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Penn IMIG Publications Involving Microscopy


  • Mentlik, A.M, Sanborn, K.B., Holzbaur, E.L., Orange, J.S. Rapid lytic granule convergence to the MTOC in natural killer cells is dependent upon dynein but not cytolytic commitment. Mol. Biol. Cell. 2010 ePub May 5.
  • Banerjee PP, Orange JS. Quantitative measurement of F-actin accumulation at the NK cell immunological synapse J Immunol Methods. 2010. In Press.
  • Capraro BR, Yoon Y, Cho W, Baumgart T. Curvature sensing by the epsin N-terminal homology (ENTH) domain measured on cylindrical lipid membrane tethers. J Am Chem Soc. 2010;132(4):1200-1.
  • Heinrich M, Tian A, Esposito C, Baumgart T. Dynamic sorting of lipids and proteins by membrane curvature: a moving phase boundary problem. Proc Natl Acad Sci.  In Press.
  • Johnson S, Stinson B, Reminik J, Go M, Fang X, Baumgart T. Temperature dependent phase behavior and protein partitioning in giant plasma membrane vesicles. Biochim Biophys Acta Biomembr. In Press.
  • Sanborn KS, Rak G, Mentlik A, Banerjee PP, Orange JS. Analysis of the NK cell immunological synapse. Methods Mol. Biol. 2010;612:127-48.
  • Sonnenberg GF, Mangan PR, Bezman NA, Sekiguchi DR, Luning Prak ET, Maltzman JS, Jordan MS, Koretzky GA. Mislocalization of SLP-76 leads to aberrant inflammatory cytokine and autoantibody production. Blood. 2010;115:2186-95.


  • Baker RG, Hsu CJ, Lee D, Jordan MS, Maltzman JS, Hammer DA, Baumgart T, Koretzky GA. The adapter protein SLP-76 mediates “outside-in” integrin signaling and function in T cells. Mol Cell Biol. 2009;29(20):5578-89.
  • Barr VA, Bernot KM, Shaffer MH, Burkhardt JK, Samelson LE. Formation of STIM and Orai complexes: Puncta and Distal Caps. Immunol Rev. 2009;31:148-59.
  • Bezman NA, Baker RG, Lenox LE, Jordan MS, Koretzky GA. Cutting Edge: Rescue of preTCR but not mature TCR signaling in mice expressing membrane-targeted SLP-76. J Immunol. 2009;182:5183-7.
  • Carrizosa E. Gomez TS, Labno CM, Klos Dehring DA, Liu X, Freedman BD, Billadeau DD, Burkhardt JK. Hematopoietic lineage cell-specific protein1 is recruited to the immunological synapse by IL-2-inducible T cell kinase and regulates phospholipase C gamma-1 microcluster dynamics in T cell spreading. J Immunol. 2009;183:7352-61.
  • Christian D, Tian A, Ellenbroek W, Levental I, Rajagopal K, Janmey P, Liu A, Baumgart T, Discher D. Spotted vesicles, striped micelles and Janus assemblies induced by ligand binding. Nat Mater. 2009;8:843-9.
  • Das SL, Jenkins JT, Baumgart T. Neck geometry and shape transitions in vesicles with co-existing fluid phases: Role of Gaussian curvature stiffness versus spontaneous curvature. Europhys Lett. 2009;86:48003-8.
  • John B, Harris T, Tait E, Wilson EH, Ng L, Mrass P, Dzierszinski F, Weninger W, Hunter CA. Dynamic imaging of CD8+ T cells and dendritic cells during infection with Toxoplasma gondii. PLoS Pathog. 2009;5(7)e1000505. PMCID: PMC2700268.
  • Kambayashi T, Allenspach EJ, Chang JT, Zou T, Shoag JE, Reiner SL, Caton AJ, Koretzky GA. Inducible MHC class II expression by mast cells supports regulatory T cell expansion. J Immunol. 2009;182:4686-95.
  • King LB, Freedman BD. B cell calcium signaling In-Flux.  Immunol Rev. 2009; 231:265-77.
  • Lenox LE, Kambayashi T, Okumura M, Prieto C, Sauer K, Bunte RM, Jordan MS, Koretzky GA, Nichols KE. Mutation of tyrosine 145 of lymphocyte cytosolic protein 2 (Lcp2; SLP-76) protects mice from anaphylaxis and arthritis. J Allergy Clin Immunol. 2009;124:1088-98.
  • Levental I, Byfield FJ, Choudhourie P, Madara J, Gai F, Baumgart T, Janmey PA. Cholesterol-dependent phase separation in cell-derived giant plasma membrane vesicles. Biochem J. 2009;424(2):163-7.
  • Makedonas G, Banerjee PP, Pandey R, Hersperger AR, Sanborn KB, Hardy GAD, Orange JS, Betts MR. Rapid upregulation and granule-independent transport of perforin to the immunological synapse define a novel mechanism of antigen-specific CD8+ T cell cytotoxic activity. J Immunol. 2009;182:5560-9.
  • Oh H, Mohler III ER, Tian A, Baumgart T, Diamond SL. Membrane cholesterol is a biomechanical regulator of neutrophil adhesion. Arterioscler, Thromb, Vasc Biol. 2009;29:1290-7.
  • Ostrovsky O, Ahmed NT, Argon Y. The chaperone activity of GRP94 toward insulin-like growth factor II is necessary for the stress response to serum deprivation. Mol Biol Cell. 2009;20:1855-64.
  • Ostrovsky O, Makarewich CA, Snapp EL, Argon Y. An essential role for ATP binding and hydrolysis in the chaperone activity of GRP94 in cells.  Proc Nat Acad Sci. 2009;106:11600-5.
  • Ostrovsky O, Makarawich C, Snapp EL, Argon Y. Glucose regulated protein 94 is required for muscle differentiation through its control of the autocrine production of insulin-like growth factors. Biochim Biophys Acta, Mol Cell Res. 2009;1803:333-41.
  • Pien GC, Basner-Tschakarjan E, Hui DJ, Mentlik A, Finn JD, Hasbrouk NC, Zhou S, Murphy SL, Maus MV, Mingozzi F, Orange JS, High KA. Capsid antigen presentation flags hepatocytes for destruction after transduction by adeno-associated viral vectors. J Clin Invest. 2009;119:1688-95.
  • Sanborn KB, Rak G, Maru SY, Demers K, Difeo A, Martignetti JA, Betts MR, Favier R, Banerjee PP, Orange JS. Myosin IIA associates with NK cell lytic granules to enable their interaction with F-actin and function at the immunological synapse. J Immunol. 2009;182:6969-84.
  • Savic V, Sanborn KB, Orange JS, Bassing CH. Chipping away at g-H2AX Foci.  Cell Cycle. 2009;8:3285-90.
  • Shaffer MH, Dupree RS, Zhu P, Saotome I, Schmidt RF, McClatchey AI, Freedman BD, Burkhardt JK. Ezrin and moesin function together to promote T cell activation. J Immunol. 2009;182:1021-32.
    Tian A, Baumgart T. Sorting of lipids and proteins in membrane curvature gradients. Biophys J. 2009;96(7):2676-88.
  • Tian A, Capraro BR, Esposito C, Baumgart T. Bending stiffness depends on curvature of ternary lipid mixture tubular membranes. Biophys J. 2009;97(6):1636-1646.
  • Veler H, Hu A, Fatma S, Grunstein J, DeStephan CM, Campbell D, Orange JS, Grunstein MM.  Superantigen presentation by airway smooth muscle to CD4+ T lymphocytes elicits reciprocal pro-asthmatic changes in airway function. J Immunol. 2007;178:3672-6.
  • Wilson EH, Harris TH, Mrass P, John B, Tait ED, Wu GF, Pepper M, Wherry EJ, Dzierzinski F, Roos D, Haydon PG, Laufer TM, Weninger W, Hunter CA. Behavior of parasite-specific effector CD8+ T cells in the brain and visualization of a kinesis-associated system of reticular fibers. Immunity 2009;30:300-11. PMCID: PMC2696229.
  • Zhu P, Liu X, Treml LS, Cancro MP, Freedman BD. Mechanism and regulatory function of CpG signaling via scavenger receptor-B1 in primary B lymphocytes. J Biol Chem. 2009;284:22878-87.


  • Bezman NA, Lian L, Abrams CS, Brass LF, Kahn ML, Jordan MS, Koretzky GA. Requirements of SLP-76 tyrosines in ITAM and integrin receptor signaling and in platelet function in vivo.  J Exp Med. 2008;205:1775-88.
  • Chang JT, Reiner SL. Asymmetric division and stem cell renewal without a permanent niche: lessons from lymphocytes. Cold Spring Harb Symp Quant Biol. 2008;73:73-9.
  • Das SL, Tian A, Baumgart T. Mechanical stability of micropipette aspirated giant vesicles with fluid phase coexistence. J Phys Chem. 2008;112(37):11625-30.
  • Heinrich MC, Levental I, Gelman H, Janmey PA, Baumgart T. Critical exponents for line tension and dipole density difference from lipid monolayer domain boundary fluctuations. J Phys Chem. 2008;112(27):8063-8.
  • Huang Y, Comiskey EO, Dupree RS, Li S, Koleske AJ, Burkhardt JK. The c-Abl tyrosine kinase regulates actin remodeling at the immune synapse. Blood. 2008;112:111-9.
  • Kambayashi T, Baranski JD, Baker RG, Zou T, Allenspach EJ, Shoag JE, Jones PL, Koretzky GA. Indirect involvement of allergen-captured mast cells in antigen presentation. Blood. 2008;111:1489-96.
  • Maruvada R, Argon Y, Prasadarao NV. Microvascular endothelial cells induces STAT3 association with the C-terminal domain of Ec-gp96, the outer membrane protein A receptor for invasion. Cell Microbiol. 2008;10:2326-38.
  • Mrass P, Kinjyo I, Ng LG, Reiner SL, Pure E, Weninger W. CD44 mediates successful interstitial navigation by killer T cells and enables efficient antitumor immunity. Immunity. 2008;29:971-85.
  • Orange JS. Formation and function of the lytic NK cell immunological synapse.  Nat Rev Immunol. 2008;8:713-25.
    Pepper M, Dzierszinski F, Tait E, Wilson E, Yarovinsky F, Sher A, Roos DA, Hunter CA. A role for plasmacytoid dendritic cells as antigen presenting cells during infection with Toxoplasma gondii. J Immunol. 2008;180: 6229-36.
  • Perez EE, Wang J, Miller JC, Jouvenot YA, Kim KA, Liu O, Wang N, Lee G, Bartsevich VV, Lee Y-L, Guschin DY, Rupniewski I, Waite AJ, Carpenito C, Carroll RG, Orange JS, Urno FD, Reba, EJ, Ando D, Gregory PD, Riley JL, Holmes MC, June CH. Establishment of HIV-1 Resistance in CD4 T-cells by Genome Editing using Zinc Finger Nucleases. Nat Biotech. 2008;26:808-16.


  • Andzelm MM, Chen Z, Krzewski K, Orange JS, Strominger JL. Myosin IIA is required for cytolytic granule exocytosis in human NK cells. J Exp Med. 2007;204:2285-91.
  • Bach TL, Kerr WT, Wang Y, Bauman EM, Kine P, Whiteman EL, Morgan RS, Williamson EK, Ostap EM, Burkhardt JK, Koretzky GA, Birnbaum MJ, Abrams CS. PI3K regulates pleckstrin-2 in T-cell cytoskeletal re-organization. Blood. 2007;109:1147-55.
  • Banerjee PP, Pandey R, Zheng R, Suhoski M, Monaco-Shawver L, Orange JS. Cdc42-interacting protein-4 functionally links actin and microtubule networks at the cytolytic NK cell immunological synapse. J Exp Med. 2007;204:2305-20.
  • Biswas C, Ostrovsky O, Makarewich CA, Wanderling S, Gidalevitz T, Argon Y. The peptide binding activity of GRP94 is regulated by calcium. Biochem J. 2007;405:233-41.
  • Chang JT, Palanivel VR, Kinjyo I, Schambach F, Intlekofer AM, Banerjee A, Longworth SA, Vinup KE, Mrass P, Oliaro J, Killeen N, Orange JS, Russell SM, Weninger W, Reiner SL. Asymmetric T lymphocyte division initiating adaptive immunity. Science. 2007;315:1687-91.
  • Clemens RA, Lenox L, Kambayashi T, Bezman N, Maltzman JS, Nichols KE, Koretzky GA. Loss of SLP-76 expression within myeloid cells confers resistance to neutrophil-mediated tissue damage while maintaining effective bacterial killing. J Immunol. 2007;178:4606-14.
  • Dzierszinski F, Pepper M, Stumhofer JS, LaRosa DF, Wilson EH, Turka LA, Halonen SK, Hunter CA, Roos DS. Presentation of Toxoplasma gondii antigens via the endogenous major histocompatibility complex class I pathway in nonprofessional and professional antigen-presenting cells. Infect Immun. 2007;75:5200-9.
  • Esposito C, Tian A, Melamed S, Johnson C, Tee SY, Baumgart T. Flicker spectroscopy of thermal lipid bilayer domain boundary fluctuations. Biophys J. 2007;93(3):3169-81.
  • Hess S, Gudheti M, Mlodzianoski M, Baumgart T. Shape analysis of giant vesicles with fluid phase coexistence by laser scanning microscopy to determine curvature, bending elasticity and line tension. Methods Mol Biol. 2007;400:367-87.
  • Masek KS, Zhu P, Freedman BD, Hunter CA. Toxoplasma gondii induces changes in intracellular calcium in macrophages. Parasitology. 2007;134:1973-79.
  • Nolz JC, Medeiros RB, Mitchell JS, Zhu P, Freedman BD, Shimizu Y, Billadeau DD. WAVE2 regulates high-affinity integrin-binding by recruiting vinculin and talin to the Immunological Synapse. Mol Cell Biol. 2007;27:5986-6000.
  • Pandey R, Destephan CM, Madge LA, May MJ, Orange JS. NKp30 ligation induces rapid activation of the canonical NF-kB pathway in NK cells. J Immunol. 2007;179:7385-96.
  • Stumhofer JS, Silver JS, Laurence A, Porrett PM, Harris TH, Turka LA, Ernst M, Saris CJ, O'Shea JJ, Hunter CA. Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10. Nat Immunol. 2007;8:1363-71.
  • Tian A, Johnson C, Wang W, Baumgart T. Line tension at fluid membrane domain boundaries measured by micropipette aspiration. Phys Rev Lett. 2007;98(20):208102.
  • Villarino AV, Tato C, Stumhofer J, Yao Z, Cui YK, Hennighausen L, O’Shea JJ, Hunter CA. Helper T cell IL-2 production is limited by negative feedback and STAT-dependent cytokine signals. J Exp Med. 2007;204: 65-71.
  • Wanderling S, Simen BB, Ostrovsky O, Ahmed NT, Vogen SM, Gidalevitz T, Argon Y. GRP94 is essential for mesoderm induction and muscle development because it regulates IGF-II. Mol Biol Cell. 2007;18:3764-75.


  • Biswas C, Sriram U, Ciric B, Ostrovsky O, Gallucci S, Argon Y. The N-terminal fragment of GRP94 is sufficient for peptide presentation via professional APCs. Int Immunol. 2006;18:1147-57.
  • Eck S, Zhu P, Pepper M, Bensinger SJ, Freedman BD, Laufer TM. Developmental alterations in thymocyte sensitivity are actively regulated by MHC Class II expression in the thymic medulla. J Immunol. 2006;176:2229-37.
  • Freedman BD. Ca2+ signaling mechanisms and functions in lymphocytes. Critical Rev Immunol. 2006;26:97-111.
  • Gomez TS, McCarney SD, Carrizosa E, Labno CM, Comiskey EO, Nolz JC, Zhu P, Freedman BD, Clark MR, Rawlings DJ, Billadeau DD, Burkhardt JK. HS1 functions as an essential actin-regulatory adapter protein at the immune synapse. Immunity 2006;24:741-52.
  • Krezwski K, Chen X, Orange JS, Strominger JL. Formation of a WIP, WASp, actin and myosin IIA-containing multiprotein complex in activated NK cells and its alteration by KIR inhibitory signaling. J Cell Biol. 2006;173(1):121-32.
  • Liu X, Zhu P, Freedman BD. Multiple eicosanoid-activated non-selective cation channels regulate B cell adhesion to integrin ligands. Am J Physiol: Cell Physiology. 2006;290:C873-82.
  • Masek KS, Fiore J, Leitges M, Yan S, Freedman BD, Hunter CA. Host cell calcium and PKC regulate Toxoplasma gondii-induced mitogen-activated protein kinase signaling in macrophages. J Cell Sci. 2006;119:4565-73.
  • Nolz JC, Gomez TS, Zhu P, Li S, Medeiros RB, Shimizu Y, Burkhardt JK, Freedman BD, Billadeau DD. WAVE2 regulates actin cytoskeletal reorganization and CRAC-mediated calcium entry during T cell activation. Curr Biol. 2006;16:24-34.
  • Sebzda E, Hibbard C, Abtahian F, Bezman N, Clemens R, Sweeney S, Maltzman JS, Cheng L, Zhou D, Turner M, Tybulewicz B, Koretzky GA, and Kahn ML. Syk and SLP-76 mutant mice reveal a cell autonomous hematopoietic cell contribution to vascular development. Dev Cell. 2006;1:349-61.
  • Silverman MA, Shoag J, Wu J, Koretzky GA. Disruption of SLP-76 interaction with Gads inhibits dynamic clustering of SLP-76 and FceRI signaling in mast cells. Mol Cell Biol. 2006;26:1826-38.
  • Stumhofer JS, Laurence A, Wilson EH, Huang E, Tato CM, Johnson LM, Villarino AV, Huang Q, Yoshimura A, Sehy D, Saris CJ, O'Shea JJ, Hennighausen L, Ernst M, Hunter CA. Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat Immunol. 2006;7:937-45.
  • Wu JN, Gheith S, Bezman NA, Liu QH, Fostel LV, Swanson AM, Freedman BD, Koretzky GA, Peterson EG. Adhesion- and degranulation-promoting adapter protein is required for efficient thymocyte development and selection. J Immunol. 2006;176:6681-89.