 2(4):459-475.  [PMC3410579]

Wong GS, Lee JS, Park YY, Klein-Szanto AJ, Waldron TJ, Cukierman E, Herlyn M, Gimotty PA, Nakagawa H, Rustgi AK. Periostin cooperates with mutant p53 to mediate invasion through the induction of STAT1 signaling in the esophageal tumor microenvironment.  Oncogenesis. 2013 Aug 5; 2:e59. [PMC3759121]

Basu D, Bewley AF, Sperry SM, Montone KT, Gimotty PA, Rasanen K, Facompre ND, Weinstein GS, Nakagawa H, Diehl JA, Rustgi AK, Herlyn M.  EGFR Inhibition Promotes an Aggressive Invasion Pattern Mediated by Mesenchymal-like Tumor Cells within Squamous Cell Carcinomas. Mol Cancer Ther. 2013 Oct;12(10):2176-86. [PMC3796003]

Rasanen K, Sriswasdi S, Valiga A, Tang HY, Zhang G, Perego M, Somasundaram R, Li L, Speicher K, Klein-Szanto A, Basu D, Rustgi AK, Speicher DW, Herlyn M. Comparative secretome analysis of epithelial and mesenchymal subpopulations of head and neck squamous cell carcinoma identifies S100A4 as a potential therapeutic target. Mol Cell Proteomics. 2013 Dec;12(12):3778-92. [PMC3861723]


Jonathan Katz Publications:

Katz JP, Perreault N, Goldstein BG, McNally SR, Silberg DG, Furth EE, Kaestner KH.  Loss of Klf4 in mice causes altered proliferation and differentiation and precancerous changes in the adult stomach. Gastroenterology 2005: 128: 935-945. [pdf]

Yang Y, Goldstein BG, Chao H, Katz JP.  KLF4 and KLF5 regulate proliferation, apoptosis, and invasion in esophageal cancer cells.  Cancer Biology and Therapy 2005: 4: 1216-1221. [pdf]

Yang Y, Goldstein BG, Nakagawa H, Katz JPKrüppel-like factor 5 activates MEK/ERK signaling via EGFR in primary squamous epithelial cells.  FASEB Journal  2007; 21: 543-550. [pdf]

Goldstein BG, Chao H, Yang Y, Yermolina Y, Tobias JW, Katz JP.  Overexpression of Krüppel-like factor 5 in esophageal epithelia in vivo leads to increased proliferation in basal but not suprabasal cells.  Am J Physiol Gastrointest Liver Physiol  2007: 292: G1784-1792. [pdf]

Crissey MA, Guo RJ, Fogt F, Li H, Katz JP, Silberg DG, Suh ER, Lynch JP.  The homeodomain transcription factor Cdx1 does not behave as an oncogene in normal mouse intestine.  Neoplasia  2008; 10:8-19.  [PMC2213897]

Tetreault MP, Yang Y, Travis J, Yu QC, Klein-Szanto A, Tobias JW, Katz JP. Esophageal squamous cell dysplasia and delayed differentiation with deletion of krüppel-like factor 4 in murine esophagus. Gastroenterology. 2010 Jul;139(1):171-81. [PMC3265336]

Ohashi S, Natsuizaka M, Yashiro-Ohtani Y, Kalman RA, Nakagawa M, Wu L, Klein-Szanto AJ, Herlyn M, Diehl JA, Katz JP, Pear WS, Seykora JT, Nakagawa H. NOTCH1 and NOTCH3 coordinate esophageal squamous differentiation through a CSL-dependent transcriptional network. Gastroenterology 2010; 139(6): 2113-2123.  [PMC2997138]

Tetreault MP, Wang ML, Yang Y, Travis J, Yu QC, Klein-Szanto AJ, Katz JP. Klf4 overexpression activates epithelial cytokines and inflammation-mediated esophageal squamous cell cancer in mice. Gastroenterology. 2010 Dec;139(6):2124-2134. [PMC3457785]

Yang Y, Nakagawa H, Tetreault MP, Billig J, Victor N, Goyal A, Sepulveda AR, Katz JP. Loss of transcription factor KLF5 in the context of p53 ablation drives invasive progression of human squamous cell cancer. Cancer Res  2011; 71(20):6475-84. Epub 2011 Aug 25. [PMC3193554]

Stairs DB, Bayne LJ, Rhoades B, Vega ME, Kalabis J, Klein-Szanto JA, Lee J-S, Katz JP, Diehl JA, Vonderheide RH, Reynolds AB, Rustgi AK.  Deletion of p120-catenin results in a tumor microenvironment with inflammation and cancer that establishes it as a bone fide tumor suppressor.  Cancer Cell  2011; 19(4): 470-483.  [PMC3077713]

Yang Y, Nakagawa H, Tetreault MP, Billig J, Victor N, Goyal A, Sepulveda AR, Katz JP. Loss of transcription factor KLF5 in the context of p53 ablation drives invasive progression of human squamous cell cancer. Cancer Res. 2011 Oct 15;71(20):6475-84. [PMC3193554]

Yang Y, Tarapore RS, Jarmel MH, Tetreault MP, Katz JP.  p53 mutation alters the effect of the esophageal tumor suppressor KLF5 on keratinocyte proliferation.  Cell Cycle. 2012 Nov 1;11(21):4033-9. doi: 10.4161/cc.22265. Epub 2012 Sep 18. [PMC3507498]

Tetreault MP, Alrabaa R, McGeehan M, Katz JP.  Krüppel-like factor 5 protects against murine colitis and activates JAK-STAT signaling in vivo.  PLoS One. 2012;7(5):e38338. [PMC3364979]

Tarapore RS, Yang Y, Katz JP. Restoring KLF5 in esophageal squamous cell cancer cells activates the JNK pathway leading to apoptosis and reduced cell survival.  Neoplasia. 2013 May;15(5):472-80. [PMC3638350]


Andres Klein-Szanto Publications:

Liu SC, Bassi DE, Zhang SY, Holoran D, Conti CJ, Klein-Szanto AJP.  Overexpression of cyclin D2 is associated with increased in vivo invasiveness of human squamous carcinoma cells.  Mol Carcin  2002;  34: 131-139. [pdf]

Lopez de Cicco R, Bassie DE, Page RE, Klein-Szanto AJP.  Furin expression in squamous cell carcinomas of the oral cavity and other sites evaluated by tissue microarray technology.  Acta Odontol Latinoamer  2002; 15: 29-37.

Bassi DE, Mahloogi H, Lopez de Cicco R, Klein-Szanto AJP. Increased furin activity enhances the maligmant phenotype of human head and neck cancer cells.  Am J Pathol  2003; 162: 439-447.  [PMC1851171f]

Mahloogi H, González Guerrico AM, Lopez de Cicco R, Bassi DE, Goodrow T, Braunewell KH, Klein-Szanto AJP.  Overexpression of the calcium sensor visinin-like protein-1 leads to a cAMP-mediated decrease of in vivo and in vitro growth and invasiveness of squamous cell carcinoma cells.  Cancer Res 2003; 63: 4997-5004.  [pdf]

Lopez de Cicco R, Watson JC, Bassi DE, Litwin S, Klein-Szanto AJP.  Simultaneous expression of furin and vascular endothelial growth factor in human oral tongue squamous carcinoma progression.  Clin Cancer Res  2004; 10: 4480-4488. [pdf]

Takaoka M, Harada H, Andl CD, Oyama K, Naomoto Y, Dempsey K, Klein-Szanto AJP, El-Deiry W, Grimberg A, Nakagawa H.  Epidermal growth factor receptor regulates aberrant expression of insulin-like growth factor-binding protein 3.  Cancer Res  2004; 64: 7711-7723.  [pdf]

Gonzalez Guerrico AM, Jaffer ZM, Page RE, Braunewell KH, Chernoff J, Klein-Szanto AJP. Visinin-like protein-1 is a potent inhibitor of cell adhesion and migration in squamous carcinoma cells.  Oncogene 2005; 24: 2307-2316. [pdf]

Bassi DE, Lopez de Cicco R, Cenna J, Cukierman E, Klein-Szanto AJP.  PACE4 expression in mouse basal keratinocytes results in basement membrane disruption and acceleration of tumor progression. Cancer Res  2005; 65: 7310-7319.  [pdf]

Lopez de Cicco R, Bassi DE, Zucker S, Seidah NG, Klein-Szanto AJP.  Human squamous carcinoma cell growth and invasiveness is impaired by the propeptide of the ubiquitous proprotein convertase furin. Cancer Res  2005; 65: 7310-7319. [pdf]

Kim S, Nakagawa H, Navaraj A, Naomoto Y, Klein-Szanto AJP, Rustgi AK, El-Deiry WS. Tumorigenic conversion of primary human esophageal epithelial cells using oncogene combinations in the absence of exogenous Ras.  Cancer Res  2006; 66: 10415-10424. [pdf]

Lin DI, Barbash O, Kumar KG, Weber JD, Harper JW, Klein-Szanto AJP, Rustgi AK, Fuchs Sy, Diehl JA. Phosphorylation-dependent ubiquitination of cyclin D1 by the SCF(FBX4-alphaB crystallin) complex.  Mol Cell 2006 Nov 3;24(3):355-366. [PMC1702390]

Oyama K, Okawa T, Nakagawa H, Takaoka M, Andl CD, Kim S, Klein-Szanto AJP, Herlyn M, El-Deiry WS, Rustgi AK.  AKT induces senescence in primary esophageal epithelial cells but is permissive for differentiation as revealed in organotypic culture.  Oncogene  2007; 26:2353-2364.  [PMC2996093]

Takaoka M, Kim SH, Okawa T, Michaylira C, Andl CD, Stairs D, Johnstone C, Rhoades B, Mitchell S, Lee J, Dezfuli A, Klein-Szanto AJP, El-Deiry WS, Nakagawa H.  IGFBP-3 regulates esophageal tumor growth through IGF-dependent and independent mechanisms.  Cancer Bio Ther  2007; 6: 534-540. [PMC2996006]

Bassi DE, Klein-Szanto AJP.  Carcinogen induced animal models of head and neck squamous cell cancer.  Curr Prot Pharmacol  2007; 14:2. 

Okawa T, Michaylira C, Nakagawa H, Andl C, Stairs D, Johnstone C, Klein-Szanto AJP, El-Diery W, Cukierman E, Herlyn M, Rustgi AK.  The functional interplay between EGFR overexpression, hTERT activation and p53 mutation in esophageal epithelial cells with activation of stromal fibroblasts induce tumor development, invasion and differentiation.  Genes & Dev  2007; 21: 2788-2803.  [PMC2045132] 

Aggarwal P, Lessie M, Lin DI, Gladden AD, Nuskey B, Goradia A, Wasik M, Klein-Szanto AJP, Rustgi A, Bassing C, Diehl JA. Nuclear Accumulation of Cyclin D1 During S-phase Inhibits Cul4-dependent Cdt1 Proteolysis and Triggers p53-dependent DNA Re-replication. Genes & Dev  2007; 21: 2908-2922. [PMC2049193]

Stairs D, Nakagawa H, Klein-Szanto AJP, Mitchell S, Silberg D, Gimotty P, Tobias J, Lynch J, Rustgi AK.  Cdx1 and c-myc Foster the Initiation of Transdifferentiation of the Normal Esophageal Squamous Epithelium towards Barrett's Esophagus. PLoS Once 2008; 3(10):e3534. PMID: 18953412. [PMC2568822]

Lioni M, Noma K, Snyder A, Klein-Szanto A, Diehl JA, Rustgi AK, Herlyn M, Smalley KS. Bortezomib induces apoptosis in esophageal squamous cell carcinoma cells through activation of the p38 mitogen-activated protein kinase pathway.  Mol Cancer Ther. 2008 Sep;7(9):2866-75. [PMC2903039]

Grugan K, Miller CG, Yao Y, Michaylira C, Ohashi S, Klein-Szanto AJ, Diehl JA, Herlyn M, Han M, Nakagawa H, Rustgi AK. Fibroblasts secreted hepatocyte growth factor is essential for esophageal squamous cell carcinoma invasion. Proceedings of the National Academy of Sciences. 2010; 107(24):11026-11031 [PMC2890722]

Michaylira C, Wong GS, Miller CG, Gutierrez CM, Nakagawa H, Hammond R, Klein-Szanto AJ, Lee JS, Herlyn M, Diehl JA, Gimotty P, Rustgi AK. Periostin, a cell adhesion molecule, facilitates invasion in the tumor microenvironment and annotes a novel tumor invasive signature in esophageal cancer. Cancer Research 2010; 70(13):5281-5292 [PMC3274349]

Ohasi S, Natsuizaka M, Wong G, Michaylira C, Grugan K, Stairs DB, Kalabis J, Vega ME, Kalman R, Nakagawa M, Klein-Szanto AJ, Herlyn M, Diehl JA, Rustgi AK, Nakagawa H.  EGFR and mutant p53 expand esophageal cellular subpopulation capable of epithelial-to-mesenchymal transition through ZEB transcription factors.  Cancer Research  2010; 116(23): 4948-4957.  [PMC3007622]

Natsuizaka M, Ohashi S, Wong G, Ahmadi A, Kalman R, Budo D, Klein-Szanto A, Herlyn M, Diehl JA, Nakagawa H. Insulin-like growth factor binding protein-3 promotes transforming growth factor-ß1-mediated epithelial-to-mesenchymal transition and motility in transformed human esophageal cells. Carcinogenesis  2010; 31(8): 1344-1353.  [PMC2915630]

Ohashi S, Natsuizaka M, Yashiro-Ohtani Y, Kalman RA, Nakagawa M, Wu L, Klein-Szanto AJ, Herlyn M, Diehl JA, Katz JP, Pear WS, Seykora JT, Nakagawa H. NOTCH1 and NOTCH3 coordinate esophageal squamous differentiation through a CSL-dependent transcriptional network. Gastroenterology 2010; 139(6): 2113-2123.  [PMC2997138]

Stairs DB, Bayne LJ, Rhoades B, Vega ME, Kalabis J, Klein-Szanto JA, Lee J-S, Katz JP, Diehl JA, Vonderheide RH, Reynolds AB, Rustgi AK.  Deletion of p120-catenin results in a tumor microenvironment with inflammation and cancer that establishes it as a bone fide tumor suppressor.  Cancer Cell  2011; 19(4): 470-483.  [PMC3077713]

Vaites LP, Lee EK, Lian Z, Barbash O, Roy D, Wasik M, Klein-Szanto AJ, Rustgi AK, Diehl JA. The Fbx4 tumor suppressor regulates cyclin D1 accumulation and prevents neoplastic transformation.  Mol Cell Biol. 2011; 31(22):4513-23. Epub 2011 Sep 12. [PMC3209253]

Ohashi S, Natsuizaka M, Naganuma S, Kagawa S, Kimura S, Itoh H, Kalman RA, Nakagawa M, Darling DS, Basu D, Gimotty PA, Klein-Szanto AJ, Diehl JA, Herlyn M, Nakagawa H. A NOTCH3-mediated squamous cell differentiation program limits expansion of EMT-competent cells that express the ZEB transcription factors.Cancer Res. 2011; 71(21):6836-47. Epub 2011 Sep 2. [PMC3206139]

Watts JA, Zhang C, Klein-Szanto AJ, Kormish JD, Fu J, Zhang MK, Zaret KS.  Study of FoxA pioneer factor at silent genes reveals Rfx-repressed enhancer at Cdx2 and a potential indicator of esophageal adenocarcinoma development.  PLoS Genet  2011; 7:e1002277. [PMC3174211]

Natsuizaka M, Naganuma S, Kagawa S, Ohashi S, Ahmadi A, Subramanian H, Chang S, Nakagawa KJ, Ji X, Liebhaber SA, Klein-Szanto AJ, Nakagawa H. Hypoxia induces IGFBP3 in esophageal squamous cancer cells through HIF-1α-mediated mRNA transcription and continuous protein synthesis. FASEB J   2012; 26(6):2620-2630.  [PMC3360153]

Naganuma S, Whelan KA, Natsuizaka M, Kagawa S, Kinugasa H, Chang S, Subramanian H, Rhoades B, Ohashi S, Itoh H, Herlyn M, Diehl JA, Gimotty PA, Klein-Szanto AJ, Nakagawa H. Genetic Notch inhibition reveals cyclin D1 and Wnt signaling in invasive esophageal squamous cell carcinoma.  Am J Cancer Res  2012; 2(4):459-475.  [PMC3410579]

Wong GS, Habibollahi P, Heidari P, Lee JS, Klein-Szanto AJ, Waldron TJ, Gimotty PA, Nakagawa H, Taylor PR, Wang TC, Mahmood U, Rustgi AK.  Optical imaging of periostin enables early endoscopic detection and characterization of esophageal cancer in mice. Gastroenterology. 2013 Feb;144(2):294-7. [PMC3624041]

Wong GS, Lee JS, Park YY, Klein-Szanto AJ, Waldron TJ, Cukierman E, Herlyn M, Gimotty PA, Nakagawa H, Rustgi AK. Periostin cooperates with mutant p53 to mediate invasion through the induction of STAT1 signaling in the esophageal tumor microenvironment.  Oncogenesis. 2013 Aug 5; 2:e59. [PMC3759121]

Rasanen K, Sriswasdi S, Valiga A, Tang HY, Zhang G, Perego M, Somasundaram R, Li L, Speicher K, Klein-Szanto A, Basu D, Rustgi AK, Speicher DW, Herlyn M. Comparative secretome analysis of epithelial and mesenchymal subpopulations of head and neck squamous cell carcinoma identifies S100A4 as a potential therapeutic target. Mol Cell Proteomics. 2013 Dec;12(12):3778-92. [PMC3861723]


John Lynch Publications:

Xiao F, Crissey MS, Lynch JP, Silberg DG, Suh E.  Intestinal metaplasia with high-salt diet induces epithelial prolifertion and alters cell composition in the gastric mucosa of mice.  Cancer Bio Ther  2005; 4(6): 669-675. [pdf]

Stairs D, Nakagawa H, Klein-Szanto A, Mitchell S, Silberg D, Gimotty P, Tobias J, Lynch JP, Rustgi AK.  Cdx1 and c-myc Foster the Initiation of Transdifferentiation of the Normal Esophageal Squamous Epithelium towards Barrett's Esophagus. PLoS Once 2008; 3(10):e3534. [PMC2568822]

Kong J, Nakagawa H, Isariyawongse B, Funakoshi S, Silberg D, Rustgi AK, Lynch JP.  Induction of intestinalizatioin in human esophageal keratinocytes is a multi-step process. Carcinogenesis 2009 Jan; 30(1):122-30. [PMC2722140]

Kong J, Stairs DB, Lynch JP. Modelling Barrett's esophagus. Biochem Soc Trans. 2010; 38:3216. [pdf]

Guo RJ, Funakoshi S. Lee HH, Kong J, Lynch JP. The intestine-specific transcription factor Csx2 inhibits beta-catenin/TCF transcriptional activity by disrupting the beta-cantenin-TCF protein complex. Carcinogenisis 2010; 31(2):159-66. PMID: 19734199 [PMC2812568]

Stairs DB, Kong J, Lynch JP.  Cdx genes, inflammation and the pathogenesis of intestinal metaplasia.  Prog Mol Biol Transl Sci  2010;  96: 231-270.  [PMID: 21075347]

Huo X, Zhang HY, Zhang X, Lynch JP, Strauch ED, Wang JY, Melton SD, Genta RM, Wang DH, Spechler SJ, Souza RF. Acid and Bile Salt Induced CDX2 Expression Differs in Squamous Cells from Patients with and without Barrett's Esophagus. Gastroenterology  2010; 139(1): 194-203.  [PMC2902607]

Kong J, Crissey MA, Funakoshi S, Kreindler JL, Lynch JP.  Ectopic cdx2 expression in murine esophagus models and intermediate state in the emergence of Barrett’s Esophagus.  PLoS One  2011; 6(4): e18280. [PMC3071814]

Kong J, Crissey MA, Sepulveda AR, Lynch JP. Math1/Atoh1 contributes to intestinalization of esophageal keratinocytes by inducing the expression of Muc2 and Keratin-20. Dig Dis Sci. 2012; 57(4):845-57. Epub 2011 Dec 7. [PMC3407817]

Kong J, Crissey MA, Stairs DB, Sepulveda AR, Lynch JP. Cox2 and β-catenin/T-cell factor signaling intestinalize human esophageal keratinocytes when cultured under organotypic conditions. Neoplasia. 2011; 13(9):792-805. [PMC3182272]

Dvorak K, Goldman A, Kong J, Lynch JP, Hutchinson L, Houghton JM, Chen H, Chen X, Krishnadath KK, Westra WM. Molecular mechanisms of Barrett's esophagus and adenocarcinoma. Ann N Y Acad Sci. 2011 Sep; 1232:381-91. [PMID: 21950830]

Souza RF, Freschi G, Taddei A, Ringressi MN, Bechi P, Castiglione F, Rossi Degl'Innocenti D, Triadafilopoulos G, Wang JS, Chang AC, Barr H, Bajpai M, Das KM, Schneider PM, Krishnadath KK, Malhotra U, Lynch JP. Barrett's esophagus: genetic and cell changes. Ann N Y Acad Sci. 2011; 1232:18-35. [PMID: 21950805]


Hiroshi Nakagawa Publications:

Nakagawa H, Wang TC, Zukerberg L, Odze R, Togawa K, May GH, Wilson J, Rustgi AK.  The targeting of the cyclin D1 oncogene by an Epstein-Barr virus promoter in transgenic mice causes dysplasia in the tongue, esophagus and forestomach.  Oncogene  1997; 14: 1185-1190. [pdf]

Nakagawa H, Inomoto T, Rustgi AK.  A CACCC box-like cis-regulatory element of the Epstein-Barr virus ED-L2 promoter interacts with a novel transcriptional factor in tissue-specific squamous epithelia.  J Biol Chem  1997; 272: 16688-16699. [pdf]

Jenkins TD, Nakagawa H, Rustgi AK.  The keratinocyte specific Epstein-Barr virus ED-L2 promoter is regulated by phorbol 12-myristate 13-Acetate through two cis-regulatory elements containing e-box and Krüppel-like factor motifs. J Biol Chem 1997; 272: 24433-24442. [pdf]

Mueller A, Odze R, Jenkins TD, Shahsesfaei A, Nakagawa H, Inomoto T, Rustgi AK.  A transgenic mouse model with cyclin D1 overexpression results in cell cycle, epidermal growth factor receptor, and p53 abnormalities.  Cancer Res  1997; 57: 5542-5549. [pdf]

Yan YX, Nakagawa H, Lee MH, Rustgi AK.  Transforming growth factor-alpha enhances cyclin D1 transcription through the binding of early growth response protein to a cis-regulatory element in the cyclin D1 promoter.  J Biol Chem  1997; 272: 33181-33190. [pdf]

Compton C, Garland W, Nakagawa H, Opitz O, Rustgi AK.  Cellular characterization and successful transfection of serially subcultured normal human esophageal keratinocytes.  Journal of Cellular Physiology 1998; 177: 274-281. [pdf]

Okano J, Opitz OG, Nakagawa H, Jenkins TD, Friedman SL, Rustgi AK.  The Kruppel-like transcriptional factors Zf9 and GKLF coactivate the human keratin 4 promoter and physically interact.  FEBS Lett  2000; 473: 95-100.  [pdf]

Okano J, Gaslightwala I, Birnbaum MJ, Rustgi AK, Nakgawa H.  Akt/protein kinase B isoforms are differentially regulated by epidermal growth factor stimulation.  J Biol Chem  2000; 275: 30934-30942.  [pdf]

Mizushima T, Nakagawa H, Kamberov YG, Wilder EL, Klein PS, Rustgi AK.  Wnt-1 but not epidermal growth factor induces beta-catenin/T-cell factor-dependent transcription in esophageal cancer cells.  Cancer Res  2002; 62: 277-282. [pdf]

Opitz OG, Harada H, Suliman Y, Rhoades B, Sharpless NE, Kent R, Kopelovich L, Nakagawa H, Rustgi AK.  A mouse genetic model of human oral-esophageal cancer.  J. Clin Invest  2002; 110: 761-769. [PMC151126]

Andl CD, Mizushima T, Nakagawa H, Oyama K, Harada H, Chruma K, Herlyn M, Rustgi AK.  Epidermal growth factor receptor mediates increased cell proliferation, migration, and aggregation in esophageal keratinocytes in vitro and in vivo.  J Biol Chem  2003; 278(3): 1824-1830. [pdf]

Fong LY, Mancini R, Nakagawa H, Rustgi AK, Huebner K.  Combined cyclin D1 overexpression and zinc deficiency disrupts cell cycle and accelerates mouse forestomach carcinogenesis.  Cancer Res  2003; 63: 4244-4252. [pdf]

Harada H, Nakagawa H, Oyama K, Takaoka M, Andl CD, Jacobmeier B, von Werder A, Enders GH, Opitz OG, Rustgi AK.  Telomerase induces immortalization of human esophageal keratinocytes without p16INK4A inactivation.  Molecular Cancer Research  2003; 1: 729-738. [pdf]

Kim K, Nakagawa H, Fei P, Rustgi AK, El-Deiry WS.  Targeting Bcl-XL in esophageal squamous cancer to sensitize to chemotherapy plus TRAIL-induced apoptosis while normal epithelial cells are protected by blockade of caspase 9.  Cell Death Diff  2004; 11: 583-587. [pdf]

Takaoka M, Harada H, Deramaudt TB, Oyama K, Andl CD, Johnstone CN, Rhoades B, Opitz OG, Nakagawa H.  Ha-RasG12V induces senescence in primary and immortalized human esophageal keratinocytes with p53 dysfunction.  Oncogene  2004; 23: 6760-6768. [pdf]

Andl CD, Mizushima T, Oyama K, Nakagawa H, Rustgi AK.  EGFR induced cell migration is mediated predominantly by the JAK/Stat pathway in primary esophageal keratinocytes.  American Journal of Physiology - Gastrointestinal and Liver Physiology  2004; 287: G1227-1237. [pdf]

Takaoka M, Harada H, Andl CD, Oyama K, Naomoto Y, Dempsey K, Klein-Szanto AJ, El-Deiry WS, Grimberg A, Nakagawa H.  Epidermal growth factor receptor regulates aberrant expression of insulin-like growth factor binding protein-3.  Cancer Research  2004; 64: 7711-7723. [pdf]

Takaoka M, Smith CE, Mashiba MK, Okawa T, Andl CD, El-Deiry WS, Nakagawa H.  EGF-mediated regulation of insulin-like growth factor binding protein (IGFBP)-3 determines esophageal epithelial cellular response to IGF-I.  Am J Physiol - Gastrointestinal and Liver Physiology  2006; 290: G404-416.  [PMC2996094]

Kobayashi M, Naomoto Y, Nobuhisa T, Okawa T, Takaoka M, Shirakawa Y, Yamatsuji T, Matsuoka J., Mizushima T, Matsuura H, Nakajima M, Nakagawa H, Rustgi AK, Tanaka N.  Heparanase regulates esophageal keratinocyte differentiation through nuclear translocation and heparin sulfate cleavage. Differentiation  2006; 74(5): 235-243.  [pdf]

Andl CD , Fargnoli B, Okawa T, Bowser M, Takaoka M, Nakagawa H, Klein-Szanto A, Hua X, Herlyn M, Rustgi AK.  Coordinated functions of E-cadherin and TGFb receptor II in vitro and in vivo.  Cancer Research  2006; 66(20): 9878-9885.  [PMC2996096]

Kim SH, Nakagawa H, Navaraj A, Naomoto Y, Klein-Szanto A, Rustgi AK, El-Deiry WS.  Tumorigenic conversion of primary human esophageal epithelial cells using oncogene combinations in the absence of exogenous Ras.  Cancer Research  2006; 66: 10415-10424.  [pdf]

Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, Vassiliou LVF, Kolettas E, Niforou K, Zoumpourlis VC, Takaoka M, Nakagawa H, Tort F, Fugger K, Johansson F, Sehested M, Andersen CL, Dyrskjot L, Orntoft T, Lukas J, Kittas C, Helleday T, Halazonetis TD, Bartek J, Gorgoulis V.G.  Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints.  Nature  2006; 444: 633-637. [pdf]

Oyama K, Okawa T, Nakagawa H, Takaoka M, Andl CD, Kim SH, Klein-Szanto A, Diehl JA, Herlyn M, El-Deiry W, Rustgi AK.  AKT induces senescence in primary esophageal epithelial cells but is permissive for differentiation as revealed in organotypic culture.  Oncogene  2007; 26(16): 2353-2364. [PMC2996093]

Yang Y, Goldstein BG, Nakagawa H, Katz JP.  Krüppel-like factor 5 activates MEK/ERK signaling via EGFR in primary squamous epithelial cells.  FASEB J  2007; 21: 543-550. [pdf]

Takaoka M, Kim SH, Okawa T, Michaylira CZ, Stairs D, Johnstone CN, Andl CD, Rhoades B, Lee J, Klein-Szanto AJP, El-Deiry WS, Nakagawa H.  IGFBP-3 regulates esophageal tumor growth through IGF-dependent and independent mechanisms.  Cancer Biol Ther  2007; 6: 534-540.  [PMC2993006]

Okawa T, Michaylira CZ, Nakagawa H, Andl CD, Stairs DB, Johnstone CN, Klein-Szanto AJP, El-Deiry WS, Cukierman E, Herlyn M, Rustgi AK.  The functional interplay between EGFR overexpression, hTER activation and p53 mutation in esophageal epithelial cells with activation of stromal fibroblasts induce tumor development, invasion and differentiation.  Genes & Development  2007; 21: 2788-2083.  [PMC2045132]

Harada H, Nakagawa H, Takaoka M, Lee J, Gimotty P, Herlyn M, Diehl AJ, Rustgi AK.  Cleavage of MCM2 licensing proteins fosters senescence in human keratinocytes.  Cell Cycle 2008 Nov 15; 7(22):3534-3538. Epub 2008 Nov. 18 PMC: 2736109. [PMC2736109]

Barbash O, Zamfirova P, Lin DI, Chen LX, Yang K, Nakagawa H, Lu F, Rustgi AK, Diehl JA.  Mutations in Fbx4 inhibit phosphorylation-dependent dimerization of the SCF-Fbx4 ligase and contribute to cyclin D1overexpression in human cancer. Cancer Cell 2008; 14(1):68-78. PMC2597358 [PMC2597358]

Stairs D, Nakagawa H, Klein-Szanto A, Mitchell S, Silberg D, Gimotty P, Tobias J, Lynch J, Rustgi AK.  Cdx1 and c-myc Foster the Initiation of Transdifferentiation of the Normal Esophageal Squamous Epithelium towards Barrett's Esophagus. PLoS Once 2008; 3(10):e3534. PMID: 18953412. [PMC2568822]

Kalabis J, Oyama K, Okawa T, Nakagawa H, Michaylira CZ, Stairs DB, Figueiredo JL, Mahmood U, Diehl JA, Herlyn M, Rustgi AK. A subpopulation of mouse esophageal basal cells has properties of stem cells with the capacity for self-renewal and lineage specification. J Clin Invest 2008 Dec; 118(12):38360-3869. [PMC2579884]

Kong J, Nakagawa H, Isariyawongse B, Funakoshi S, Silberg D, Rustgi AK, Lynch JP.  Induction of intestinalizatioin in human esophageal keratinocytes is a multi-step process. Carcinogenesis 2009 Jan; 30(1):122-30. [PMC2722140]

Wilkey JF, Buchberger G, Saucier K, Patel SM, Eisenberg E, Nakawawa H, Michaylira CZ, Rustgi AK, Mallya SM. Cyclin D1 overexpression increases susceptibility to 4-nitroquinoline-1-oxide-induced dysplasia and neoplasia in murine squamous oral epithelium. Mol Carcinog 2009 Sep; 48(9):853-861. [PMC2736315]

Bass AJ, Watanabe H, Mermel CH, Yu S, Perner S, Verhaak RG, Kim Sy, Wardwell L, Tamayo P, Gat-Viks I, Ramos AH, Woo MS, Weir BA, Getz G, Beroukhim R, O'Kelly M, Dutt A, Rozenblatt-Rosen O, Dziunycz P, Komisarof J, Chirieac LR, Lafargue CJ, Scheble V, Wilbertz T, Ma C, Rao S, Nakagawa H, Stairs DB, Lin L, Giordano TJ, Wagner P, Minna JD, Gazdar AF, Zhu CQ, Brose MS, Cecconello I, Jr UR, Marie SK, Dahl O, Shivdasani RA, Tsao MS, Rubin MA, Wong KK, Regev A, Hahn WC, Beer DG, Rustgi AK, Meyerson M. SOX2 is an amplified lineage-survival oncogene in lung and esophageal squamous cell carcinomas. Nat Genet. 2009 Nov; 41(11):1238-42. [PMC2783775]

Grugan K, Miller CG, Yao Y, Michaylira C, Ohashi S, Klein-Szanto AJ, Diehl JA, Herlyn M, Han M, Nakagawa H, Rustgi AK. Fibroblasts secreted hepatocyte growth factor is essential for esophageal squamous cell carcinoma invasion. Proceedings of the National Academy of Sciences. 2010; 107(24):11026-11031 [PMC2890722]

Michaylira C, Wong GS, Miller CG, Gutierrez CM, Nakagawa H, Hammond R, Klein-Szanto AJ, Lee JS, Herlyn M, Diehl JA, Gimotty P, Rustgi AK. Periostin, a cell adhesion molecule, facilitates invasion in the tumor microenvironment and annotes a novel tumor invasive signature in esophageal cancer. Cancer Research 2010; 70(13):5281-5292 [PMC3274349]

Ohasi S, Natsuizaka M, Wong G, Michaylira C, Grugan K, Stairs DB, Kalabis J, Vega ME, Kalman R, Nakagawa M, Klein-Szanto AJ, Herlyn M, Diehl JA, Rustgi AK, Nakagawa H.  EGFR and mutant p53 expand esophageal cellular subpopulation capable of epithelial-to-mesenchymal transition through ZEB transcription factors.  Cancer Research  2010; 116(23): 4948-4957.  [PMC3007622]

Natsuizaka M, Ohashi S, Wong G, Ahmadi A, Kalman R, Budo D, Klein-Szanto A, Herlyn M, Diehl JA, Nakagawa H. Insulin-like growth factor binding protein-3 promotes transforming growth factor-ß1-mediated epithelial-to-mesenchymal transition and motility in transformed human esophageal cells. Carcinogenesis  2010; 31(8): 1344-1353.  [PMC2915630]

Ohashi S, Natsuizaka M, Yashiro-Ohtani Y, Kalman RA, Nakagawa M, Wu L, Klein-Szanto AJ, Herlyn M, Diehl JA, Katz JP, Pear WS, Seykora JT, Nakagawa H. NOTCH1 and NOTCH3 coordinate esophageal squamous differentiation through a CSL-dependent transcriptional network. Gastroenterology 2010; 139(6): 2113-2123.  [PMC2997138]

Aggarwal P, Vaites LP, Kim JK, Mellert H, Nakagawa H, Herlyn M, Rustgi A, McMahon SB, Diehl JA. Nuclear Cyclin D1/CDK4 minase regulates CUL4 expression and triggers neoplastic growth via activation of the PRMT5 methyltransferase.  Cancer Cell  2010; 18(4): 329-340. [PMC295747]

Kalabis J, Wong GS, Vega ME, Natsuizaka M, Robertson ES, Herlyn M, Nakagawa H, Rustgi AK. Isolation and characterization of mouse and human esophageal epithelial cells in 3D organotypic culture. Nat Protoc. 2012; 7(2):235-46. [PMC3505594]

Predina JD, Judy B, Aliperti LA, Fridlender ZG, Blouin A, Kapoor V, Laguna B, Nakagawa H, Rustgi AK, Aguilar L, Aguilar-Cordova E, Albelda SM, Singhal S. Neoadjuvant in situ gene-mediated cytotoxic immunotherapy improves postoperative outcomes in novel syngeneic esophageal carcinoma models.  Cancer Gene Ther. 2011; 18(12):871-83. doi: 10.1038/cgt.2011.56. Epub 2011 Aug 26. [PMC3215998]

Ohashi S, Natsuizaka M, Naganuma S, Kagawa S, Kimura S, Itoh H, Kalman RA, Nakagawa M, Darling DS, Basu D, Gimotty PA, Klein-Szanto AJ, Diehl JA, Herlyn M, Nakagawa H. A NOTCH3-mediated squamous cell differentiation program limits expansion of EMT-competent cells that express the ZEB transcription factors.Cancer Res. 2011; 71(21):6836-47. Epub 2011 Sep 2. [PMC3206139]

Ohashi S, Natsuizaka M, Nakagawa H. MMP7 and activation of IGF-1R: a new insight into anti-EGFR therapeutic resistance in metastatic colorectal cancer. Cancer Biol Ther. 2011; 11(2):184-7.  [PMID: 21099345]

Yang Y, Nakagawa H, Tetreault MP, Billig J, Victor N, Goyal A, Sepulveda AR, Katz JP. Loss of transcription factor KLF5 in the context of p53 ablation drives invasive progression of human squamous cell cancer. Cancer Res. 2011; 71(20):6475-84. Epub 2011 Aug 25. [PMC3193554]

Facompre N, Nakagawa H, Herlyn M, Basu D. Stem-like cells and therapy resistance in squamous cell carcinomas. Advances in Pharmacology  2012; 65:235-265.  [PMC3595160]

Natsuizaka M, Naganuma S, Kagawa S, Ohashi S, Ahmadi A, Subramanian H, Chang S, Nakagawa KJ, Ji X, Liebhaber SA, Klein-Szanto AJ, Nakagawa H. Hypoxia induces IGFBP3 in esophageal squamous cancer cells through HIF-1α-mediated mRNA transcription and continuous protein synthesis. FASEB J. 2012 Jun;26(6):2620-30. [PMC3360153]

Kalabis J, Wong GS, Vega ME, Natsuizaka M, Robertson ES, Herlyn M, Nakagawa H, Rustgi AK. Isolation and characterization of mouse and human esophageal epithelial cells in 3D organotypic culture. Nat Protoc  2012; 7:235-246.  [PMC3505594]

Naganuma S, Whelan KA, Natsuizaka M, Kagawa S, Kinugasa H, Chang S, Subramanian H, Rhoades B, Ohashi S, Itoh H, Herlyn M, Diehl JA, Gimotty PA, Klein-Szanto AJ, Nakagawa H. Genetic Notch inhibition reveals cyclin D1 and Wnt signaling in invasive esophageal squamous cell carcinoma.  Am J Cancer Res  2012; 2(4):459-475.  [PMC3410579]

Wong GS, Habibollahi P, Heidari P, Lee JS, Klein-Szanto AJ, Waldron TJ, Gimotty PA, Nakagawa H, Taylor PR, Wang TC, Mahmood U, Rustgi AK.  Optical imaging of periostin enables early endoscopic detection and characterization of esophageal cancer in mice. Gastroenterology. 2013 Feb;144(2):294-7. [PMC3624041]

Li, K, Jiang M,  Lu, Y, Chen H, Sun J,  Wu S, Ku WY, Nakagawa H, Kita Y, Natsugoe S, Peters JH, Rustgi AK, Onaitis MW, Kiernan A, Chen X, Que J: Sox2 Cooperates with Inflammation-Mediated Stat3 Activation in the Malignant Transformation of Foregut Basal Progenitor Cells. Cell Stem Cell 2013 Mar 7; 12(3):304-315. [PMC3594795]

Wong GS, Lee JS, Park YY, Klein-Szanto AJ, Waldron TJ, Cukierman E, Herlyn M, Gimotty PA, Nakagawa H, Rustgi AK. Periostin cooperates with mutant p53 to mediate invasion through the induction of STAT1 signaling in the esophageal tumor microenvironment.  Oncogenesis. 2013 Aug 5; 2:e59. [PMC3759121]

Basu D, Bewley AF, Sperry SM, Montone KT, Gimotty PA, Rasanen K, Facompre ND, Weinstein GS, Nakagawa H, Diehl JA, Rustgi AK, Herlyn M.  EGFR Inhibition Promotes an Aggressive Invasion Pattern Mediated by Mesenchymal-like Tumor Cells within Squamous Cell Carcinomas. Mol Cancer Ther. 2013 Oct;12(10):2176-86. [PMC3796003]


Kwok-Kin Wong Publications:

Bass AJ, Watanabe H, Mermel CH, Yu S, Perner S, Verhaak RG, Kim SY, Wardwell L, Tamayo P, Gat-Viks I, Ramos AH, Woo MS, Weir BA, Getz G, Beroukhim R, O'Kelly M, Dutt A, Rozenblatt-Rosen O, Dziunycz P, Komisarof J, Chirieac LR, Lafargue CJ, Scheble V, Wilbertz T, Ma C, Rao S, Nakagawa H, Stairs DB, Lin L, Giordano TJ, Wagner P, Minna JD, Gazdar AF, Zhu CQ, Brose MS, Cecconello I, Jr UR, Marie SK, Dahl O, Shivdasani RA, Tsao MS, Rubin MA, Wong KK, Regev A, Hahn WC, Beer DG, Rustgi AK, Meyerson M.  SOX2 is an amplified lineage-survival oncogene in lung and esophageal squamous cell carcinomas. Nat Genet  2009; 41(11):1238-1242. [PMC2783775]

Watanabe H, Ma Q, Peng S, Adelmant G, Swain D, Song W, Fox C, Francis JM, Pedamallu CS, DeLuca DS, Brooks AN, Wang S, Que J, Rustgi AK, Wong KK, Ligon KL, Liu XS, Marto JA, Meyerson M, Bass AJ. SOX2-p63 interaction and genomic co-localization in squamous cell carcinomas. Under re-review in Journal of Clinical Investigation. 2013.


Cyclin' to Cancer through Histone Methylation

Esophageal P01 Archive:
https://www-dev.bioinformatics.upenn.edu/p01/index.do

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University of Pennsylvania | Perelman School of Medicine