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    Susan L Swain PhD

    TitleProfessor
    InstitutionUniversity of Massachusetts Medical School
    DepartmentPathology
    AddressUniversity of Massachusetts Medical School
    55 Lake Avenue North
    Worcester MA 01655
      Other Positions
      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentImmunology and Virology

        Overview 
        Narrative

        Research and Professional Experience:

        1976-1977 Lecturer, UCSD, La Jolla, CA
        1976-1981 Assistant Research Biologist, UCSD
        1981-1984 Associate Research Biologist, UCSD
        1984-1989 Associate Professor of Biology in Residence, UCSD
        1989-1995 Professor of Biology in Residence, UCSD
        1985-1996 Member, UCSD Cancer Center, San Diego, CA
        1996-2007 Director, Trudeau Institute, Saranac Lake, NY
        1996-present Member, Trudeau Institute, Saranac Lake, NY
        1996-2007 Edward C. Brewster Chair, Trudeau Inst., Saranac Lake, NY
        1998-present Adjunct Professor, Dept of Micro, Immunol & Mol. Gen, Albany Medical College, Albany, NY
        2001-present Adjunct Professor, University of Vermont College of Medicine, Burlington, VT
        2003-2007 President,Trudeau Institute, Saranac Lake, NY
        2008-2010 President Emeritus, Trudeau Institute
        2010 Professor of Pathology, UMASS Medical School, Worcester, MA

        Study Sections and Advisory Panels: Past:NIH Immunobiology Study Section (1984-1988); AIDS Basic Research Advisory Committee, NIAID (1990-1992); National Taskforce on Aging, NIA/NIAID (1994); FY1997 AIDS Planning Committee (1995); Ad Hoc Member, Board of Scientific Councilors NIAID (1995, 2000); Scientific Advisory Board, Inst. for Advanced Studies in Immunol. Aging (1996-1999); Reviewer's Reserve, NIH (1988-present); NHLBI SCOR Review in Asthma Panel (2001); Board of Scientific Councilors, National Institute of Aging (2001-2006), Arthritis Review Panel in Cellular Immunology (1996-1998); Board of Trustees, Ordway Institute, Albany, NY (2001-2005), External Advisory Committee, University of Montana COBRE (2005-2007). External Advisory Board Duke University Dept. of Immunology (2008), Current: Board of Directors La Jolla Institute of Allergy and Immunology (2004-present), Selection Committee Albany Medical Prize (2005-present), External Advisory Committee (EAC): Wistar BAA (2006-present) and Dartmouth University COBRE (2007-present). National Advisory Council on Aging 2008-2012, Scientific Advisory Board La Jolla Institute of Allergy and Immunology 2008-present, Advisory Group Aeras 2007-present, Distinguished Editorial Panel NIAID (2009), Council, NIAID (Ad Hoc, 2009)

        Editorial Boards:Past: Lymphokines (1985-1988); Journal of Immunology Associate Editor (1985-1987), Section Editor (1987-1991), Primary Reviewer (1997-present); International Immunology (1988-present); Cellular Immunology (1988-present); Cell (1990-1992); Current Opinion in Immunology, issue editor (1994, 1996, 2003, 2009); Current Biology (1994), Journal of Experimental Medicine (1997-2008), Current: Deputy Editor, Journal of Immunology 2008-2012, Faculty of 1000, Section Leader (2002-present).

        Meeting Organization: Workshop on T and B Cell Memory (1993, 1998); Midwinter Immunology Conference Council (1992), Midwinter Conference of Immunologists (1996); Keystone Symposium on Lymphocyte Activation (1996); International Cytokine Conference (1997); Delegate IUIS (2002-2006), Workshop on Immunity and Aging, Trudeau Institute, NY (2004); Cold Spring Harbor Vaccine Meeting (2005, 2007, 2009), Keystone Symposium on Immunological Memory (2007), FASEB Summer Conference (2008, 2010).

        Community Service:American Association of Immunology: Committee on Women (1988-1994), Program Committee (1988-1994); Chair, T Cell Block for FASEB Meeting (1992-1995); Nominations Committee (Elected, 1991, 1995,1996). Publication Committee (Elected, 1994-1998).

        Elected Positions: Council Member, American Association of Immunologists (1999-2006); Electorate Nominating Committee of the Section on Medical Sciences, AAAS (2004); President, American Association of Immunologists (2004).

        Honors and Awards:Phi Beta Kappa, Magna Cum Laude, B.A. (1968); Sigma Xi (1972); Established Investigator, American Heart Association (1981-1986); NIH Merit Award (1995, 2005); New York State Woman of Distinction (2002); Fellow of the American Association for Advancement of Science (2007); American Association of Immunologists Lifetime Achievement Award (2010).

        Dr. Susan SwainOur past research has focused on defining the cellular and molecular mechanisms by which CD4 T cells contribute to immunity. In particular we have 1) Defined, generated and determined the function of T cell subsets at the effector stage; 2) Studied the requirements for the generation of long-live memory CD4 T cells and their role in protection against influenza infection and 3) Analyzed the defects that develop in T cell function with aging and the causes of those defects.

        Our top priorities at this time are to discover new basic cellular and molecular mechanisms that are used by memory CD4 T cells to provide effective immunity to infectious diseases and to better define the age-associated defects in CD4 T cells that contribute to poor immunity of the aged and to discover strategies to overcome those defects.



        Rotation Projects

        Rotations: Projects in the following areas

        CD4 T cell memory. We can generate in vitro CD4 T cells that are for all extents and purposes identical to the memory CD4 T cells observed in vivo. In situ memory CD4 T cells persist at very low frequency and in most instances it is difficult to analyze them thoroughly using tetramer or multimer reagents both because of their low frequency and the relatively low specific affinity of the Class II reagents for the TcR. Being able to generate “recent” memory cells in vitro gives us the opportunity to analyze in detail the mechanisms by which memory CD4 T cells may contribute to secondary immunity and immune protection. Once identified. will determine if particular pathways are relevant in situ. We have discovered that memory CD4 T cells are superior in protection to those from the primary response and that they display pleitropic functions that have not been previously identified.

        Cytotoxic CD4 Effectors. One unexpected function of CD4 T cells we identified is robust, perforin-dependent cytotoxic activity (7, 16). Cytotoxic activity by CD4 T cells has been reported in response to several infections, but its significance has not heretofore been established. We find that “Th1 polarized” CD4 effectors and more relevantly the CD4 effectors found in the lung following influenza infection, are able to kill infected or peptide-pulsed Class II-bearing targets and we find that this perforin dependent activity can work together with antibody to provide protection against lethal influenza challenge in otherwise unprimed mice (17). We also will determine when memory CD4 T cells re-express cytotoxic activity following in vivo challenge and how cytotoxic killing contributes to the memory cell mediated protection. We want to analyze how the program of cytotoxicity is induced in these “ThCTL”.

        Memory CD4 Cells Enhance an Innate Response. Memory cells can act by becoming secondary effectors but they are best characterized by their ability respond rapidly even to low antigen doses, by producing cytokines and chemokines and it is assumed that these initial abilities are key to memory cell activity. However this assumption has not been directly demonstrated and the mechanisms involved and how they might contribute to immunity have not been elucidated. We find that restimulation of memory CD4 T cells leads to a markedly enhanced early innate response to influenza infection both in the lung and systemically (17). This response peaks 2-3 days after infection and is transient. We see enhanced production of IL-6 locally and systemically and enhanced production a broad spectrum of innate inflammatory mediators in the lung. We hope to determine in detail the pathways leading to optimum memory T cell-induced innate responses. We suggest a concurrent activation of CD4 memory cells may be an effective adjuvant for vaccination and will be testing this hypothesis as well as mechanisms that lead to viral control over the next couple of years.

        Aging and Immunity: The study of the impact of aging on CD4 T cell function at the naïve and memory stages has lead us to better understanding of fundamental aspects of T cell behavior in addition to providing important information about what vaccine approaches are most likely to be successful for the aged.

        Nature of CD4 Aging “Defects”. We have identified multiple levels at which aged naïve CD4 T cells are defective including initial early response to TcR triggering, IL-2 production, expansion and effector generation. The defects in helper function and in the 20 response of memory cells generated from aged naïve CD4 T cells are particularly dramatic. In recent studies we have recapitulated memory age-associated defects in recently generated memory cells in vitro (23). In vitro aged memory cells are markedly defective in production of particular cytokines, IL-4, IL-5 and IL-2, while others are little affected (IFNg, IL-10, TNF), suggesting the aging “defect” may be restricted to loss of potential to make certain CD4 T cell subsets, such as those responsible for help to B cells .We will pursue this hypothesis both in vitro and in vivo.

        We have found that aged naïve CD4 T cells are in fact longer-lived than their naïve counterparts (23). We find that reduced expression of Bim, a proapoptotic protein, is responsible for this increase in lifespan and that the increase in lifespan is required for the development of aging defects. We are now investigating the factors that regulate Bim expression.

        Enhancement by Inflammatory Cytokines. We have shown that the defective effector generation responses of naïve CD4 T cells from aged animals can be overcome by IL-2 and by proinflammatory cytokines, in particular a mix of IL-1, IL-6 and TNF (20,21). We want to determine the extent to which the inflammatory cytokines can reverse the heritable aging defects and restore functional memory generation. We have developed in vitro models to test the generation of effectors and memory. In these models we are evaluating TLR agonists for their ability to restore aged naïve CD4 responses to peptide-pulsed derived dendritic cells (DC). Pre-incubation of DC with many TLR agonists, enhances expansion of the responding aged naïve CD4 T cells via a mechanism dependent on IL-6 that acts in part by increasing survival of the developing effector population. We plan to use this model to identify the extent of the rescue and what pathways and mechanisms contribute with the ultimate goal of evaluating whether specific TLR stimulation or stimulation of specific pathways might improve the response of the elderly to vaccines. We want to see if we can reproduce this model with human naïve CD4 T cells and DC derived from peripheral blood and if TLR agonists can also enhance those responses.



        Post Docs

        An entry level postdoctoral position is open immediately in the laboratory of Dr. Susan L. Swain to study the factors that control the development and survival of CD4 and CD8 T cell memory. Graduate student experience with tissue culture, in vitro assay, flow cytometry, experience in mouse models on infectious disease and a knowledge of cellular and molecular immunology are all strongly desired.



        Bibliographic 
        selected publications
        List All   |   Timeline
        1. McKinstry KK, Dutton RW, Swain SL, Strutt TM. Erratum to: Memory CD4 T Cell-Mediated Immunity against Influenza A Virus: More than a Little Helpful. Arch Immunol Ther Exp (Warsz). 2013 Oct; 61(5):355.
          View in: PubMed
        2. Strutt TM, McKinstry KK, Marshall NB, Vong AM, Dutton RW, Swain SL. Multipronged CD4(+) T-cell effector and memory responses cooperate to provide potent immunity against respiratory virus. Immunol Rev. 2013 Sep; 255(1):149-64.
          View in: PubMed
        3. Swain SL, Blomberg BB. Immune senescence: new insights into defects but continued mystery of root causes. Curr Opin Immunol. 2013 Aug; 25(4):495-7.
          View in: PubMed
        4. Kai McKinstry K, Dutton RW, Swain SL, Strutt TM. Memory CD4 T Cell-Mediated Immunity against Influenza A Virus: More than a Little Helpful. Arch Immunol Ther Exp (Warsz). 2013 Oct; 61(5):341-53.
          View in: PubMed
        5. Hamada H, Bassity E, Flies A, Strutt TM, Garcia-Hernandez Mde L, McKinstry KK, Zou T, Swain SL, Dutton RW. Multiple Redundant Effector Mechanisms of CD8+ T Cells Protect against Influenza Infection. J Immunol. 2013 Jan 1; 190(1):296-306.
          View in: PubMed
        6. Strutt TM, McKinstry KK, Kuang Y, Bradley LM, Swain SL. Memory CD4+ T-cell-mediated protection depends on secondary effectors that are distinct from and superior to primary effectors. Proc Natl Acad Sci U S A. 2012 Sep 18; 109(38):E2551-60.
          View in: PubMed
        7. Pearl JE, Torrado E, Tighe M, Fountain JJ, Solache A, Strutt T, Swain S, Appelberg R, Cooper AM. Nitric oxide inhibits the accumulation of CD4(+) CD44(hi) Tbet(+) CD69(lo) T cells in mycobacterial infection. Eur J Immunol. 2012 Aug 14.
          View in: PubMed
        8. McKinstry KK, Strutt TM, Kuang Y, Brown DM, Sell S, Dutton RW, Swain SL. Memory CD4+ T cells protect against influenza through multiple synergizing mechanisms. J Clin Invest. 2012 Aug 1; 122(8):2847-56.
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        9. Haynes L, Swain SL. Aged-related shifts in T cell homeostasis lead to intrinsic T cell defects. Semin Immunol. 2012 Oct; 24(5):350-5.
          View in: PubMed
        10. Brown DM, Lee S, Garcia-Hernandez Mde L, Swain SL. Multifunctional CD4 Cells Expressing Gamma Interferon and Perforin Mediate Protection against Lethal Influenza Virus Infection. J Virol. 2012 Jun; 86(12):6792-803.
          View in: PubMed
        11. Swain SL, McKinstry KK, Strutt TM. Expanding roles for CD4(+) T cells in immunity to viruses. Nat Rev Immunol. 2012; 12(2):136-48.
          View in: PubMed
        12. Marshall NB, Swain SL. Cytotoxic CD4 T cells in antiviral immunity. J Biomed Biotechnol. 2011; 2011:954602.
          View in: PubMed
        13. An J, Golech S, Klaewsongkram J, Zhang Y, Subedi K, Huston GE, Wood WH, Wersto RP, Becker KG, Swain SL, Weng N. Kruppel-like factor 4 (KLF4) directly regulates proliferation in thymocyte development and IL-17 expression during Th17 differentiation. FASEB J. 2011 Oct; 25(10):3634-45.
          View in: PubMed
        14. McKinstry KK, Strutt TM, Swain SL. Hallmarks of CD4 T cell immunity against influenza. J Intern Med. 2011 May; 269(5):507-18.
          View in: PubMed
        15. Strutt TM, McKinstry KK, Swain SL. Control of innate immunity by memory CD4 T cells. Adv Exp Med Biol. 2011; 780:57-68.
          View in: PubMed
        16. Swain S. Grand challenges in immunological memory. Front Immunol. 2010; 1:103.
          View in: PubMed
        17. Jones SC, Brahmakshatriya V, Huston G, Dibble J, Swain SL. TLR-activated dendritic cells enhance the response of aged naive CD4 T cells via an IL-6-dependent mechanism. J Immunol. 2010 Dec 1; 185(11):6783-94.
          View in: PubMed
        18. Tsukamoto H, Huston GE, Dibble J, Duso DK, Swain SL. Bim dictates naive CD4 T cell lifespan and the development of age-associated functional defects. J Immunol. 2010 Oct 15; 185(8):4535-44.
          View in: PubMed
        19. McKinstry KK, Strutt TM, Swain SL. Regulation of CD4+ T-cell contraction during pathogen challenge. Immunol Rev. 2010 Jul; 236:110-24.
          View in: PubMed
        20. Strutt TM, McKinstry KK, Dibble JP, Winchell C, Kuang Y, Curtis JD, Huston G, Dutton RW, Swain SL. Memory CD4+ T cells induce innate responses independently of pathogen. Nat Med. 2010 May; 16(5):558-64, 1p following 564.
          View in: PubMed
        21. McKinstry KK, Strutt TM, Swain SL. The potential of CD4 T-cell memory. Immunology. 2010 May; 130(1):1-9.
          View in: PubMed
        22. Tsukamoto H, Clise-Dwyer K, Huston GE, Duso DK, Buck AL, Johnson LL, Haynes L, Swain SL. Age-associated increase in lifespan of naive CD4 T cells contributes to T-cell homeostasis but facilitates development of functional defects. Proc Natl Acad Sci U S A. 2009 Oct 27; 106(43):18333-8.
          View in: PubMed
        23. Dorshkind K, Swain S. Age-associated declines in immune system development and function: causes, consequences, and reversal. Curr Opin Immunol. 2009 Aug; 21(4):404-7.
          View in: PubMed
        24. Maue AC, Yager EJ, Swain SL, Woodland DL, Blackman MA, Haynes L. T-cell immunosenescence: lessons learned from mouse models of aging. Trends Immunol. 2009 Jul; 30(7):301-5.
          View in: PubMed
        25. McKinstry KK, Strutt TM, Buck A, Curtis JD, Dibble JP, Huston G, Tighe M, Hamada H, Sell S, Dutton RW, Swain SL. IL-10 deficiency unleashes an influenza-specific Th17 response and enhances survival against high-dose challenge. J Immunol. 2009 Jun 15; 182(12):7353-63.
          View in: PubMed
        26. Brown DM, Kamperschroer C, Dilzer AM, Roberts DM, Swain SL. IL-2 and antigen dose differentially regulate perforin- and FasL-mediated cytolytic activity in antigen specific CD4+ T cells. Cell Immunol. 2009; 257(1-2):69-79.
          View in: PubMed
        27. Hamada H, Garcia-Hernandez Mde L, Reome JB, Misra SK, Strutt TM, McKinstry KK, Cooper AM, Swain SL, Dutton RW. Tc17, a unique subset of CD8 T cells that can protect against lethal influenza challenge. J Immunol. 2009 Mar 15; 182(6):3469-81.
          View in: PubMed
        28. Swain SL, Nikolich-Zugich J. Key research opportunities in immune system aging. J Gerontol A Biol Sci Med Sci. 2009 Feb; 64(2):183-6.
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        29. Strutt TM, McKinstry KK, Swain SL. Functionally diverse subsets in CD4 T cell responses against influenza. J Clin Immunol. 2009 Mar; 29(2):145-50.
          View in: PubMed
        30. Eaton SM, Maue AC, Swain SL, Haynes L. Bone marrow precursor cells from aged mice generate CD4 T cells that function well in primary and memory responses. J Immunol. 2008 Oct 1; 181(7):4825-31.
          View in: PubMed
        31. Kamperschroer C, Roberts DM, Zhang Y, Weng NP, Swain SL. SAP enables T cells to help B cells by a mechanism distinct from Th cell programming or CD40 ligand regulation. J Immunol. 2008 Sep 15; 181(6):3994-4003.
          View in: PubMed
        32. Jones SC, Clise-Dwyer K, Huston G, Dibble J, Eaton S, Haynes L, Swain SL. Impact of post-thymic cellular longevity on the development of age-associated CD4+ T cell defects. J Immunol. 2008 Apr 1; 180(7):4465-75.
          View in: PubMed
        33. Jelley-Gibbs DM, Strutt TM, McKinstry KK, Swain SL. Influencing the fates of CD4 T cells on the path to memory: lessons from influenza. Immunol Cell Biol. 2008 May-Jun; 86(4):343-52.
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        34. McKinstry KK, Strutt TM, Swain SL. The effector to memory transition of CD4 T cells. Immunol Res. 2008; 40(2):114-27.
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        35. Hinshaw-Makepeace J, Huston G, Fortner KA, Russell JQ, Holoch D, Swain S, Budd RC. c-FLIP(S) reduces activation of caspase and NF-kappaB pathways and decreases T cell survival. Eur J Immunol. 2008 Jan; 38(1):54-63.
          View in: PubMed
        36. McKinstry KK, Golech S, Lee WH, Huston G, Weng NP, Swain SL. Rapid default transition of CD4 T cell effectors to functional memory cells. J Exp Med. 2007 Sep 3; 204(9):2199-211.
          View in: PubMed
        37. Aubert B, Bona M, Boutigny D, Karyotakis Y, Lees JP, Poireau V, Prudent X, Tisserand V, Zghiche A, Garra Tico J, Grauges E, Lopez L, Palano A, Eigen G, Ofte I, Stugu B, Sun L, Abrams GS, Battaglia M, Brown DN, Button-Shafer J, Cahn RN, Groysman Y, Jacobsen RG, Kadyk JA, Kerth LT, Kolomensky YG, Kukartsev G, Lopes Pegna D, Lynch G, Mir LM, Orimoto TJ, Pripstein M, Roe NA, Ronan MT, Tackmann K, Wenzel WA, Del Amo Sanchez P, Hawkes CM, Watson AT, Held T, Koch H, Lewandowski B, Pelizaeus M, Schroeder T, Steinke M, Boyd JT, Burke JP, Cottingham WN, Walker D, Asgeirsson DJ, Cuhadar-Donszelmann T, Fulsom BG, Hearty C, Knecht NS, Mattison TS, McKenna JA, Khan A, Saleem M, Teodorescu L, Blinov VE, Bukin AD, Druzhinin VP, Golubev VB, Onuchin AP, Serednyakov SI, Skovpen YI, Solodov EP, Todyshev KY, Bondioli M, Bruinsma M, Curry S, Eschrich I, Kirkby D, Lankford AJ, Lund P, Mandelkern M, Martin EC, Stoker DP, Abachi S, Buchanan C, Foulkes SD, Gary JW, Liu F, Long O, Shen BC, Zhang L, Paar HP, Rahatlou S, Sharma V, Berryhill JW, Campagnari C, Cunha A, Dahmes B, Hong TM, Kovalskyi D, Richman JD, Beck TW, Eisner AM, Flacco CJ, Heusch CA, Kroseberg J, Lockman WS, Schalk T, Schumm BA, Seiden A, Williams DC, Wilson MG, Winstrom LO, Chen E, Cheng CH, Dvoretskii A, Fang F, Hitlin DG, Narsky I, Piatenko T, Porter FC, Mancinelli G, Meadows BT, Mishra K, Sokoloff MD, Blanc F, Bloom PC, Chen S, Ford WT, Hirschauer JF, Kreisel A, Nagel M, Nauenberg U, Olivas A, Smith JG, Ulmer KA, Wagner SR, Zhang J, Chen A, Eckhart EA, Soffer A, Toki WH, Wilson RJ, Winklmeier F, Zeng Q, Altenburg DD, Feltresi E, Hauke A, Jasper H, Merkel J, Petzold A, Spaan B, Wacker K, Brandt T, Klose V, Lacker HM, Mader WF, Nogowski R, Schubert J, Schubert KR, Schwierz R, Sundermann JE, Volk A, Bernard D, Bonneaud GR, Latour E, Thiebaux Ch, Verderi M, Clark PJ, Gradl W, Muheim F, Playfer S, Robertson AI, Xie Y, Andreotti M, Bettoni D, Bozzi C, Calabrese R, Cecchi A, Cibinetto G, Franchini P, Luppi E, Negrini M, Petrella A, Piemontese L, Prencipe E, Santoro V, Anulli F, Baldini-Ferroli R, Calcaterra A, de Sangro R, Finocchiaro G, Pacetti S, Patteri P, Peruzzi IM, Piccolo M, Rama M, Zallo A, Buzzo A, Contri R, Lo Vetere M, Macri MM, Monge MR, Passaggio S, Patrignani C, Robutti E, Santroni A, Tosi S, Chaisanguanthum KS, Morii M, Wu J, Dubitzky RS, Marks J, Schenk S, Uwer U, Bard DJ, Dauncey PD, Flack RL, Nash JA, Nikolich MB, Panduro Vazquez W, Behera PK, Chai X, Charles MJ, Mallik U, Meyer NT, Ziegler V, Cochran J, Crawley HB, Dong L, Eyges V, Meyer WT, Prell S, Rosenberg EI, Rubin AE, Gritsan AV, Lae CK, Denig AG, Fritsch M, Schott G, Arnaud N, Béquilleux J, Davier M, Grosdidier G, Höcker A, Lepeltier V, Le Diberder F, Lutz AM, Pruvot S, Rodier S, Roudeau P, Schune MH, Serrano J, Sordini V, Stocchi A, Wang WF, Wormser G, Lange DJ, Wright DM, Chavez CA, Forster IJ, Fry JR, Gabathuler E, Gamet R, Hutchcroft DE, Payne DJ, Schofield KC, Touramanis C, Bevan AJ, George KA, Di Lodovico F, Menges W, Sacco R, Cowan G, Flaecher HU, Hopkins DA, Jackson PS, McMahon TR, Salvatore F, Wren AC, Brown DN, Davis CL, Allison J, Barlow NR, Barlow RJ, Chia YM, Edgar CL, Lafferty GD, West TJ, Yi JI, Anderson J, Chen C, Jawahery A, Roberts DA, Simi G, Tuggle JM, Blaylock G, Dallapiccola C, Hertzbach SS, Li X, Moore TB, Salvati E, Saremi S, Cowan R, Fisher PH, Sciolla G, Sekula SJ, Spitznagel M, Taylor F, Yamamoto RK, Kim H, McLachlin SE, Patel PM, Robertson SH, Lazzaro A, Lombardo V, Palombo F, Bauer JM, Cremaldi L, Eschenburg V, Godang R, Kroeger R, Sanders DA, Summers DJ, Zhao HW, Brunet S, Côté D, Simard M, Taras P, Viaud FB, Nicholson H, De Nardo G, Fabozzi F, Lista L, Monorchio D, Sciacca C, Baak MA, Raven G, Snoek HL, Jessop CP, Losecco JM, Benelli G, Corwin LA, Gan KK, Honscheid K, Hufnagel D, Kagan H, Kass R, Morris JP, Rahimi AM, Regensburger JJ, Ter-Antonyan R, Wong QK, Blount NL, Brau J, Frey R, Igonkina O, Kolb JA, Lu M, Rahmat R, Sinev NB, Strom D, Strube J, Torrence E, Gagliardi N, et al. Measurement of the Time-Dependent CP Asymmetry in B;{0}-->D_{CP};{(*)}h;{0} Decays. Phys Rev Lett. 2007 Aug 24; 99(8):081801.
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        38. Li X, McKinstry KK, Swain SL, Dalton DK. IFN-gamma acts directly on activated CD4+ T cells during mycobacterial infection to promote apoptosis by inducing components of the intracellular apoptosis machinery and by inducing extracellular proapoptotic signals. J Immunol. 2007 Jul 15; 179(2):939-49.
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        39. Jelley-Gibbs DM, Dibble JP, Brown DM, Strutt TM, McKinstry KK, Swain SL. Persistent depots of influenza antigen fail to induce a cytotoxic CD8 T cell response. J Immunol. 2007 Jun 15; 178(12):7563-70.
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        110. Zhang X, Brunner T, Carter L, Dutton RW, Rogers P, Bradley L, Sato T, Reed JC, Green D, Swain SL. Unequal death in T helper cell (Th)1 and Th2 effectors: Th1, but not Th2, effectors undergo rapid Fas/FasL-mediated apoptosis. J Exp Med. 1997 May 19; 185(10):1837-49.
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        111. Carter LL, Swain SL. Single cell analyses of cytokine production. Curr Opin Immunol. 1997 Apr; 9(2):177-82.
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        112. Haynes L, Linton PJ, Swain SL. Age-related changes in CD4 T cells of T cell receptor transgenic mice. Mech Ageing Dev. 1997 Feb; 93(1-3):95-105.
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        113. Linton PJ, Haynes L, Klinman NR, Swain SL. Antigen-independent changes in naive CD4 T cells with aging. J Exp Med. 1996 Nov 1; 184(5):1891-900.
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        114. Dubey C, Croft M, Swain SL. Naive and effector CD4 T cells differ in their requirements for T cell receptor versus costimulatory signals. J Immunol. 1996 Oct 15; 157(8):3280-9.
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        115. Muralidhar G, Koch S, Broome HE, Swain SL. TCR triggering of anergic CD4 T cells in murine AIDS induces apoptosis rather than cytokine synthesis and proliferation. J Immunol. 1996 Jul 15; 157(2):625-35.
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        116. Raz E, Tighe H, Sato Y, Corr M, Dudler JA, Roman M, Swain SL, Spiegelberg HL, Carson DA. Preferential induction of a Th1 immune response and inhibition of specific IgE antibody formation by plasmid DNA immunization. Proc Natl Acad Sci U S A. 1996 May 14; 93(10):5141-5.
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        117. Yoshimoto K, Swain SL, Bradley LM. Enhanced development of Th2-like primary CD4 effectors in response to sustained exposure to limited rIL-4 in vivo. J Immunol. 1996 May 1; 156(9):3267-74.
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        118. Swain SL, Croft M, Dubey C, Haynes L, Rogers P, Zhang X, Bradley LM. From naive to memory T cells. Immunol Rev. 1996 Apr; 150:143-67.
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        119. Jaiswal AI, Dubey C, Swain SL, Croft M. Regulation of CD40 ligand expression on naive CD4 T cells: a role for TCR but not co-stimulatory signals. Int Immunol. 1996 Feb; 8(2):275-85.
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        120. Zhang X, Giangreco L, Broome HE, Dargan CM, Swain SL. Control of CD4 effector fate: transforming growth factor beta 1 and interleukin 2 synergize to prevent apoptosis and promote effector expansion. J Exp Med. 1995 Sep 1; 182(3):699-709.
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        121. Bradley LM, Yoshimoto K, Swain SL. The cytokines IL-4, IFN-gamma, and IL-12 regulate the development of subsets of memory effector helper T cells in vitro. J Immunol. 1995 Aug 15; 155(4):1713-24.
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        122. Swain SL. T-cell subsets. Who does the polarizing? Curr Biol. 1995 Aug 1; 5(8):849-51.
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        123. Dubey C, Croft M, Swain SL. Costimulatory requirements of naive CD4+ T cells. ICAM-1 or B7-1 can costimulate naive CD4 T cell activation but both are required for optimum response. J Immunol. 1995 Jul 1; 155(1):45-57.
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        124. Croft M, Swain SL. Recently activated naive CD4 T cells can help resting B cells, and can produce sufficient autocrine IL-4 to drive differentiation to secretion of T helper 2-type cytokines. J Immunol. 1995 May 1; 154(9):4269-82.
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        125. Swain SL. CD4 T cell development and cytokine polarization: an overview. J Leukoc Biol. 1995 May; 57(5):795-8.
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        126. Bradley LM, Watson SR, Swain SL. Entry of naive CD4 T cells into peripheral lymph nodes requires L-selectin. J Exp Med. 1994 Dec 1; 180(6):2401-6.
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        127. Croft M, Carter L, Swain SL, Dutton RW. Generation of polarized antigen-specific CD8 effector populations: reciprocal action of interleukin (IL)-4 and IL-12 in promoting type 2 versus type 1 cytokine profiles. J Exp Med. 1994 Nov 1; 180(5):1715-28.
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        128. Swain SL. Generation and in vivo persistence of polarized Th1 and Th2 memory cells. Immunity. 1994 Oct; 1(7):543-52.
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        129. Duncan DD, Swain SL. Role of antigen-presenting cells in the polarized development of helper T cell subsets: evidence for differential cytokine production by Th0 cells in response to antigen presentation by B cells and macrophages. Eur J Immunol. 1994 Oct; 24(10):2506-14.
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        130. Koch S, Muralidhar G, Swain SL. Both naive and memory CD4 T cell subsets become anergic during MAIDS and each subset can sustain disease. J Immunol. 1994 Jun 1; 152(11):5548-56.
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        131. Croft M, Bradley LM, Swain SL. Naive versus memory CD4 T cell response to antigen. Memory cells are less dependent on accessory cell costimulation and can respond to many antigen-presenting cell types including resting B cells. J Immunol. 1994 Mar 15; 152(6):2675-85.
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        132. Tonkonogy SL, Swain SL. Distinct lymphokine production by CD4+ T cells isolated from mucosal and systemic lymphoid organs. Immunology. 1993 Dec; 80(4):574-80.
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        133. Swain SL. IL4 dictates T-cell differentiation. Res Immunol. 1993 Oct; 144(8):616-20.
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        134. Swain SL. Effector functions of helper T cells. J Immunother Emphasis Tumor Immunol. 1993 Aug; 14(2):150-4.
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        135. Bradley LM, Croft M, Swain SL. T-cell memory: new perspectives. Immunol Today. 1993 May; 14(5):197-9.
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        136. Bradley LM, Duncan DD, Yoshimoto K, Swain SL. Memory effectors: a potent, IL-4-secreting helper T cell population that develops in vivo after restimulation with antigen. J Immunol. 1993 Apr 15; 150(8 Pt 1):3119-30.
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        137. Swain SL. Helper T cells: polarized patterns of cytokine secretion. Curr Biol. 1993 Feb; 3(2):115-7.
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        138. Croft M, Swain SL. Analysis of CD4+ T cells that provide contact-dependent bystander help to B cells. J Immunol. 1992 Nov 15; 149(10):3157-65.
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        139. Croft M, Duncan DD, Swain SL. Response of naive antigen-specific CD4+ T cells in vitro: characteristics and antigen-presenting cell requirements. J Exp Med. 1992 Nov 1; 176(5):1431-7.
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        140. Muralidhar G, Koch S, Haas M, Swain SL. CD4 T cells in murine acquired immunodeficiency syndrome: polyclonal progression to anergy. J Exp Med. 1992 Jun 1; 175(6):1589-99.
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        141. Weinberg AD, Whitham R, Swain SL, Morrison WJ, Wyrick G, Hoy C, Vandenbark AA, Offner H. Transforming growth factor-beta enhances the in vivo effector function and memory phenotype of antigen-specific T helper cells in experimental autoimmune encephalomyelitis. J Immunol. 1992 Apr 1; 148(7):2109-17.
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        142. Swain SL, Bradley LM. Helper T cell memory: more questions than answers. Semin Immunol. 1992 Feb; 4(1):59-68.
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        143. Bradley LM, Atkins GG, Swain SL. Long-term CD4+ memory T cells from the spleen lack MEL-14, the lymph node homing receptor. J Immunol. 1992 Jan 15; 148(2):324-31.
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        144. Croft M, Swain SL. B cell response to T helper cell subsets. II. Both the stage of T cell differentiation and the cytokines secreted determine the extent and nature of helper activity. J Immunol. 1991 Dec 1; 147(11):3679-89.
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        145. Swain SL, Huston G, Tonkonogy S, Weinberg A. Transforming growth factor-beta and IL-4 cause helper T cell precursors to develop into distinct effector helper cells that differ in lymphokine secretion pattern and cell surface phenotype. J Immunol. 1991 Nov 1; 147(9):2991-3000.
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        146. Swain SL, Bradley LM, Croft M, Tonkonogy S, Atkins G, Weinberg AD, Duncan DD, Hedrick SM, Dutton RW, Huston G. Helper T-cell subsets: phenotype, function and the role of lymphokines in regulating their development. Immunol Rev. 1991 Oct; 123:115-44.
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        147. Bradley LM, Duncan DD, Tonkonogy S, Swain SL. Characterization of antigen-specific CD4+ effector T cells in vivo: immunization results in a transient population of MEL-14-, CD45RB- helper cells that secretes interleukin 2 (IL-2), IL-3, IL-4, and interferon gamma. J Exp Med. 1991 Sep 1; 174(3):547-59.
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        148. Croft M, Swain SL. B cell response to fresh and effector T helper cells. Role of cognate T-B interaction and the cytokines IL-2, IL-4, and IL-6. J Immunol. 1991 Jun 15; 146(12):4055-64.
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        149. Swain SL. Lymphokines and the immune response: the central role of interleukin-2. Curr Opin Immunol. 1991 Jun; 3(3):304-10.
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        150. Swain SL, Dutton RW. Is autoimmunity good for you? The Molecular Basis of Recognition in the Immune System sponsored by the European Federation of Immunological Societies, Edinburgh, UK, September 10-12, 1990. New Biol. 1991 Feb; 3(2):117-20.
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        151. Kubota E, McKenzie DT, Dutton RW, Swain SL. Role of T cells in the B-cell response: glutaraldehyde-fixed T-helper hybridoma cells synergize with the lymphokine IL-4 to induce B-cell activation and proliferation. Immunology. 1991 Jan; 72(1):40-7.
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        152. Swain SL. Regulation of the development of distinct subsets of CD4+ T cells. Res Immunol. 1991 Jan; 142(1):14-8.
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        153. Swain SL. Regulation of the development of helper T cell subsets. Immunol Res. 1991; 10(3-4):177-82.
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        154. Swain SL, Weinberg AD, English M, Huston G. IL-4 directs the development of Th2-like helper effectors. J Immunol. 1990 Dec 1; 145(11):3796-806.
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        155. Weinberg AD, Swain SL. IL-2 receptor (Tac antigen) protein expression is down-regulated by the 5'-untranslated region of the mRNA. J Immunol. 1990 Jun 15; 144(12):4712-20.
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        156. Swain SL, Croft M. Critical role of cognate interactions in the response of small, high-density B cells. Res Immunol. 1990 May-Jun; 141(4-5):431-40.
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        157. Weinberg AD, English M, Swain SL. Distinct regulation of lymphokine production is found in fresh versus in vitro primed murine helper T cells. J Immunol. 1990 Mar 1; 144(5):1800-7.
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        158. Swain SL, Weinberg AD, English M. CD4+ T cell subsets. Lymphokine secretion of memory cells and of effector cells that develop from precursors in vitro. J Immunol. 1990 Mar 1; 144(5):1788-99.
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        159. Tonkonogy SL, McKenzie DT, Swain SL. Regulation of isotype production by IL-4 and IL-5. Effects of lymphokines on Ig production depend on the state of activation of the responding B cells. J Immunol. 1989 Jun 15; 142(12):4351-60.
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        160. Swain SL. Role of helper T cells in the B cell response. Contrib Microbiol Immunol. 1989; 11:43-72.
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        161. Southern SO, Swain SL, Dutton RW. Induction of the H-2 D antigen during B cell activation. J Immunol. 1989 Jan 1; 142(1):336-42.
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        162. Swain SL, McKenzie DT, Weinberg AD, Hancock W. Characterization of T helper 1 and 2 cell subsets in normal mice. Helper T cells responsible for IL-4 and IL-5 production are present as precursors that require priming before they develop into lymphokine-secreting cells. J Immunol. 1988 Nov 15; 141(10):3445-55.
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        163. Swain SL, Dutton RW, McKenzie D, Helstrom H, English M. Role of antigen in the B cell response. Specific antigen and the lymphokine IL-5 synergize to drive B cell lymphoma proliferation and differentiation to Ig secretion. J Immunol. 1988 Jun 15; 140(12):4224-30.
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        164. Tonkonogy SL, Swain SL. Stimulation of gut-associated lymphoid cells by IL-4 and B-cell growth factor II. Immunology. 1988 May; 64(1):155-61.
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        165. Swain SL, McKenzie DT, Dutton RW, Tonkonogy SL, English M. The role of IL4 and IL5: characterization of a distinct helper T cell subset that makes IL4 and IL5 (Th2) and requires priming before induction of lymphokine secretion. Immunol Rev. 1988 Feb; 102:77-105.
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        166. Pfeifer JD, McKenzie DT, Swain SL, Dutton RW. B cell stimulatory factor 1 (interleukin 4) is sufficient for the proliferation and differentiation of lectin-stimulated cytolytic T lymphocyte precursors. J Exp Med. 1987 Nov 1; 166(5):1464-70.
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        167. Murray PD, McKenzie DT, Swain SL, Kagnoff MF. Interleukin 5 and interleukin 4 produced by Peyer's patch T cells selectively enhance immunoglobulin A expression. J Immunol. 1987 Oct 15; 139(8):2669-74.
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        168. McKenzie DT, Filutowicz HI, Swain SL, Dutton RW. Purification and partial sequence analysis of murine B cell growth factor II (interleukin 5). J Immunol. 1987 Oct 15; 139(8):2661-8.
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        169. Swain SL, Dutton RW. Consequences of the direct interaction of helper T cells with B cells presenting antigen. Immunol Rev. 1987 Oct; 99:263-80.
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        170. Kupfer A, Singer SJ, Janeway CA, Swain SL. Coclustering of CD4 (L3T4) molecule with the T-cell receptor is induced by specific direct interaction of helper T cells and antigen-presenting cells. Proc Natl Acad Sci U S A. 1987 Aug; 84(16):5888-92.
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        171. Kupfer A, Swain SL, Singer SJ. The specific direct interaction of helper T cells and antigen-presenting B cells. II. Reorientation of the microtubule organizing center and reorganization of the membrane-associated cytoskeleton inside the bound helper T cells. J Exp Med. 1987 Jun 1; 165(6):1565-80.
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        172. Southern SO, Swain SL, Dutton RW. B cell surface glycoprotein induced during growth response: molecular structure and expression pattern. J Immunol. 1987 Apr 15; 138(8):2568-75.
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        173. Swain SL, Dutton RW. B cell growth factor interactions. Adv Exp Med Biol. 1987; 213:215-25.
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        174. Kupfer A, Swain SL, Janeway CA, Singer SJ. The specific direct interaction of helper T cells and antigen-presenting B cells. Proc Natl Acad Sci U S A. 1986 Aug; 83(16):6080-3.
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        175. Murray PD, Swain SL, Kagnoff MP. Regulation of the IgM and IgA anti-dextran B1355S response: synergy between IFN-gamma, BCGF II, and IL 2. J Immunol. 1985 Dec; 135(6):4015-20.
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        176. Swain SL. Role of BCGFII in the differentiation to antibody secretion normal and tumor B cells. J Immunol. 1985 Jun; 134(6):3934-43.
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        177. Swain SL, Dutton RW. T-cell factors that promote B-cell proliferation and differentiation. Contemp Top Mol Immunol. 1985; 10:219-29.
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        178. Wetzel GD, Swain SL, Dutton RW, Kettman JR. Evidence for two distinct activation states available to B lymphocytes. J Immunol. 1984 Nov; 133(5):2327-32.
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        179. Dutton RW, Wetzel GD, Swain SL. Partial purification and characterization of a BCGFII from EL4 culture supernatants. J Immunol. 1984 May; 132(5):2451-6.
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        180. Swain SL, Dialynas DP, Fitch FW, English M. Monoclonal antibody to L3T4 blocks the function of T cells specific for class 2 major histocompatibility complex antigens. J Immunol. 1984 Mar; 132(3):1118-23.
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        181. Kagnoff MF, Arner LS, Swain SL. Lymphokine-mediated activation of a T cell-dependent IgA antipolysaccharide response. J Immunol. 1983 Nov; 131(5):2210-4.
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        182. Swain SL, Howard M, Kappler J, Marrack P, Watson J, Booth R, Wetzel GD, Dutton RW. Evidence for two distinct classes of murine B cell growth factors with activities in different functional assays. J Exp Med. 1983 Sep 1; 158(3):822-35.
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        183. Swain SL, Dutton RW, Schwab R, Yamamoto J. Xenogeneic human anti-mouse T cell responses are due to the activity of the same functional T cell subsets responsible for allospecific and major histocompatibility complex-restricted responses. J Exp Med. 1983 Feb 1; 157(2):720-9.
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        184. Swain SL. T cell subsets and the recognition of MHC class. Immunol Rev. 1983; 74:129-42.
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        185. Swain SL, Dutton RW. Production of a B cell growth-promoting activity, (DL)BCGF, from a cloned T cell line and its assay on the BCL1 B cell tumor. J Exp Med. 1982 Dec 1; 156(6):1821-34.
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        186. Zimmerman B, Swain SL, Dutton RW. Immunosuppressive ATS. V. Analysis of the effect of anti-thymocyte serum on T lymphocyte subsets. J Immunol. 1982 Aug; 129(2):515-20.
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        187. Wetzel GD, Swain SL, Dutton RW. A monoclonal T cell-replacing activity can act directly on B cells to enhance clonal expansion. J Exp Med. 1982 Jul 1; 156(1):306-11.
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        188. Dutton RW, Swain SL. Regulation of the immune response T-cell interactions. CRC Crit Rev Immunol. 1982 Feb; 3(3):209-61.
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        189. Swain SL, Wetzel GD, Soubiran P, Dutton RW. T cell replacing factors in the B cell response to antigen. Immunol Rev. 1982; 63:111-28.
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        190. Swain SL, Dutton RW. The role of IA in G-cell activation. Transplant Proc. 1981 Dec; 13(4):1843-5.
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        191. Puré E, Isakson PC, Takatsu K, Hamaoka T, Swain SL, Dutton RW, Dennert G, Uhr JW, Vitetta ES. Induction of B cell differentiation by T cell factors. I. Stimulation of IgM secretion by products of a T cell hybridoma and a T cell line. J Immunol. 1981 Nov; 127(5):1953-8.
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        192. Swain SL. Significance of Lyt phenotypes: Lyt2 antibodies block activities of T cells that recognize class 1 major histocompatibility complex antigens regardless of their function. Proc Natl Acad Sci U S A. 1981 Nov; 78(11):7101-5.
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        193. Swain SL. Significance of class 1 and class 2 major histocompatibility complex antigens: help to allogeneic K and D antigens does not involve I recognition. J Immunol. 1981 Jun; 126(6):2307-9.
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        194. Swain SL, Dennert G, Warner JF, Dutton RW. Culture supernatants of a stimulated T-cell line have helper activity that acts synergistically with interleukin 2 in the response of B cells to antigen. Proc Natl Acad Sci U S A. 1981 Apr; 78(4):2517-21.
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        195. Swain SL, Dennert G, Wormsley S, Dutton RW. The Lyt phenotype of a long-term allospecific T cell line. Both helper and killer activities to IA are mediated by Ly-1 cells. Eur J Immunol. 1981 Mar; 11(3):175-80.
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        196. Dennert G, Swain SL, Waterfield JD, Warner JF, Dutton RW. Fine specificity mapping of two allospecific T cell lines: recognition of private specificities in the H-2 IA subregion. Eur J Immunol. 1981 Jan; 11(1):62-4.
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        197. Swain SL. Association of Ly phenotypes, T cell function and MHC recognition. Fed Proc. 1980 Nov; 39(13):3110-3.
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        198. Shih WW, Matzinger PC, Swain SL, Dutton RW. Analysis of histocompatibility requirements for proliferative and helper T cell activity. T cell populations depleted of alloreactive cells by negative selection. J Exp Med. 1980 Nov 1; 152(5):1311-28.
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        199. Swain SL. Role of Ia-positive cells in the production of T cell-replacing factors: blocking of factor production with anti-Ia serum. J Immunol. 1980 Sep; 125(3):1224-9.
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        200. Silver J, Swain SL, Hubert JJ. Small subunit of I-A subregion antigens determines the allospecificity recognized by a monoclonal antibody. Nature. 1980 Jul 17; 286(5770):272-4.
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        201. Swain SL, Dutton RW. Production of Con A-induced helper T cell replacing factor requires a T cell and an Ia-positive non-T cells. J Immunol. 1980 Jan; 124(1):437-44.
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        202. Swain SL, Bakke A, English M, Dutton RW. Ly phenotypes and MHC recognition: the allohelper that recognizes K or D is a mature Ly123 cell. J Immunol. 1979 Dec; 123(6):2716-24.
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        203. Swain SL, Panfili PR, Dutton RW, Lefkovits I. Frequency of allogeneic helper T cells responding to whole H-2 differences and to an H-2K difference alone. J Immunol. 1979 Sep; 123(3):1062-7.
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        204. Waterfield JD, Dennert G, Swain SL, Dutton RW. Continuously proliferating allospecific T cells. I. Specificity of cooperation with allogeneic B cells in the humoral antibody response to sheep erythrocytes. J Exp Med. 1979 Apr 1; 149(4):808-14.
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        205. Swain SL, Panfili PR. Helper cells activated by allogeneic H-2K or H-2D differences have a Ly phenotype distinct from those responsive to I differences. J Immunol. 1979 Feb; 122(2):383-91.
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        206. Swain SL. Mechanism of allosuppression: evidence for direct suppression of responding B cells. J Immunol. 1978 Aug; 121(2):671-7.
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        207. Dutton RW, Panfili PR, Swain SL. Alloreactivity, the development of the T cell repertoire and the understanding of T cell function. Immunol Rev. 1978; 42:20-59.
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        208. Swain SL, Dutton RW. Negative allogeneic effects in vitro. II. Mapping of histocompatibility differences leading to allosuppression. J Immunol. 1977 Sep; 119(3):1179-86.
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        209. Swain SL, Dutton RW. Negative allogeneic effects in vitro. I. Allogeneic T cells markedly suppress the secondary antibody-forming cell response. J Immunol. 1977 Jun; 118(6):2262-8.
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        210. Swain SL, Trefts PE, Tse HY, Dutton RW. The significance of T-B collaboration across haplotype barriers. Cold Spring Harb Symp Quant Biol. 1977; 41 Pt 2:597-609.
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        211. Swain S, Coons AH. Characterization of T and B antigen-binding cells for beta-galactosidase. III. Independence of antigen-binding cells in normal animals from antigenic stimulation. J Immunol. 1976 Oct; 117(4):1067-72.
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        212. Swain S, Modabber F, Coons AH. Characterization of T and B antigen-binding cells for beta-galactosidase. II. T antigen-binding cells. J Immunol. 1976 Apr; 116(4):923-8.
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        213. Swain S, Modabber F, Coons AH. Characterization of T and B antigen-binding cells for beta-galactosidase. I. beta-galactosidase-binding cells in the thymus and spleen of normal mice. J Immunol. 1976 Apr; 116(4):915-22.
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