Alumni

Stanley Adoro, PhD

Principal Investigator

Experimental Immunology Branch, National Cancer Institute

Education

BSc Biochemistry and MSc Cellular Parasitology, University of Ibadan, Nigeria

PhD Immunology, University of Pennsylvania, 2009 (Mentor: Dr. Alfred Singer, NCI)

Thesis

Stanley established that the genetic loci encoding CD4 and CD8 co-receptor proteins dictated T-cell lineage fate during T cell development in the thymus.

Publications From Graduate Work

• Adoro S, Park JH and Singer A. Coreceptor gene imprinting”: a genetic solution to a developmental dilemma in T cells. Cell Cycle 11:833-834. 2012.
• Adoro S, McCaughtry T, Erman B, Alag A, Van Laethem F, Park JH, Tai X, Kimura M, Wang L, Grinberg A, Kubo M, Bosselut R, Love P and Singer A. Coreceptor gene imprinting governs thymocyte lineage fate. EMBO Journal 31:366-377. 2012.
• Park JH, Adoro S, Guinter T, Erman B, Alag AS, Catalfamo M, Kimura MY, Cui Y, Lucas PJ, Gress RE, Kubo M, Hennighausen L, Feigenbaum L and Singer A. Signaling by intrathymic cytokines, not T cell antigen receptors, specifies CD8 lineage choice and promotes the differentiation of cytotoxic lineage T cells. Nature Immunology 11:257-264. 2010.
• Singer A, Adoro S and Park JH. Lineage fate and intense debate: myths, models and mechanisms of CD4/CD8 lineage choice. Nature Reviews Immunology 8:788-801. 2008.
• Adoro S, Erman B, Sarafova S, Van Laethem F, Park JH, Feigenbaum L and Singer A. Targeting CD4 coreceptor expression to post-selection thymocytes reveals that CD4/CD8 lineage choice is neither error-prone nor stochastic. Journal of Immunology 181:6975-6983. 2008.
• Park JH, Adoro S, Lucas PJ, Sarafova SD, Alag SA, Doan LL, Erman B, Liu X, Ellmeier W, Bosselut R, Feigenbaum L and Singer A. Coreceptor tuning’: cytokine signals transcriptionally tailor CD8 coreceptor expression in CD8 T cells to the self-specificity of their TCR. Nature Immunology 8:1049-1059. 2007.

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Michael Askenase, PhD

Senior Scientist II, Computational Biology, Flagship Pioneering

Education

BS Biology Tufts University, USA

PhD Immunology, University of Pennsylvania, 2015 (Mentor: Dr. Yasmine Belkaid, NIAID)

Thesis

Mike’s graduate work investigated how acute and chronic infection functionally educates monocyte development and results in the emergence of monocyte populations with enhanced regulatory functions.

Publications From Graduate Work

• Clever D, Roychoudhuri R, Constantinides MG, Askenase MH, Sukumar M, Klebanoff CA, Eil RL, Hickman HD, Yu Z, Pan JH, Palmer DC, Phan AT, Goulding J, Gattinoni L, Goldrath AW, Belkaid Y, Restifo NP. Oxygen Sensing by T Cells Establishes an Immunologically Tolerant Metastatic Niche. Cell. 166(5):1117-1131. 2016.
• Askenase MH, Han SJ, Byrd AL, Morais da Fonseca D, Bouladoux N, Wilhelm C, Konkel JE, Hand TW, Lacerda-Queiroz N, Su XZ, Trinchieri G, Grainger JR, Belkaid Y. Bone-Marrow Resident NK Cells Prime Monocytes for Regulatory Function during Infection. Immunity. 42(6):1130-42. 2015.
• Grainger JR, Askenase MH, Guimont-Desrochers F, da Fonseca DM, Belkaid Y. Contextual functions of antigen-presenting cells in the gastrointestinal tract. Immunol Rev. 259(1):75-87. 2014.
• Grainger JR, Wohlfert EA, Fuss IJ, Bouladoux N, Askenase MH, Legrand F, Koo LY, Brenchley JM, Fraser ID, Belkaid Y. Inflammatory monocytes regulate pathologic responses to commensals during acute gastrointestinal infection. Nat Med. 19(6):713-21. 2013.

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Tony Barnitz, PhD

Director, Manufacturing Sciences and Technologies, Adaptimmune

Education

BS Biology, Wake Forest University, USA

PhD Immunology, University of Pennsylvania, 2010 (Mentor: Dr. Michael Lenardo; NIAID)

Thesis

Tony examined the mechanism of HIV-1 induced cytopathicity of CD4⁺ T cells by investigating the role of HIV-1 Vpr protein in cell cycle arrest and cell death.

Publications From Graduate Work

• Barnitz RA, Chaigne-Delalande B, Bolton DL, Lenardo MJ. Exposed hydrophobic residues in human immunodeficiency virus type 1 Vpr helix-1 are important for cell cycle arrest and cell death. PLoS One. 6(9): e24924. 2011.
• Sakai K, Barnitz RA, Chaigne-Delalande B, Bidère N, Lenardo MJ. Human immunodeficiency virus type 1 Vif causes dysfunction of Cdk1 and CyclinB1: implications for cell cycle arrest. Virol J. 8:219. 2011.
• Barnitz RA, Wan F, Tripuraneni V, Bolton DL, Lenardo MJ. Protein kinase A phosphorylation activates Vpr-induced cell cycle arrest during human immunodeficiency virus type 1 infection. J Virol. 84(13):6410-24. 2010.
• Bolton DL, Barnitz RA, Sakai K, Lenardo MJ. 14-3-3 theta binding to cell cycle regulatory factors is enhanced by HIV-1 Vpr. Biol Direct. 3:17. 2008.
• Wan F, Anderson DE, Barnitz RA, Snow A, Bidere N, Zheng L, Hegde V, Lam LT, Staudt LM, Levens D, Deutsch WA, Lenardo MJ. Ribosomal protein S3: a KH domain subunit in NF-kappaB complexes that mediates selective gene regulation. Cell. 131(5):927-939.  2007.

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Laura Chopp, PhD

MD Student, University of Michigan Medicinal School

Education

MD Student, University of Michigan Medicinal School

PhD Immunology, University of Pennsylvania (Advisor: Rémy Bosselut, MD, PhD), 2022

BS Biomedical Sciences, Minnesota State University, Mankato, 2015

Thesis

Integration of single cell transcriptomics and epigenomics to identify new regulators of T cell development and function

Publications from Graduate Work

• Chopp LB, Zhu X, Gao Y, Nie J, Singh J, Kumar P, Young KZ, Patel S, Li C, Balmaceno-Criss M, Vacchio MS, Wang MM, Livak F, Merchant JL, Wang L, Kelly MC, Zhu J, Bosselut R. Zfp281 and Zfp148 control CD4⁺ T cell thymic development and T_H2 functions. Science Immunology 2023 8(89):eadi9066. doi: 10.1126/sciimmunol.adi9066
• Gao Y, Wang Y, Chauss D, Villarino AV, Link VM, Nagashima H, Spinner CA, Koparde VN, Bouladoux N, Abers MS, Break TJ, Chopp LB, Park JH, Zhu J, Wiest DL, Leonard WJ, Lionakis MS, O'Shea JJ, Afzali B, Belkaid Y, Lazarevic V. Transcription factor EGR2 controls homing and pathogenicity of TH17 cells in the central nervous system. Nature Immunology 2023 8:1331-1344. doi: 10.1038/s41590-023-01553-7.
• Georgiev H, Chopp LB, Hogquist KA. Ultrasound-guided intra-thymic cell injection. Methods Mol Biol. 2023 2580:283-292. doi: 10.1007/978-1-0716-2740-2_17
• Carpenter AC, Chopp LB, Kim JK, Bosselut R. Purification of thymocyte and T cell subsets. Methods Mol Biol. 2023 2580:151-163. doi: 10.1007/978-1-0716-2740-2_8
• Gao Y, Zamisch M, Vacchio M, Chopp LB, Ciucci T, Paine EL, Lyons GC, Nie J, Xiao Q, Zvezdova E, Love PE, Vinson CR, Jenkins LM, Bosselut R. NuRD complex recruitment to Thpok mediates CD4+ T cell lineage differentiation. Science Immunology 2022, 7(72):eabn5917. doi: 10.1126/sciimmunol.abn5917.
• Nie J, Carpenter AC, Chopp LB, Chen T, Balmaceno-Criss M, Ciucci T, Xiao Q, Kelly MC, McGavern DB, Belkaid Y, Bosselut R. The transcription factor LRF promotes integrin β7 expression by and gut homing of CD8αα⁺ intraepithelial lymphocyte precursors. Nature Immunology 2022 23(4):594-604. doi: 10.1038/s41590-022-01161-x.
• Ciucci T, Vacchio MS, Chen T, Nie J, Chopp LB, McGavern DB, Kelly MC, Bosselut R. Dependence on Bcl6 and Blimp1 drive distinct differentiation of murine memory and follicular helper CD4+ T cells. Journal of Experimental Medicine 2022 219(1):e20202343. doi: 10.1084/jem.20202343.
• Stamos DB, Clubb LM, Mitra A, Chopp LB, Nie J, Ding Y, Das A, Venkataganesh H, Lee J, El-Khoury D, Li L, Bhandoola A, Bosselut R, Love PE. The histone demethylase Lsd1 regulates multiple repressive gene programs during T cell development. Journal of Experimental Medicine 2021 218(12):e20202012. doi: 10.1084/jem.20202012.
• Chopp LB, Gopalan V, Ciucci T, Ruchinskas A, Rae Z, Lagarde M, Gao Y, Li C, Bosticardo M, Pala F, Livak F, Kelly MC, Hannenhalli S, Bosselut R. An Integrated Epigenomic and Transcriptomic Map of Mouse and Human αβ T Cell Development. Immunity 2020 53(6):1182-1201.e8. doi: 10.1016/j.immuni.2020.10.024.
• Amir M, Chaudhari S, Wang R, Campbell S, Mosure SA, Chopp LB, Lu Q, Shang J, Pelletier OB, He Y, Doebelin C, Cameron MD, Kojetin DJ, Kamenecka TM, Solt LA. REV-ERBα Regulates Th17 Cell Development and Autoimmunity. Cell Reports 2018 25(13):3733-3749.e8. doi: 10.1016/j.celrep.2018.11.101.
• Carpenter AC, Wohlfert E, Chopp LB, Vacchio MS, Nie J, Zhao Y, Shetty J, Xiao Q, Deng C, Tran B, Cam M, Gaida MM, Belkaid Y, Bosselut R. Control of Regulatory T Cell Differentiation by the Transcription Factors Thpok and LRF. Journal of Immunology 2017 199(5):1716-1728. doi: 10.4049/jimmunol.1700181.
• Reed BK^*, Chopp LB^*, Malo CS, Renner DN, Van Keulen VS, Girtman MA, Nevala WN, Pavelko KD, Gil D, Schrum AG, Johnson AJ, Pease LR. A Versatile Simple Capture Assay for Assessing the Structural Integrity of MHC Multimer Reagents. PLoS One 2015 10(9):e0137984. doi: 10.1371/journal.pone.0137984.

Jason Hall, PhD

Associate Director, Cell Therapy, Oncology Discovery, AbbVie

Education

BS Chemical Engineering, Northwestern University, USA

PhD Immunology, University of Pennsylvania, 2010 (Mentor: Dr. Yasmine Belkaid, NIAID)

Thesis

Jason’s graduate work centered on the role of microbial signaling and vitamin A metabolism in mucosal homeostasis and immunity.

Publications From Graduate Work

• Spencer SP, Wilhelm C, Yang Q, Hall JA, Bouladoux N, Boyd A, Nutman TB, Urban JF Jr, Wang J, Ramalingam TR, Bhandoola A, Wynn TA, Belkaid Y. Adaptation of innate lymphoid cells to a micronutrient deficiency promotes type 2 barrier immunity. Science. 343(6169):432-7. 2014.
• Klebanoff CA, Spencer SP, Torabi-Parizi P, Grainger JR, Roychoudhuri R, Ji Y, Sukumar M, Muranski P, Scott CD, Hall JA, Ferreyra GA, Leonardi AJ, Borman ZA, Wang J, Palmer DC, Wilhelm C, Cai R, Sun J, Napoli JL, Danner RL, Gattinoni L, Belkaid Y, Restifo NP. Retinoic acid controls the homeostasis of pre-cDC-derived splenic and intestinal dendritic cells. J Exp Med. 210(10): 1961–1976. 2013.
• Bouladoux N, Hall JA., Grainger J.R., dos Santos L., Kann M.G., Nagarajan V., Verthelyi D, Belkaid Y. Regulatory role of suppressive motifs from commensal DNA. Mucosal Immunol. 5:623:34. 2012.
• Naik S, Bouladoux N, Wilhelm C, Molloy MJ, Salcedo R, Kastenmuller W, Deming C, Quinones M, Koo L, Conlan S, Spencer S, Hall JA, Dzutsev A, Kong H, Campbell DJ, Trinchieri G, Segre JA, Belkaid Y. Compartmentalized control of skin immunity by resident commensals. Science. 2012.
• Hall JA, Grainger J, Dos Santos L, Naik S, Wohlfert E, Oldenhove G, Hand T, Robinson M, Chou M, Kastenmayer R, Belkaid Y. Essential role for retinoic acid in the promotion of CD4+ T cell effector responses via retinoic acid receptor alpha. Immunity. 34:435-47.  2011.
• Hall, JA, Granger J, Spencer S, Belkaid Y. Roles of Retinoic acid in Immunity and Tolerance. Immunity. 35:13-22.  2011.
• Wohlfert EA, Oldenhove G, Hager Ribeiro C, Hall JA, Yagi R, Grainger J, Paul WE, Bosselut R, Wei G, Zhao K, Zhu J, Belkaid Y. GATA3 controls Foxp3+ regulatory T cells plasticity in mice. JCI. 121:4503-15. 2011.
•  DePaolo RW, Abadie, V, Tang F, Hall JA, Wang W, Marietta EV, Murray JA, Belkaid Y, Jabri B. Co-adjuvant effects of retinoic acid and IL-15 induce inflammatory immunity to dietary antigens. Nature. 471:220-4. 2011.

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Timothy Johnston, PhD

Postdoctoral Researcher, NIH/NIAID Vaccine Research Center

Education

BS in Biology, University of Minnesota

PhD Immunology, University of Pennsylvania, 2026 (Mentor: Dr. Daniel Douek, Vaccine Research Center, NIAID)

Thesis

Tim is interested in studying how initial exposures to SARS-CoV-2 shape humoral responses to future exposures to mutated variants of the virus. He hopes to use insights from single cell sequencing of B cells and monoclonal antibody production to improve vaccine design.

Publications from Graduate Work

• Johnston, T.S., Li, S.H., Painter, M.M., Atkinson, R.K., Douek, N.R., Reeg, D.B., Douek, D.C., Wherry, E.J., Hensley, S.E. Immunological imprinting shapes the specificity of human antibody responses against SARS-CoV-2 variants. Immunity 2024 57:912-925 https://doi.org/10.1016/j.immuni.2024.02.017
• Matassoli, F., Cagigi, A., Shen, C.-H., Henry, A.R., Johnston, T.S., Schramm, C.A., Cottrell, C.A., Kalyuzhniy, O., Spangler, A., Ndung’u, T., Dong, K., Eller, L., Robb, M., Eller, M., Naluyima, P., Kwong, P.D., Douek, D.C., Schief, W.R., Andrews, S.F., McDermott, A.B. High frequency of HIV precursor-target-specific B cells in sub-Saharan populations. Cell Reports 2023 42:113450. https://doi.org/10.1016/j.celrep.2023.113450
• Painter, M.M., Johnston, T.S., Lundgreen, K.A., Santos, J.J.S., Qin, J.S., Goel, R.R., Apostolidis, S.A., Mathew, D., Fulmer, B., Williams, J.C., McKeague, M.L., Pattekar, A., Goode, A., Nasta, S., Baxter, A.E., Giles, J.R., Skelly, A.N., Felley, L.E., McLaughlin, M., Weaver, J., Kuthuru, O., Dougherty, J., Adamski, S., Long, S., Kee, M., Clendenin, C., da Silva Antunes, R., Grifoni, A., Weiskopf, D., Sette, A., Huang, A.C., Rader, D.J., Hensley, S.E., Bates, P., Greenplate, A.R., Wherry, E.J. Prior vaccination promotes early activation of memory T cells and enhances immune responses during SARS-CoV-2 breakthrough infection. Nature Immunology 2023 24:1711–1724. https://doi.org/10.1038/s41590-023-01613-y
• Wang, S., Matassoli, F., Zhang, B., Liu, T., Shen, C.-H., Bylund, T., Johnston, T.S., Henry, A.R., Teng, I.-T., Tripathi, P., Becker, J.E., Changela, A., Chaudhary, R., Cheng, C., Gaudinski, M., Gorman, J., Harris, D.R., Lee, M., Morano, N.C., Novik, L., O’Dell, S., Olia, A.S., Parchment, D.K., Rawi, R., Roberts-Torres, J., Stephens, T., Tsybovsky, Y., Wang, D., Van Wazer, D.J., Zhou, T., Doria-Rose, N.A., Koup, R.A., Shapiro, L., Douek, D.C., McDermott, A.B., Kwong, P.D. HIV-1 neutralizing antibodies elicited in humans by a prefusion-stabilized envelope trimer form a reproducible class targeting fusion peptide. Cell Reports 2023 42:112755 https://doi.org/10.1016/j.celrep.2023.11275
• Yogev, O., Weissbrod, O., Battistoni, G., Bressan, D., Naamati, A., Falciatori, I., Berkyurek, A.C., Rasnic, R., Izuagbe, R., Hosmillo, M., Ilan, S., Grossman, I., McCormick, L., Honeycutt, C.C., Johnston, T.S., Gagne, M., Douek, D.C., Goodfellow, I., Hannon, G.J., Erlich, Y. From a genome-wide screen of RNAi molecules against SARS-CoV-2 to a validated broad-spectrum and potent prophylaxis. Communications Biology 2023 6:1–12. https://doi.org/10.1038/s42003-023-04589-5

Ian Lamborn, MD, PhD

Clinical Fellow, Medicine, Yale University

Education

BS Chemistry and Molecular Biology, Grove City College, Grove City, PA, USA

MD, PhD Immunology, University of Pennsylvania, 2016 (Mentor: Dr. Helen Su, NIAID)

Thesis

Ian studied genetic determinants of host immunity against human rhinovirus infections. Specifically, he found that children with inherited MDA5 gene deficiency have recurrent rhinovirus infections.

Publications From Graduate Work

• Lamborn IT, Su HC. Genetic determinants of host immunity against human rhinovirus infections. Hum Genet. 2020
• Lamborn IT, Jing H, Zhang Y, Drutman SB, Abbott JK, Munir S, Bade S, Murdock HM, Santos CP, Brock LG, Masutani E, Fordjour EY, McElwee JJ, Hughes JD, Nichols DP, Belkaid A, Oler AJ, Happel CS, Matthews HF, Abel L, Collins PL, Subbarao K, Gelfand EW, Ciancanelli MJ, Casanova JL, Su HC. Recurrent rhinovirus infections in a child with inherited MDA5 deficiency. J Exp Med. 214(7):1949-1972. 2017
• Zhang Y, Yu X, Ichikawa M, Lyons JJ, Datta S, Lamborn IT, Jing H, Kim ES, Biancalana M, Wolfe LA, DiMaggio T, Matthews HF, Kranick SM, Stone KD, Holland SM, Reich DS, Hughes JD, Mehmet H, McElwee J, Freeman AF, Freeze HH, Su HC, Milner JD. Autosomal recessive phosphoglucomutase 3 (PGM3) mutations link glycosylation defects to atopy, immune deficiency, autoimmunity, and neurocognitive impairment. J Allergy Clin Immunol. 133(5):1400-9. 2014.
• Xu J, Hopkins K, Sabin L, Yasunaga A, Subramanian H, Lamborn I, Gordesky-Gold B, Cherry S. ERK signaling couples nutrient status to antiviral defense in the insect gut. Proc Natl Acad Sci U S A. 110(37):15025-30. 2013.
• Snow AL, Xiao W, Stinson JR, Lu W, Chaigne-Delalande B, Zheng L, Pittaluga S,  Matthews HF, Schmitz R, Jhavar S, Kuchen S, Kardava L, Wang W, Lamborn IT, Jing H, Raffeld M, Moir S, Fleisher TA, Staudt LM, Su HC, Lenardo MJ. Congenital B cell lymphocytosis explained by novel germline CARD11 mutations. J Exp Med. 209(12):2247-61. 2012.
• Sawamukai N, Satake A, Schmidt AM, Lamborn IT, Ojha P, Tanaka Y, Kambayashi T. Cell-autonomous role of TGFβ and IL-2 receptors in CD4+ and CD8+ inducible regulatory T-cell generation during GVHD. Blood. 119(23):5575-83.  2012.  
•  Zhang Q, Davis JC, Lamborn IT, Freeman AF, Jing H, Favreau AJ, Matthews HF, Davis J, Turner ML, Uzel G, Holland SM, Su HC. Combined immunodeficiency associated with DOCK8 mutations. N Engl J Med. 361(21):2046-55. 2009.

Michael Leney-Greene, PhD

Investigator, AI Proteins

Education

BS, Microbiology & Immunology, McGill University, Montreal, Quebec, Canada

PhD Immunology, University of Pennsylvania, 2019 (Mentors: Drs. Helen Su and Michael Lenardo, NIAID)

Thesis

Alex studied genetic susceptibility to autoimmunity. He identified that mutations in Gimap5, a small GTPase expressed in T, NK and endothelial cells, were responsible for a novel recessive Mendelian disease of immune dysregulation, characterized by severe lymphopenia, splenomegaly, thrombocytopenia and liver failure.

Publications From Graduate Work

• Leney-Greene MA, Boddapati AK, Su HC, Cantor JR, Lenardo MJ. Human Plasma-like Medium Improves T Lymphocyte Activation. iScience. 23(1):100759. 2020.
• Liu Y, Gordesky-Gold B, Leney-Greene M, Weinbren NL, Tudor M, Cherry S. Inflammation-Induced, STING-Dependent Autophagy Restricts Zika Virus Infection in the Drosophila Brain. Cell Host Microbe. 24(1):57-68.e3. 2018.
• Dupont CD, Christian DA, Selleck EM, Pepper M, Leney-Greene M, Harms Pritchard G, Koshy AA, Wagage S, Reuter MA, Sibley LD, Betts MR, Hunter CA. Parasite fate and involvement of infected cells in the induction of CD4+ and CD8+ T cell responses to Toxoplasma gondii. PLoS Pathog. 10(4):e1004047. 2014.
• Caignard G, Leiva-Torres GA, Leney-Greene M, Charbonneau B, Dumaine A, Fodil-Cornu N, Pyzik M, Cingolani P, Schwartzentruber J, Dupaul-Chicoine J, Guo H, Saleh M, Veillette A, Lathrop M, Blanchette M, Majewski J, Pearson A, Vidal SM. Genome-wide mouse mutagenesis reveals CD45-mediated T cell function as critical in protective immunity to HSV-1. PLoS Pathog. 9(9):e1003637. 2013.

Shruti Naik, PhD

Associate Professor of Pathology, Medicine, and Dermatology NYU Langone Health

Education

BS, Cell and Molecular Biology, University of Maryland, USA

PhD Immunology, University of Pennsylvania, 2012 (Mentor: Dr. Yasmine Belkaid, NIAID)

Thesis

During her doctoral studies, Shruti discovered that skin commensals educate the immune system and help protect us from harmful pathogens. Her work has opened the door for microbiota-based therapies in the skin.

Publications From Graduate Work

• Naik S, Bouladoux N, Linehan JL, Han SJ, Harrison OJ, Wilhelm C, Conlan S,Himmelfarb S, Byrd AL, Deming C, Quinones M, Brenchley JM, Kong HH, Tussiwand R, Murphy KM, Merad M, Segre JA, Belkaid Y. Commensal-dendritic-cell interaction specifies a unique protective skin immune signature. Nature. 520(7545):104-108. 2015.
• Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, Molina DA, Salcedo R, Back T, Cramer S, Dai RM, Kiu H, Cardone M, Naik S, Patri AK, Wang E, Marincola FM, Frank KM, Belkaid Y, Trinchieri G, Goldszmid RS. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science. 342(6161):967-70. 2013.
• Molloy MJ, Grainger JR, Bouladoux N, Hand TW, Koo LY, Naik S, Quinones M, Dzutsev AK, Gao JL, Trinchieri G, Murphy PM, Belkaid Y. Intraluminal containment of commensal outgrowth in the gut during infection-induced dysbiosis. Cell Host Microbe. 14(3):318-28. 2013.
• Chappert P, Bouladoux N, Naik S, Schwartz RH. Specific gut commensal flora locally alters T cell tuning to endogenous ligands. Immunity. 38(6):1198-210. 2013.
• Myles IA, Fontecilla NM, Valdez PA, Vithayathil PJ, Naik S, Belkaid Y, Ouyang W, Datta SK. Signaling via the IL-20 receptor inhibits cutaneous production of IL-1β and IL-17A to promote infection with methicillin-resistant Staphylococcus aureus. Nat Immunol. 14(8):804-11. 2013. 
• Belkaid Y, Naik S. Compartmentalized and systemic control of tissue immunity by commensals. Nat Immunol. 14(7):646-53. 2013
• Carpenter AC, Grainger JR, Xiong Y, Kanno Y, Chu HH, Wang L, Naik S, dos
• Santos L, Wei L, Jenkins MK, O'Shea JJ, Belkaid Y, Bosselut R. The transcription factors Thpok and LRF are necessary and partly redundant for T helper cell differentiation. Immunity. 37(4):622-33. 2012.
• Naik S, Bouladoux N, Wilhelm C, Molloy MJ, Salcedo R, Kastenmuller W, Deming C, Quinones M, Koo L, Conlan S, Spencer S, Hall JA, Dzutsev A, Kong H, Campbell DJ, Trinchieri G, Segre JA, Belkaid Y. Compartmentalized control of skin immunity by resident commensals. Science. 337(6098):1115-9. 2012.
• Gaidamakova EK, Myles IA, McDaniel DP, Fowler CJ, Valdez PA, Naik S, Gayen M, Gupta P, Sharma A, Glass PJ, Maheshwari RK, Datta SK, Daly MJ. Preserving immunogenicity of lethally irradiated viral and bacterial vaccine epitopes using a radio- protective Mn2+-Peptide complex from Deinococcus. Cell Host Microbe. 12(1):117-124. 2012.
• Wohlfert EA, Grainger JR, Bouladoux N, Konkel JE, Oldenhove G, Ribeiro CH,Hall JA, Yagi R, Naik S, Bhairavabhotla R, Paul WE, Bosselut R, Wei G, Zhao K, Oukka M, Zhu J, Belkaid Y. GATA3 controls Foxp3⁺ regulatory T cell fate during inflammation in mice. J Clin Invest. 121(11):4503-15. 2011.
• Hall JA, Cannons JL, Grainger JR, Dos Santos LM, Hand TW, Naik S, Wohlfert EA, Chou DB, Oldenhove G, Robinson M, Grigg ME, Kastenmayer R, Schwartzberg PL, Belkaid Y. Essential role for retinoic acid in the promotion of CD4(+) T cell effector responses via retinoic acid receptor alpha. Immunity. 25;34(3):435-47.  2011.

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Jacob Paiano, PhD

Post-doctoral Fellow, Norbert Perrimon Laboratory, Harvard Medical School

Education

BA, Biology, Chemistry, Case Western Reserve University, USA

PhD Immunology, University of Pennsylvania, 2020 (Mentor: Dr. Andre Nussenzweig, Ph.D, NCI/CCR)

Thesis

During Jacob's doctoral studies, he studied DNA repair mechanisms responsible for maintaining genomic stability during mitosis and meiosis

Publications From Graduate Work

• Paiano J, Zolnerowich N, Wu W, Pavani R, Wang C, Li H, Zheng L, Shen B, Sleckman BP, Chen BR, Nussenzweig A. Role of 53BP1 in end protection and DNA synthesis at DNA breaks. Genes & Development 35(19-20): 1356-1367. 2021

• Wu W*, Hill SE*, Nathan WJ*, Paiano J, Callen E, Wang D, Shinoda K, van Wietmarschen N, Colón-Mercado JM, Zong D, De Pace R, Shih HY, Coon S, Parsadanian M, Pavani R, Hanzlikova H, Park S, Jung SK, McHugh PJ, Canela A, Chen C, Casellas R, Caldecott KW, Ward ME, Nussenzweig A. Neuronal enhancers are hotspots for DNA single-strand break repair. Nature. 2021 Mar 25. doi: 10.1038/s41586-021-03468-5. PMID: 33767446.
• Mahgoub M*, Paiano J*, Bruno M, Wu W, Pathuri S, Zhang X, Ralls S, Cheng X, Nussenzweig A, Macfarlan T. Dual histone methyl reader ZCWPW1 facilitates repair of meiotic double strand breaks. eLife 9:e53360. 2020
• Paiano J, Nussenzweig A. Burning bridges in cancer genomes. Science 368(6488): 240-241. 2020
• Paiano J*, Wu W*, Yamada S, Sciascia N, Callen E, Cotrim AP, Deshpande RA, Maman Y, Day A, Paull TT, Nussenzweig A. ATM and PRDM9 regulate SPO11-bound recombination intermediates during meiosis. Nature Communications 11(1):857. 2020
• Paiano J*, Harland M*, Strainic MG, Nedrud J, Hussain W, Medof ME. Follicular B2 cell activation and class switch recombination depend on autocrine C3ar1/C5ar1 signaling in B2 cells. J. Immunol. 203(2):379-388. 2019
• Paiano JJ, Johnson JL, Vahedi G. Enhancing our understanding of enhancers in T helper cells. European Journal of Immunology 45(11): 2998-3001. 2015

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Indira Rao, PhD

Education

2003 – 2006 University of Mumbai, India, BSc Chemistry

2007 – 2008 Heriot-Watt University, United Kingdom, MSc Forensic Materials

2018 - 2025 University of Pennsylvania, Philadelphia, PhD Immunology

Thesis

Host-microbe interactions at barrier tissues mediate context-specific immune responses to commensal microbiota. Staphylococcus aureus can asymptomatically colonize the skin or cause recurrent opportunistic infections with limited protective immunity. My work reveals that homeostatic non-inflammatory skin colonization with S. aureus is sufficient to induce not only local response, but a systemic innate-like T cell response also at mucosal, lymphoid, and metabolic sites. In the mouse model, using microbial genetics, immunophenotyping, imaging and next-generation sequencing methods, I aim to (1) characterize innate-like homeostatic immunity to the topical microbe, (2) investigate how the topical skin microbe promotes said systemic response, and, importantly, (3) what the functional consequences of such a systemic response may be. Specifically, we endeavor to determine whether steady-state immunity represents an anticipatory response for protection during infection. These studies can shed light on the basic biology of how skin commensalism promotes overall metaorganism fitness.

Publications From Graduate Work

• Sorobetea,D., Matsuda, R., Peterson, S.T., Grayczyk, J.P., Rao, I., Krespan, E., Lanza, M., Assenmacher, C.A., Matthias Mack, M., Beiting, D.P., Radaelli, E., and Brodsky, I.E. Inflammatory monocytes promote granuloma control of Yersinia infection. Nature Microbiology 2023 8: 666–678 doi: 10.1038/s41564-023-01338-6

• Enamorado M., Kulalert W., Han S.J., Rao I., Delaleu J., Link V.M., Yong D., Smelkinson M., Gil L., Nakajima S., Linehan J.L., Bouladoux N., Wlaschin J., Kabat J., Kamenyeva O., Deng L., Gribonika I., Chesler A.T., Chiu I.M., Le Pichon C.E., Belkaid Y. Immunity to the microbiota promotes sensory neuron regeneration. Cell 2023 186(3):607-620. doi: https://doi.org/10.1016/j.cell.2022.12.037
• Lima-Junior D.S., Krishnamurthy S.R., Bouladoux N., Collins N., Han S.J., Chen E.Y., Constantinides M.G., Link V.M., Lim A.I., Enamorado M., Cataisson C., Gil L., Rao I., Farley T.K., Koroleva G., Attig J., Yuspa S.H., Fischbach M.A., Kassiotis G., Belkaid Y. Endogenous retroviruses promote homeostatic and inflammatory responses to the microbiota. Cell 2021 184(14):3794-3811 doi: 10.1016/j.cell.2021.05.020

Sean Spencer, MD, PhD

Instructor, Medicine, Gastroenterology and Hepatology, Stanford University

Education

BS, Medical Microbiology and Immunology, University of Wisconsin-Madison, USA

MD, PhD Immunology, University of Pennsylvania, 2013 (Mentor: Dr. Yasmine Belkaid, NIAID)

Thesis

Sean published seminal studies on the role of innate lymphoid cells (ILCs) in mediated barrier protection in the gastrointestinal tract during malnutrition and infections.

Publications From Graduate Work

• Wilhelm C, Harrison OJ, Schmitt V, Pelletier M, Spencer SP, Urban JF Jr, Ploch M, Ramalingam TR, Siegel RM, Belkaid Y. Critical role of fatty acid metabolism in ILC2-mediated barrier protection during malnutrition and helminth infection. 213(8):1409-18. J Exp Med. 2016.
• Mortha A, Chudnovskiy A, Hashimoto D, Bogunovic M, Spencer SP, Belkaid Y, Merad M. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science. 343(6178):1249288. 2014.
• Spencer SP, Wilhelm C, Yang Q, Hall JA, Bouladoux N, Boyd A, Nutman TB, Urban JF Jr, Wang J, Ramalingam TR, Bhandoola A, Wynn TA, Belkaid Y. Adaptation of innate lymphoid cells to a micronutrient deficiency promotes type 2 barrier immunity. Science. 343(6169):432-437. 2014.
• Korn LL, Thomas HL, Hubbeling HG, Spencer SP, Sinha R, Simkins HM, Salzman NH, Bushman FD, Laufer TM. Conventional CD4+ T cells regulate IL-22-producing intestinal innate lymphoid cells. 7(5):1045-57. Mucosal Immunol. 2014
• Klebanoff CA, Spencer SP, Torabi-Parizi P, Grainger JR, Roychoudhuri R, Ji Y, Sukumar M, Muranski P, Scott CD, Hall JA, Ferreyra GA, Leonardi AJ, Borman ZA, Wang J, Palmer DC, Wilhelm C, Cai R, Sun J, Napoli JL, Danner RL, Gattinoni L, Belkaid Y, Restifo NP. Retinoic acid controls the homeostasis of pre-cDC-derived splenic and intestinal dendritic cells. J Exp Med. 210(10):1961-76. 2013.
• Sciumé G, Hirahara K, Takahashi H, Laurence A, Villarino AV, Singleton KL, Spencer SP, Wilhelm C, Poholek AC, Vahedi G, Kanno Y, Belkaid Y, O'Shea JJ. Distinct requirements for T-bet in gut innate lymphoid cells. J Exp Med. 209(13):2331-8. 2012.
• Spencer SP, Belkaid Y. Dietary and commensal derived nutrients: shaping mucosal and systemic immunity. Curr Opin Immunol. 24(4):379-84. 2012
• Hall JA, Grainger JR, Spencer SP, Belkaid Y. The role of retinoic acid in tolerance and immunity. Immunity. 2011. 35(1):13-22.  
• Saenz SA, Siracusa MC, Perrigoue JG, Spencer SP, Urban JF Jr, Tocker JE, Budelsky AL, Kleinschek MA, Kastelein RA, Kambayashi T, Bhandoola A, Artis D. IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses. Nature. 464(7293):1362-6. 2010.

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Anastasia Tikhonova, PhD

Assistant Professor, Department of Medical Biophysics, University of Toronto

Education

BS, Natural Sciences, Bethel College, North Newton, KS, USA

PhD Immunology, University of Pennsylvania, 2011 (Mentor: Dr. Alfred Singer; NCI)

Thesis

During her thesis work, Anastasia investigated why the immune system preferentially generates MHC-restricted T cells. Her research led to the discovery of the first MHC-independent T cells and their conformational ligand, CD155. 

Publications From Graduate Work

• Van Laethem F, Tikhonova AN, Pobezinsky LA, Tai X, Kimura MY, Le Saout C, Guinter TI, Adams A, Sharrow SO, Bernhardt G, Feigenbaum L, Singer A. Lck availability during thymic selection determines the recognition specificity of the T cell repertoire. 154(6):1326-41. Cell. 2013.
• Van Laethem F, Tikhonova AN, Singer A. MHC restriction is imposed on a diverse T cell receptor repertoire by CD4 and CD8 co-receptors during thymic selection. Trends Immunol. 33(9):437-41.  2012.
• Tikhonova AN, Van Laethem F, Hanada K, Lu J, Pobezinsky LA, Hong C, Guinter TI, Jeurling SK, Bernhardt G, Park JH, Yang JC, Sun PD, Singer A. αβ T cell receptors that do not undergo major histocompatibility complex-specific thymic selection possess antibody-like recognition specificities. Immunity. 36(1):79-91. 2012.

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Greta Weiss, PhD

Research Officer, Burnet Institute, Centre for Biomedical Research, Melbourne, Australia

Education

AB Biology, Anthropology, Bryn Mawr College, USA

PhD Immunology, University of Pennsylvania, 2010 (Mentor: Dr. Susan Pierce; NIAID)

Thesis

Greta traveled to malaria-endemic areas (Mali and Peru) to study human B cell memory responses to Plasmodium falciparum. Her studies revealed the cellular basis of the delayed acquisition of protective humoral immunity against malaria.

Publications From Graduate Work

• Weiss GE, Ndungu FM, McKittrick N, Li S, Kimani D, Crompton PD, Marsh K, Pierce SK. High efficiency human memory B cell assay and its application to studying Plasmodium falciparum-specific memory B cells in natural infections. J Immunol Methods. 375(1-2):68-74. 2012.
• Clark EH, Silva CJ, Weiss GE, Li S, Padilla C, Crompton PD, Hernandez JN, Branch OH. Plasmodium falciparum malaria in the Peruvian Amazon, a region of low transmission, is associated with immunologic memory. Infect Immun. 80(4):1583-92. 2012.
• Weiss GE, Clark EH, Li S, Traore B, Kayentao K, Ongoiba A, Hernandez JN, Doumbo OK, Pierce SK, Branch OH, Crompton PD. A positive correlation between atypical memory B cells and Plasmodium falciparum transmission intensity in cross-sectional studies in Peru and Mali. PLoS One. 6(1):e15983.  2011.
•  Crompton PD, Miura K, Traore B, Kayentao K, Ongoiba A, Weiss G, Doumbo S, Doumtabe D, Kone Y, Huang CY, Doumbo OK, Miller LH, Long CA, Pierce SK. In vitro growth-inhibitory activity and malaria risk in a cohort study in mali. Infect Immun. 78(2):737-45.  2010.
• Weiss GE, Traore B, Kayentao K, Ongoiba A, Doumbo S, Doumtabe D, Kone Y, Dia S, Guindo A, Traore A, Huang CY, Miura K, Mircetic M, Li S, Baughman A, Narum DL, Miller LH, Doumbo OK, Pierce SK, Crompton PD. The Plasmodium falciparum-specific human memory B cell compartment expands gradually with repeated malaria infections. PLoS Pathog. 6(5):e1000912. 2010
• Crompton PD, Kayala MA, Traore B, Kayentao K, Ongoiba A, Weiss GE, Molina DM, Burk CR, Waisberg M, Jasinskas A, Tan X, Doumbo S, Doumtabe D, Kone Y, Narum DL, Liang X, Doumbo OK, Miller LH, Doolan DL, Baldi P, Felgner PL, Pierce SK. A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proc Natl Acad Sci U S A. 107(15):6958-63. 2010.
• Weiss GE, Crompton PD, Li S, Walsh LA, Moir S, Traore B, Kayentao K, Ongoiba A, Doumbo OK, Pierce SK. Atypical memory B cells are greatly expanded in individuals living in a malaria-endemic area. J Immunol. 183(3):2176-82. 2009
• Crompton PD, Mircetic M, Weiss G, Baughman A, Huang CY, Topham DJ, Treanor JJ, Sanz I, Lee FE, Durbin AP, Miura K, Narum DL, Ellis RD, Malkin E, Mullen GE, Miller LH, Martin LB, Pierce SK. The TLR9 ligand CpG promotes the acquisition of Plasmodium falciparum-specific memory B cells in malaria-naive individuals. J Immunol. 182(5):3318-26. 2009.
• Crompton PD, Traore B, Kayentao K, Doumbo S, Ongoiba A, Diakite SA, Krause MA, Doumtabe D, Kone Y, Weiss G, Huang CY, Doumbia S, Guindo A, Fairhurst RM, Miller LH, Pierce SK, Doumbo OK. Sickle cell trait is associated with a delayed onset of malaria: implications for time-to-event analysis in clinical studies of malaria. J Infect Dis. 198(9):1265-75. 2008.

Tori Yamamoto, PhD

Post-doctoral Fellow, Alex Marson Laboratory, University of California, San Francisco

Education

BA Biochemistry, Whitman College, Walla Walla, WA, USA

PhD Immunology, University of Pennsylvania, 2019 (Mentor: Dr. Nicholas Restifo, NCI)

Thesis

Tori engineered CD8⁺ T cells that were able to overcome death signaling within tumor environment. Such engineered CD8⁺ T cells exhibited enhanced persistence within tumors, resulting in superior cancer regression and overall survival.

Publications From Graduate Work

• Yamamoto TN, Kishton RJ, Restifo NP. Developing neoantigen-targeted T cell-based treatments for solid tumors. Nat Med. 25(10):1488-1499. 2019.
• Lee PH, Yamamoto TN, Gurusamy D, Sukumar M, Yu Z, Hu-Li J, Kawabe T, Gangaplara A, Kishton RJ, Henning AN, Vodnala SK, Germain RN, Paul WE, Restifo NP. Host conditioning with IL-1β improves the antitumor function of adoptively transferred T cells. J Exp Med. 216(11):2619-2634. 2019
• Kanellopoulou C, George AB, Masutani E, Cannons JL, Ravell JC, Yamamoto TN, Smelkinson MG, Jiang PD, Matsuda-Lennikov M, Reilley J, Handon R, Lee PH, Miller  JR, Restifo NP, Zheng L, Schwartzberg PL, Young M, Lenardo MJ. Mg(2+) regulation  of kinase signaling and immune function. J Exp Med. 216(8):1828-1842. 2019
• Vodnala SK, Eil R, Kishton RJ, Sukumar M, Yamamoto TN, Ha NH, Lee PH, Shin M, Patel SJ, Yu Z, Palmer DC, Kruhlak MJ, Liu X, Locasale JW, Huang J, Roychoudhuri R, Finkel T, Klebanoff CA, Restifo NP. T cell stemness and dysfunction in tumors are triggered by a common mechanism. Science. 363(6434). pii: eaau0135. 2019
• Yamamoto TN, Lee PH, Vodnala SK, Gurusamy D, Kishton RJ, Yu Z, Eidizadeh A, Eil R, Fioravanti J, Gattinoni L, Kochenderfer JN, Fry TJ, Aksoy BA, Hammerbacher JE, Cruz AC, Siegel RM, Restifo NP, Klebanoff CA. T cells genetically engineered  to overcome death signaling enhance adoptive cancer immunotherapy. J Clin Invest. 129(4):1551-1565. 2019.
• Klebanoff CA, Crompton JG, Leonardi AJ, Yamamoto TN, Chandran SS, Eil RL, Sukumar M, Vodnala SK, Hu J, Ji Y, Clever D, Black MA, Gurusamy D, Kruhlak MJ, Jin P, Stroncek DF, Gattinoni L, Feldman SA, Restifo NP. Inhibition of AKT signaling uncouples T cell differentiation from expansion for receptor-engineered adoptive immunotherapy. JCI Insight.2(23). pii: 95103. 2017.
• Williams CM, Schonnesen AA, Zhang SQ, Ma KY, He C, Yamamoto T, Eckhardt SG, Klebanoff CA, Jiang N. Normalized Synergy Predicts That CD8 Co-Receptor Contribution to T Cell Receptor (TCR) and pMHC Binding Decreases As TCR Affinity Increases in Human Viral-Specific T Cells. Front Immunol. 8:894. 2017
• Patel SJ, Sanjana NE, Kishton RJ, Eidizadeh A, Vodnala SK, Cam M, Gartner JJ,  Jia L, Steinberg SM, Yamamoto TN, Merchant AS, Mehta GU, Chichura A, Shalem O, Tran E, Eil R, Sukumar M, Guijarro EP, Day CP, Robbins P, Feldman S, Merlino G, Zhang F, Restifo NP. Identification of essential genes for cancer immunotherapy. Nature. 548(7669):537-542. 2017.
• Cruz AC, Ramaswamy M, Ouyang C, Klebanoff CA, Sengupta P, Yamamoto TN, Meylan F, Thomas SK, Richoz N, Eil R, Price S, Casellas R, Rao VK, Lippincott-Schwartz J, Restifo NP, Siegel RM. Fas/CD95 prevents autoimmunity independently of lipid raft localization and efficient apoptosis induction. Nat Commun. 7:13895. 2016.