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    Samuel M Behar MD, PhD

    TitleProfessor
    InstitutionUniversity of Massachusetts Medical School
    DepartmentMicrobiology and Physiological Systems
    AddressUniversity of Massachusetts Medical School
    368 Plantation Street, AS8-2053
    Worcester MA 01605
    Phone774-455-3682
      Other Positions
      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentImmunology and Virology

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentMD/PhD Program

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentMolecular Genetics and Microbiology

        Overview 
        Narrative

        Samuel Behar

        Immunity to Tuberculosis. It is estimated that 1/3 of the world’s population has been infected with Mycobacterium tuberculosis (Mtb). In the majority of infected people, the immune response is able to adequately control the infection, and consequently only 5-10% will develop clinical disease during their lifetime. My long-term goal is to understand the immunological basis for protective immunity. One way we are investigating this problem is to determine why different mouse strains differ in their susceptibility to tuberculosis. We have observed that certain susceptible mouse strains are unable to efficiently recruit T cells to the lung following infection with Mtb, and this failure likely contributes to increased mortality and morbidity of susceptible mice. Therefore, we are particularly interested in the early events leading to the initiation of the pulmonary immune response following respiratory Mtb infection. This includes establishing how T cells and myeloid cells are recruited back to the lung and how these cells mediate their effector functions.

        Although BCG is used universally as a vaccine, its efficacy in preventing pulmonary tuberculosis is controversial. Most Mtb infected individuals develop long-lived immunity that contains the infection in a T cell-dependent manner. Thus, there is considerable interest in how different T cell subsets contribute to immunity and whether vaccination can stimulate protective T cells. Delineating the role of CD8+ T cells in host immunity to Mtb has been hindered by the paucity of antigens known to be recognized by CD8+ T cells. Our antigen discovery program has successfully identified and defined several mycobacterial peptide epitopes that are recognized by CD8+ T cells. For example, CD8+ T cells specific for culture filtrate protein-10 (CFP10) are found in infected people, indicating that CFP10 can prime CD8+ T cells after infection. Notably, CFP10 is encoded in the RD1 genetic locus, which is associated with Mtb virulence. The aim of our studies is to identify, enumerate and functionally characterize antigen-specific CD8+ T cells that are elicited following pulmonary infection. Finally, we are determining whether these antigens can be used as vaccines to elicit protective immunity.

        Rotation Projects
        LAB ROTATION PROJECTS AVAILABLE -- PLEASE CONTACT SAM BEHAR FOR MORE INFORMATION

        Bibliographic 
        selected publications
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        1. Jayaraman P, Sada-Ovalle I, Nishimura T, Anderson AC, Kuchroo VK, Remold HG, Behar SM. IL-1ß Promotes Antimicrobial Immunity in Macrophages by Regulating TNFR Signaling and Caspase-3 Activation. J Immunol. 2013 Apr 15; 190(8):4196-204.
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        2. Nobrega C, Nunes-Alves C, Cerqueira-Rodrigues B, Roque S, Barreira-Silva P, Behar SM, Correia-Neves M. T cells home to the thymus and control infection. J Immunol. 2013 Feb 15; 190(4):1646-58.
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        3. Tatituri RV, Watts GF, Bhowruth V, Barton N, Rothchild A, Hsu FF, Almeida CF, Cox LR, Eggeling L, Cardell S, Rossjohn J, Godfrey DI, Behar SM, Besra GS, Brenner MB, Brigl M. Recognition of microbial and mammalian phospholipid antigens by NKT cells with diverse TCRs. Proc Natl Acad Sci U S A. 2013 Jan 29; 110(5):1827-32.
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        4. Divangahi M, Behar SM, Remold H. Dying to live: how the death modality of the infected macrophage affects immunity to tuberculosis. Adv Exp Med Biol. 2013; 783:103-20.
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        5. Behar SM. Antigen-specific CD8(+) T cells and protective immunity to tuberculosis. Adv Exp Med Biol. 2013; 783:141-63.
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        6. Sada-Ovalle I, Chávez-Galán L, Torre-Bouscoulet L, Nava-Gamiño L, Barrera L, Jayaraman P, Torres-Rojas M, Salazar-Lezama MA, Behar SM. The Tim3-Galectin 9 Pathway Induces Antibacterial Activity in Human Macrophages Infected with Mycobacterium tuberculosis. J Immunol. 2012 Dec 15; 189(12):5896-902.
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        7. Martin CJ, Booty MG, Rosebrock TR, Nunes-Alves C, Desjardins DM, Keren I, Fortune SM, Remold HG, Behar SM. Efferocytosis is an innate antibacterial mechanism. Cell Host Microbe. 2012 Sep 13; 12(3):289-300.
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        8. Layre E, Sweet L, Hong S, Madigan CA, Desjardins D, Young DC, Cheng TY, Annand JW, Kim K, Shamputa IC, McConnell MJ, Debono CA, Behar SM, Minnaard AJ, Murray M, Barry CE, Matsunaga I, Moody DB. A Comparative Lipidomics Platform for Chemotaxonomic Analysis of Mycobacterium tuberculosis. Chem Biol. 2011 Dec 23; 18(12):1537-49.
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        9. Nandi B, Behar SM. Regulation of neutrophils by interferon-? limits lung inflammation during tuberculosis infection. J Exp Med. 2011 Oct 24; 208(11):2251-62.
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        10. Sakuishi K, Jayaraman P, Behar SM, Anderson AC, Kuchroo VK. Emerging Tim-3 functions in antimicrobial and tumor immunity. Trends Immunol. 2011 Aug; 32(8):345-9.
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        11. Sillé FC, Martin C, Jayaraman P, Rothchild A, Fortune S, Besra GS, Behar SM, Boes M. Requirement for invariant chain in macrophages for Mycobacterium tuberculosis replication and CD1d antigen presentation. Infect Immun. 2011 Aug; 79(8):3053-63.
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        12. Sillé FC, Martin C, Jayaraman P, Rothchild A, Besra GS, Behar SM, Boes M. Critical role for invariant chain in CD1d-mediated selection and maturation of Va14-invariant NKT cells. Immunol Lett. 2011 Sep 30; 139(1-2):33-41.
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        13. Behar SM, Martin CJ, Nunes-Alves C, Divangahi M, Remold HG. Lipids, apoptosis, and cross-presentation: links in the chain of host defense against Mycobacterium tuberculosis. Microbes Infect. 2011 Aug; 13(8-9):749-56.
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        14. Akhrameyeva NV, Zhang P, Sugiyama N, Behar SM, Yao F. Development of a glycoprotein D-expressing dominant-negative and replication-defective herpes simplex virus 2 (HSV-2) recombinant viral vaccine against HSV-2 infection in mice. J Virol. 2011 May; 85(10):5036-47.
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        15. Dieudé M, Striegl H, Tyznik AJ, Wang J, Behar SM, Piccirillo CA, Levine JS, Zajonc DM, Rauch J. Cardiolipin binds to CD1d and stimulates CD1d-restricted ?d T cells in the normal murine repertoire. J Immunol. 2011 Apr 15; 186(8):4771-81.
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        16. Behar SM, Martin CJ, Booty MG, Nishimura T, Zhao X, Gan HX, Divangahi M, Remold HG. Apoptosis is an innate defense function of macrophages against Mycobacterium tuberculosis. Mucosal Immunol. 2011 May; 4(3):279-87.
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        17. Woodworth JS, Shin D, Volman M, Nunes-Alves C, Fortune SM, Behar SM. Mycobacterium tuberculosis directs immunofocusing of CD8+ T cell responses despite vaccination. J Immunol. 2011 Feb 1; 186(3):1627-37.
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        18. Jayaraman P, Sada-Ovalle I, Beladi S, Anderson AC, Dardalhon V, Hotta C, Kuchroo VK, Behar SM. Tim3 binding to galectin-9 stimulates antimicrobial immunity. J Exp Med. 2010 Oct 25; 207(11):2343-54.
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        19. Behar SM, Divangahi M, Remold HG. Evasion of innate immunity by Mycobacterium tuberculosis: is death an exit strategy? Nat Rev Microbiol. 2010 Sep; 8(9):668-74.
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        20. Divangahi M, Desjardins D, Nunes-Alves C, Remold HG, Behar SM. Eicosanoid pathways regulate adaptive immunity to Mycobacterium tuberculosis. Nat Immunol. 2010 Aug; 11(8):751-8.
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        21. Zeissig S, Dougan SK, Barral DC, Junker Y, Chen Z, Kaser A, Ho M, Mandel H, McIntyre A, Kennedy SM, Painter GF, Veerapen N, Besra GS, Cerundolo V, Yue S, Beladi S, Behar SM, Chen X, Gumperz JE, Breckpot K, Raper A, Baer A, Exley MA, Hegele RA, Cuchel M, Rader DJ, Davidson NO, Blumberg RS. Primary deficiency of microsomal triglyceride transfer protein in human abetalipoproteinemia is associated with loss of CD1 function. J Clin Invest. 2010 Aug 2; 120(8):2889-99.
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        22. Garces A, Atmakuri K, Chase MR, Woodworth JS, Krastins B, Rothchild AC, Ramsdell TL, Lopez MF, Behar SM, Sarracino DA, Fortune SM. EspA acts as a critical mediator of ESX1-dependent virulence in Mycobacterium tuberculosis by affecting bacterial cell wall integrity. PLoS Pathog. 2010; 6(6):e1000957.
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        23. Sada-Ovalle I, Sköld M, Tian T, Besra GS, Behar SM. Alpha-galactosylceramide as a therapeutic agent for pulmonary Mycobacterium tuberculosis infection. Am J Respir Crit Care Med. 2010 Sep 15; 182(6):841-7.
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        24. Kiener HP, Watts GF, Cui Y, Wright J, Thornhill TS, Sköld M, Behar SM, Niederreiter B, Lu J, Cernadas M, Coyle AJ, Sims GP, Smolen J, Warman ML, Brenner MB, Lee DM. Synovial fibroblasts self-direct multicellular lining architecture and synthetic function in three-dimensional organ culture. Arthritis Rheum. 2010 Mar; 62(3):742-52.
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        25. Iweala OI, Smith DW, Matharu KS, Sada-Ovalle I, Nguyen DD, Dekruyff RH, Umetsu DT, Behar SM, Nagler CR. Vaccine-induced antibody isotypes are skewed by impaired CD4 T cell and invariant NKT cell effector responses in MyD88-deficient mice. J Immunol. 2009 Aug 15; 183(4):2252-60.
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        26. Divangahi M, Chen M, Gan H, Desjardins D, Hickman TT, Lee DM, Fortune S, Behar SM, Remold HG. Mycobacterium tuberculosis evades macrophage defenses by inhibiting plasma membrane repair. Nat Immunol. 2009 Aug; 10(8):899-906.
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        27. Behar SM, Shin DS, Maier A, Coblyn J, Helfgott S, Weinblatt ME. Use of the T-SPOT.TB assay to detect latent tuberculosis infection among rheumatic disease patients on immunosuppressive therapy. J Rheumatol. 2009 Mar; 36(3):546-51.
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        28. Woodworth JS, Wu Y, Behar SM. Mycobacterium tuberculosis-specific CD8+ T cells require perforin to kill target cells and provide protection in vivo. J Immunol. 2008 Dec 15; 181(12):8595-603.
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        29. Sada-Ovalle I, Chiba A, Gonzales A, Brenner MB, Behar SM. Innate invariant NKT cells recognize Mycobacterium tuberculosis-infected macrophages, produce interferon-gamma, and kill intracellular bacteria. PLoS Pathog. 2008 Dec; 4(12):e1000239.
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        30. Sköld M, Behar SM. Tuberculosis triggers a tissue-dependent program of differentiation and acquisition of effector functions by circulating monocytes. J Immunol. 2008 Nov 1; 181(9):6349-60.
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        31. Chen M, Divangahi M, Gan H, Shin DS, Hong S, Lee DM, Serhan CN, Behar SM, Remold HG. Lipid mediators in innate immunity against tuberculosis: opposing roles of PGE2 and LXA4 in the induction of macrophage death. J Exp Med. 2008 Nov 24; 205(12):2791-801.
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        32. Pollock NR, Campos-Neto A, Kashino S, Napolitano D, Behar SM, Shin D, Sloutsky A, Joshi S, Guillet J, Wong M, Nardell E. Discordant QuantiFERON-TB Gold test results among US healthcare workers with increased risk of latent tuberculosis infection: a problem or solution? Infect Control Hosp Epidemiol. 2008 Sep; 29(9):878-86.
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        33. Matsunaga I, Naka T, Talekar RS, McConnell MJ, Katoh K, Nakao H, Otsuka A, Behar SM, Yano I, Moody DB, Sugita M. Mycolyltransferase-mediated glycolipid exchange in Mycobacteria. J Biol Chem. 2008 Oct 24; 283(43):28835-41.
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        34. Woodworth JS, Fortune SM, Behar SM. Bacterial protein secretion is required for priming of CD8+ T cells specific for the Mycobacterium tuberculosis antigen CFP10. Infect Immun. 2008 Sep; 76(9):4199-205.
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        35. Wu Y, Woodworth JS, Shin DS, Morris S, Behar SM. Vaccine-elicited 10-kilodalton culture filtrate protein-specific CD8+ T cells are sufficient to mediate protection against Mycobacterium tuberculosis infection. Infect Immun. 2008 May; 76(5):2249-55.
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        36. Ernst JD, Lewinsohn DM, Behar S, Blythe M, Schlesinger LS, Kornfeld H, Sette A. Meeting Report: NIH Workshop on the Tuberculosis Immune Epitope Database. Tuberculosis (Edinb). 2008 Jul; 88(4):366-70.
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        37. Behar SM, Woodworth JS, Wu Y. Next generation: tuberculosis vaccines that elicit protective CD8+ T cells. Expert Rev Vaccines. 2007 Jun; 6(3):441-56.
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        38. Behar SM, Porcelli SA. CD1-restricted T cells in host defense to infectious diseases. Curr Top Microbiol Immunol. 2007; 314:215-50.
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        39. Kamath A, Woodworth JS, Behar SM. Antigen-specific CD8+ T cells and the development of central memory during Mycobacterium tuberculosis infection. J Immunol. 2006 Nov 1; 177(9):6361-9.
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        40. Kinjo Y, Tupin E, Wu D, Fujio M, Garcia-Navarro R, Benhnia MR, Zajonc DM, Ben-Menachem G, Ainge GD, Painter GF, Khurana A, Hoebe K, Behar SM, Beutler B, Wilson IA, Tsuji M, Sellati TJ, Wong CH, Kronenberg M. Natural killer T cells recognize diacylglycerol antigens from pathogenic bacteria. Nat Immunol. 2006 Sep; 7(9):978-86.
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        41. Ghosh S, Chackerian AA, Parker CM, Ballantyne CM, Behar SM. The LFA-1 adhesion molecule is required for protective immunity during pulmonary Mycobacterium tuberculosis infection. J Immunol. 2006 Apr 15; 176(8):4914-22.
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        42. Woodworth JS, Behar SM. Mycobacterium tuberculosis-specific CD8+ T cells and their role in immunity. Crit Rev Immunol. 2006; 26(4):317-52.
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        43. Sköld M, Xiong X, Illarionov PA, Besra GS, Behar SM. Interplay of cytokines and microbial signals in regulation of CD1d expression and NKT cell activation. J Immunol. 2005 Sep 15; 175(6):3584-93.
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        44. Tian T, Woodworth J, Sköld M, Behar SM. In vivo depletion of CD11c+ cells delays the CD4+ T cell response to Mycobacterium tuberculosis and exacerbates the outcome of infection. J Immunol. 2005 Sep 1; 175(5):3268-72.
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        45. Kamath AB, Behar SM. Anamnestic responses of mice following Mycobacterium tuberculosis infection. Infect Immun. 2005 Sep; 73(9):6110-8.
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        46. Debbabi H, Ghosh S, Kamath AB, Alt J, Demello DE, Dunsmore S, Behar SM. Primary type II alveolar epithelial cells present microbial antigens to antigen-specific CD4+ T cells. Am J Physiol Lung Cell Mol Physiol. 2005 Aug; 289(2):L274-9.
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        47. Sköld M, Behar SM. The role of group 1 and group 2 CD1-restricted T cells in microbial immunity. Microbes Infect. 2005 Mar; 7(3):544-51.
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        48. Kamath AB, Alt J, Debbabi H, Taylor C, Behar SM. The major histocompatibility complex haplotype affects T-cell recognition of mycobacterial antigens but not resistance to Mycobacterium tuberculosis in C3H mice. Infect Immun. 2004 Dec; 72(12):6790-8.
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        49. Kamath AB, Woodworth J, Xiong X, Taylor C, Weng Y, Behar SM. Cytolytic CD8+ T cells recognizing CFP10 are recruited to the lung after Mycobacterium tuberculosis infection. J Exp Med. 2004 Dec 6; 200(11):1479-89.
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        50. Cernadas M, Sugita M, van der Wel N, Cao X, Gumperz JE, Maltsev S, Besra GS, Behar SM, Peters PJ, Brenner MB. Lysosomal localization of murine CD1d mediated by AP-3 is necessary for NK T cell development. J Immunol. 2003 Oct 15; 171(8):4149-55.
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        51. Sköld M, Behar SM. Role of CD1d-restricted NKT cells in microbial immunity. Infect Immun. 2003 Oct; 71(10):5447-55.
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        52. Rauch J, Gumperz J, Robinson C, Sköld M, Roy C, Young DC, Lafleur M, Moody DB, Brenner MB, Costello CE, Behar SM. Structural features of the acyl chain determine self-phospholipid antigen recognition by a CD1d-restricted invariant NKT (iNKT) cell. J Biol Chem. 2003 Nov 28; 278(48):47508-15.
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        53. Kamath AB, Alt J, Debbabi H, Behar SM. Toll-like receptor 4-defective C3H/HeJ mice are not more susceptible than other C3H substrains to infection with Mycobacterium tuberculosis. Infect Immun. 2003 Jul; 71(7):4112-8.
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        54. Chackerian AA, Behar SM. Susceptibility to Mycobacterium tuberculosis: lessons from inbred strains of mice. Tuberculosis (Edinb). 2003; 83(5):279-85.
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        55. Dascher CC, Hiromatsu K, Xiong X, Sugita M, Buhlmann JE, Dodge IL, Lee SY, Roura-Mir C, Watts GF, Roy CJ, Behar SM, Clemens DL, Porcelli SA, Brenner MB. Conservation of CD1 intracellular trafficking patterns between mammalian species. J Immunol. 2002 Dec 15; 169(12):6951-8.
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        56. Chackerian A, Alt J, Perera V, Behar SM. Activation of NKT cells protects mice from tuberculosis. Infect Immun. 2002 Nov; 70(11):6302-9.
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        57. Chackerian AA, Alt JM, Perera TV, Dascher CC, Behar SM. Dissemination of Mycobacterium tuberculosis is influenced by host factors and precedes the initiation of T-cell immunity. Infect Immun. 2002 Aug; 70(8):4501-9.
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        58. Hiromatsu K, Dascher CC, Sugita M, Gingrich-Baker C, Behar SM, LeClair KP, Brenner MB, Porcelli SA. Characterization of guinea-pig group 1 CD1 proteins. Immunology. 2002 Jun; 106(2):159-72.
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        59. Grant EP, Beckman EM, Behar SM, Degano M, Frederique D, Besra GS, Wilson IA, Porcelli SA, Furlong ST, Brenner MB. Fine specificity of TCR complementarity-determining region residues and lipid antigen hydrophilic moieties in the recognition of a CD1-lipid complex. J Immunol. 2002 Apr 15; 168(8):3933-40.
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        60. Riese RJ, Shi GP, Villadangos J, Stetson D, Driessen C, Lennon-Dumenil AM, Chu CL, Naumov Y, Behar SM, Ploegh H, Locksley R, Chapman HA. Regulation of CD1 function and NK1.1(+) T cell selection and maturation by cathepsin S. Immunity. 2001 Dec; 15(6):909-19.
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        61. Chackerian AA, Perera TV, Behar SM. Gamma interferon-producing CD4+ T lymphocytes in the lung correlate with resistance to infection with Mycobacterium tuberculosis. Infect Immun. 2001 Apr; 69(4):2666-74.
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        62. Behar SM, Cardell S. Diverse CD1d-restricted T cells: diverse phenotypes, and diverse functions. Semin Immunol. 2000 Dec; 12(6):551-60.
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        63. Melián A, Watts GF, Shamshiev A, De Libero G, Clatworthy A, Vincent M, Brenner MB, Behar S, Niazi K, Modlin RL, Almo S, Ostrov D, Nathenson SG, Porcelli SA. Molecular recognition of human CD1b antigen complexes: evidence for a common pattern of interaction with alpha beta TCRs. J Immunol. 2000 Oct 15; 165(8):4494-504.
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        64. Gumperz JE, Roy C, Makowska A, Lum D, Sugita M, Podrebarac T, Koezuka Y, Porcelli SA, Cardell S, Brenner MB, Behar SM. Murine CD1d-restricted T cell recognition of cellular lipids. Immunity. 2000 Feb; 12(2):211-21.
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        65. Dascher CC, Hiromatsu K, Naylor JW, Brauer PP, Brown KA, Storey JR, Behar SM, Kawasaki ES, Porcelli SA, Brenner MB, LeClair KP. Conservation of a CD1 multigene family in the guinea pig. J Immunol. 1999 Nov 15; 163(10):5478-88.
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        66. Le Roux P, Behar S, Higgins D, Charette M. OP-1 enhances dendritic growth from cerebral cortical neurons in vitro. Exp Neurol. 1999 Nov; 160(1):151-63.
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        67. Behar SM, Dascher CC, Grusby MJ, Wang CR, Brenner MB. Susceptibility of mice deficient in CD1D or TAP1 to infection with Mycobacterium tuberculosis. J Exp Med. 1999 Jun 21; 189(12):1973-80.
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        68. Chen YH, Wang B, Chun T, Zhao L, Cardell S, Behar SM, Brenner MB, Wang CR. Expression of CD1d2 on thymocytes is not sufficient for the development of NK T cells in CD1d1-deficient mice. J Immunol. 1999 Apr 15; 162(8):4560-6.
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        69. Behar SM, Podrebarac TA, Roy CJ, Wang CR, Brenner MB. Diverse TCRs recognize murine CD1. J Immunol. 1999 Jan 1; 162(1):161-7.
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        70. Vincent MS, Roessner K, Sellati T, Huston CD, Sigal LH, Behar SM, Radolf JD, Budd RC. Lyme arthritis synovial gamma delta T cells respond to Borrelia burgdorferi lipoproteins and lipidated hexapeptides. J Immunol. 1998 Nov 15; 161(10):5762-71.
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        71. Fan X, Crowe SE, Behar S, Gunasena H, Ye G, Haeberle H, Van Houten N, Gourley WK, Ernst PB, Reyes VE. The effect of class II major histocompatibility complex expression on adherence of Helicobacter pylori and induction of apoptosis in gastric epithelial cells: a mechanism for T helper cell type 1-mediated damage. J Exp Med. 1998 May 18; 187(10):1659-69.
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        72. Sugita M, Moody DB, Jackman RM, Grant EP, Rosat JP, Behar SM, Peters PJ, Porcelli SA, Brenner MB. CD1--a new paradigm for antigen presentation and T cell activation. Clin Immunol Immunopathol. 1998 Apr; 87(1):8-14.
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        73. Behar SM, Chertow GM. Olecranon bursitis caused by infection with Candida lusitaniae. J Rheumatol. 1998 Mar; 25(3):598-600.
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        74. Behar SM, Roy C, Lederer J, Fraser P, Brenner MB. Clonally expanded Valpha12+ (AV12S1),CD8+ T cells from a patient with rheumatoid arthritis are autoreactive. Arthritis Rheum. 1998 Mar; 41(3):498-506.
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        75. Prigozy TI, Sieling PA, Clemens D, Stewart PL, Behar SM, Porcelli SA, Brenner MB, Modlin RL, Kronenberg M. The mannose receptor delivers lipoglycan antigens to endosomes for presentation to T cells by CD1b molecules. Immunity. 1997 Feb; 6(2):187-97.
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        76. Beckman EM, Melián A, Behar SM, Sieling PA, Chatterjee D, Furlong ST, Matsumoto R, Rosat JP, Modlin RL, Porcelli SA. CD1c restricts responses of mycobacteria-specific T cells. Evidence for antigen presentation by a second member of the human CD1 family. J Immunol. 1996 Oct 1; 157(7):2795-803.
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        77. Sugita M, Jackman RM, van Donselaar E, Behar SM, Rogers RA, Peters PJ, Brenner MB, Porcelli SA. Cytoplasmic tail-dependent localization of CD1b antigen-presenting molecules to MIICs. Science. 1996 Jul 19; 273(5273):349-52.
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        78. Behar SM, Porcelli SA, Beckman EM, Brenner MB. A pathway of costimulation that prevents anergy in CD28- T cells: B7-independent costimulation of CD1-restricted T cells. J Exp Med. 1995 Dec 1; 182(6):2007-18.
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        79. Behar SM, Roy C, Brenner MB. Expansions of V alpha 12 CD8+ T-cells in rheumatoid arthritis. Ann N Y Acad Sci. 1995 Jul 7; 756:130-7.
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        80. Behar SM, Porcelli SA. Mechanisms of autoimmune disease induction. The role of the immune response to microbial pathogens. Arthritis Rheum. 1995 Apr; 38(4):458-76.
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        81. Beckman EM, Porcelli SA, Morita CT, Behar SM, Furlong ST, Brenner MB. Recognition of a lipid antigen by CD1-restricted alpha beta+ T cells. Nature. 1994 Dec 15; 372(6507):691-4.
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        82. Behar SM, Lustgarten DL, Corbet S, Scharff MD. Characterization of somatically mutated S107 VH11-encoded anti-DNA autoantibodies derived from autoimmune (NZB x NZW)F1 mice. J Exp Med. 1991 Mar 1; 173(3):731-41.
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        83. Behar SM, Chien NC, Corbet S, Diamond B, Getzoff ED, Lustgarten D, Roberts VA, Scharff MD, Shin SU. Impact of somatic mutation on the S107(T15) heavy-chain V region of antibodies reactive with self and nonself. Cold Spring Harb Symp Quant Biol. 1989; 54 Pt 2:921-31.
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        84. Peng AT, Behar S, Yue SJ. Long-term therapeutic effects of electro-acupuncture for chronic neck and shoulder pain--a double blind study. Acupunct Electrother Res. 1987; 12(1):37-44.
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