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Springer Seminars in Immunopathology

, Volume 26, Issue 4, pp 463–484 | Cite as

B cell superantigens: a microbe’s answer to innate-like B cells and natural antibodies

  • Carl S. GoodyearEmail author
  • Gregg J. Silverman
Original Article

Abstract

Marginal zone B cells and B-1 cells have been termed innate-like B cells as they express limited repertoires that play special roles in immune defenses against common infections. These B cells are the sources of natural antibodies and are capable of highly accelerated clonal responses that help counter blood-borne infections. We have characterized a class of microbial product with highly adapted binding interactions with host immunoglobulins/B cell receptors (BCRs), which enable the targeting of large supra-clonal sets of B cells for activation-associated apoptotic death. In recent studies, we have shown that all B cells with V region-targeted BCRs are susceptible. However, compared to follicular B cells, in vivo exposure preferentially causes innate-like B cells to undergo induced death with subsequent long-lasting supra-clonal depletion and immune tolerance. Based on these properties, it is likely that B cell superantigens influence the pathogenesis of some common infections, but also may provide novel therapeutic opportunities to treat B cell neoplastic and autoimmune diseases.

Keywords

B-1 cell Marginal zone B cell Tolerance Apoptosis Host immunity 

Notes

Acknowledgments

Work in our laboratory is supported by grants CA104815 from the NIH, the National Blood Foundation, the Cancer Research Institute (CSG) and AI40305, AR47360 and AI46637 from the NIH, and the Alliance for Lupus Research (GJS).

References

  1. 1.
    Alugupalli KR, Leong JM, Woodland RT, et al (2004) B1b lymphocytes confer T cell-independent long-lasting immunity. Immunity 21:379Google Scholar
  2. 2.
    Ansel KM, Harris RB, Cyster JG (2002) CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity. Immunity 16:67Google Scholar
  3. 3.
    Baumgarth N, Herman OC, Jager GC, et al (1999) Innate and acquired humoral immunities to influenza virus are mediated by distinct arms of the immune system. Proc Natl Acad Sci USA 96:2250Google Scholar
  4. 4.
    Baumgarth N, Herman OC, Jager GC, et al (2000) B-1 and B-2 cell-derived immunoglobulin M antibodies are nonredundant components of the protective response to influenza virus infection. J Exp Med 192:271Google Scholar
  5. 5.
    Baumgarth N, Chen J, Herman OC, et al (2000) The role of B-1 and B-2 cells in immune protection from influenza virus infection. Curr Top Microbiol Immunol 252:163Google Scholar
  6. 6.
    Beckingham JA, Bottomley SP, Hinton R, et al (1999) Interactions between a single immunoglobulin-binding domain of protein L from Peptostreptococcus magnus and a human kappa light chain. Biochem J 340:193Google Scholar
  7. 7.
    Benedict CL, Kearney JF (1999) Increased junctional diversity in fetal B cells results in a loss of protective anti-phosphorylcholine antibodies in adult mice. Immunity 10:607Google Scholar
  8. 8.
    Berland R, Wortis HH (2002) Origins and functions of B-1 cells with notes on the role of CD5. Annu Rev Immunol 20:253Google Scholar
  9. 9.
    Bjorck L (1988) Protein L. A novel bacterial cell wall protein with affinity for Ig L chains. J Immunol 140:1194Google Scholar
  10. 10.
    Boes M, Prodeus AP, Schmidt T, et al (1998) A critical role of natural immunoglobulin M in immediate defense against systemic bacterial infection. J Exp Med 188:2381Google Scholar
  11. 11.
    Briles DE, Nahm M, Schroer K, et al (1981) Antiphosphocholine antibodies found in normal mouse serum are protective against intravenous infection with type 3 Streptococcus pneumoniae. J Exp Med 153:694Google Scholar
  12. 12.
    Cary S, Krishnan M, Marion TN, et al (1999) The murine clan V(H) III related 7183, J606 and S107 and DNA4 families commonly encode for binding to a bacterial B cell superantigen. Mol Immunol 36:769Google Scholar
  13. 13.
    Cary SP, Lee J, Wagenknecht R, et al (2000) Characterization of superantigen-induced clonal deletion with a novel clan III-restricted avian monoclonal antibody: exploiting evolutionary distance to create antibodies specific for a conserved VH region surface. J Immunol 164:4730Google Scholar
  14. 14.
    Casali P, Notkins AL (1989) CD5+ B lymphocytes, polyreactive antibodies and the human B-cell repertoire. Immunol Today 10:364Google Scholar
  15. 15.
    Cazenave PA, Marche PN, Jouvin-Marche E, et al (1990) V beta 17 gene polymorphism in wild-derived mouse strains: two amino acid substitutions in the V beta 17 region greatly alter T cell receptor specificity. Cell 63:717Google Scholar
  16. 16.
    Chen M, Mun HS, Piao LX, et al (2003) Induction of protective immunity by primed B-1 cells in Toxoplasma gondii-infected B cell-deficient mice. Microbiol Immunol 47:997Google Scholar
  17. 17.
    Chen M, Aosai F, Norose K, et al (2003) The role of anti-HSP70 autoantibody-forming V(H)1-J(H)1 B-1 cells in Toxoplasma gondii-infected mice. Int Immunol 15:39Google Scholar
  18. 18.
    Cheng PC, Steele CR, Gu L, et al (1999) MHC class II antigen processing in B cells: accelerated intracellular targeting of antigens. J Immunol 162:7171Google Scholar
  19. 19.
    Cinamon G, Matloubian M, Lesneski MJ, et al (2004) Sphingosine 1-phosphate receptor 1 promotes B cell localization in the splenic marginal zone. Nat Immunol 5:713Google Scholar
  20. 20.
    Coutinho A, Kazatchkine MD, Avrameas S (1995) Natural autoantibodies. Curr Opin Immunol 7:812Google Scholar
  21. 21.
    Dalen A, Grov A, Matre R, et al (1977) A human IgA myeloma protein interacting with staphylococcal alpha-toxin and protein A. Clin Exp Immunol 27:421Google Scholar
  22. 22.
    Das T, Sa G, Ray PK (1999) Mechanisms of protein A superantigen-induced signal transduction for proliferation of mouse B cell. Immunol Lett 70:43Google Scholar
  23. 23.
    De Chateau M, Nilson BH, Erntell M, et al (1993) On the interaction between protein L and immunoglobulins of various mammalian species. Scand J Immunol 37:399Google Scholar
  24. 24.
    Derrick JP, Wigley DB (1992) Crystal structure of a streptococcal protein G domain bound to an Fab fragment. Nature 359:752Google Scholar
  25. 25.
    Derrick JP, Wigley DB (1994) The third IgG-binding domain from streptococcal protein G. An analysis by X-ray crystallography of the structure alone and in a complex with Fab. J Mol Biol 243:906Google Scholar
  26. 26.
    Fagarasan S, Shinkura R, Kamata T, et al (2000) Alymphoplasia (aly)-type nuclear factor kappaB-inducing kinase (NIK) causes defects in secondary lymphoid tissue chemokine receptor signaling and homing of peritoneal cells to the gut-associated lymphatic tissue system. J Exp Med 191:1477Google Scholar
  27. 27.
    Fearon DT, Locksley RM (1996) The instructive role of innate immunity in the acquired immune response. Science 272:50Google Scholar
  28. 28.
    Ferry H, Jones M, Vaux DJ, et al (2003) The cellular location of self-antigen determines the positive and negative selection of autoreactive B cells. J Exp Med 198:1415Google Scholar
  29. 29.
    Forsgren A, Sjoquist J (1966) Protein A from S. aureus. I. Pseudoimmune reaction with human gamma globulin. J Immunol 97:822Google Scholar
  30. 30.
    Forster I, Rajewsky K (1987) Expansion and functional activity of Ly-1+ B cells upon transfer of peritoneal cells into allotype-congenic, newborn mice. Eur J Immunol 17:521Google Scholar
  31. 31.
    Goodyear CS, Silverman GJ (2003) Death by a B cell superantigen: in vivo VH-targeted apoptotic supraclonal B cell deletion by a staphylococcal toxin. J Exp Med 197:1125Google Scholar
  32. 32.
    Goodyear CS, Narita M, Silverman GJ (2004) In vivo VL-targeted activation-induced apoptotic supraclonal deletion by a microbial B cell toxin. J Immunol 172:2870Google Scholar
  33. 33.
    Goodyear CS, Silverman GJ (2004) Staphylococcal toxin induced preferential and prolonged in vivo deletion of innate-like B lymphocytes. Proc Natl Acad Sci USA 101:11392Google Scholar
  34. 34.
    Graille M, Stura EA, Corper AL, et al (2000) Crystal structure of a Staphylococcus aureus protein A domain complexed with the Fab fragment of a human IgM antibody: structural basis for recognition of B-cell receptors and superantigen activity. Proc Natl Acad Sci USA 97:5399Google Scholar
  35. 35.
    Graille M, Stura E, Housden N, et al (2001) Complex between Peptostreptococcus magnus protein L and a human antibody reveals structural convergence in the interaction modes of Fab binding proteins. Structure 9:679Google Scholar
  36. 36.
    Gray D, Kumararatne DS, Lortan J, et al (1984) Relation of intra-splenic migration of marginal zone B cells to antigen localization on follicular dendritic cells. Immunology 52:659Google Scholar
  37. 37.
    Grimaldi CM, Michael DJ, Diamond B (2001) Cutting edge: expansion and activation of a population of autoreactive marginal zone B cells in a model of estrogen-induced lupus. J Immunol 167:1886Google Scholar
  38. 38.
    Groeneveld PH, Erich T, Kraal G (1985) In vivo effects of LPS on B lymphocyte subpopulations. Migration of marginal zone-lymphocytes and IgD-blast formation in the mouse spleen. Immunobiology 170:402Google Scholar
  39. 39.
    Grov A, Endresen C (1976) An examination of the “star-phenomenon”, a three component immunoprecipitation involving staphylococcal protein A. Acta Pathol Microbiol Scand [C] 84:333Google Scholar
  40. 40.
    Guinamard R, Okigaki M, Schlessinger J, et al (2000) Absence of marginal zone B cells in Pyk-2-deficient mice defines their role in the humoral response. Nat Immunol 1:31Google Scholar
  41. 41.
    Hakoda M, Kamatani N, Hayashimoto-Kurumada S, et al (1996) Differential binding avidities of human IgM for staphylococcal protein A derive from specific germline VH3 gene usage. J Immunol 157:2976Google Scholar
  42. 42.
    Hayakawa K, Hardy RR, Honda M, et al (1984) Ly-1 B cells: functionally distinct lymphocytes that secrete IgM autoantibodies. Proc Natl Acad Sci USA 81:2494Google Scholar
  43. 43.
    Hayakawa K, Hardy RR, Herzenberg LA, et al (1985) Progenitors for Ly-1 B cells are distinct from progenitors for other B cells. J Exp Med 161:1554Google Scholar
  44. 44.
    Hayakawa K, Hardy RR, Stall AM, et al (1986) Immunoglobulin-bearing B cells reconstitute and maintain the murine Ly-1 B cell lineage. Eur J Immunol 16:1313Google Scholar
  45. 45.
    Herzenberg LA, Stall AM, Lalor PA, et al (1986) The Ly-1 B cell lineage. Immunol Rev 93:81Google Scholar
  46. 46.
    Heyman B (1990) The immune complex: possible ways of regulating the antibody response. Immunol Today 11:310Google Scholar
  47. 47.
    Hillson JL, Karr NS, Oppliger IR, et al (1993) The structural basis of germline-encoded VH3 immunoglobulin binding to staphylococcal protein A. J Exp Med 178:331Google Scholar
  48. 48.
    Ito T, Ishikawa S, Sato T, et al (2004) Defective B1 cell homing to the peritoneal cavity and preferential recruitment of B1 cells in the target organs in a murine model for systemic lupus erythematosus. J Immunol 172:3628Google Scholar
  49. 49.
    Kantor AB, Herzenberg LA (1993) Origin of murine B cell lineages. Annu Rev Immunol 11:501Google Scholar
  50. 50.
    Kantor AB, Stall AM, Adams S, et al (1995) De novo development and self-replenishment of B cells. Int Immunol 7:55Google Scholar
  51. 51.
    Kastern W, Sjobring U, Bjorck L (1992) Structure of peptostreptococcal protein L and identification of a repeated immunoglobulin light chain-binding domain. J Biol Chem 267:12820Google Scholar
  52. 52.
    Kawahara T, Ohdan H, Zhao G, et al (2003) Peritoneal cavity B cells are precursors of splenic IgM natural antibody-producing cells. J Immunol 171:5406Google Scholar
  53. 53.
    Kawasaki K, Minoshima S, Nakato E, et al (2001) Evolutionary dynamics of the human immunoglobulin kappa locus and the germline repertoire of the Vkappa genes. Eur J Immunol 31:1017Google Scholar
  54. 54.
    Kipps TJ (1989) The CD5 B cell. Adv Immunol 47:117Google Scholar
  55. 55.
    Kirkham PM, Schroeder HWJ (1994) Antibody structure and the evolution of immunoglobulin V gene segments. Semin Immunol 6:347Google Scholar
  56. 56.
    Klein R, Jaenichen R, Zachau HG (1993) Expressed human immunoglobulin k genes and their hypermutation. Eur J Immunol 23:3248Google Scholar
  57. 57.
    Kronvall C, Williams RC (1971) The star phenomenon, a three component immunoprecipitation involving protein A. Immunochemistry 8:577Google Scholar
  58. 58.
    Kronvall G, Williams RC Jr (1969) Differences in anti-protein A activity among IgG subgroups. J Immunol 103:828Google Scholar
  59. 59.
    Lalor PA, Herzenberg LA, Adams S, et al (1989) Feedback regulation of murine Ly-1 B cell development. Eur J Immunol 19:507Google Scholar
  60. 60.
    Lalor PA, Morahan G (1990) The peritoneal Ly-1 (CD5) B cell repertoire is unique among murine B cell repertoires. Eur J Immunol 20:485Google Scholar
  61. 61.
    Liu YJ, Oldfield S, MacLennan IC (1988) Memory B cells in T cell-dependent antibody responses colonize the splenic marginal zones. Eur J Immunol 18:355Google Scholar
  62. 62.
    Lofdahl S, Guss B, Uhlen M, et al (1983) Gene for staphylococcal protein A. Proc Natl Acad Sci USA 80:697Google Scholar
  63. 63.
    Martin F, Oliver AM, Kearney JF (2001) Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14:617Google Scholar
  64. 64.
    McKenney D, Pouliot KL, Wang Y, et al (1999) Broadly protective vaccine for Staphylococcus aureus based on an in vivo-expressed antigen. Science 284:1523Google Scholar
  65. 65.
    Moks T, Abrahmsen L, Nilsson B, et al (1986) Staphylococcal protein A consists of five IgG-binding domains. Eur J Biochem 156:637Google Scholar
  66. 66.
    Mongini P, Highet P, Inman J (1997) Requirements for mIgM-triggered activation versus apoptosis in human B cells. Ann N Y Acad Sci 815:469Google Scholar
  67. 67.
    Mongini PK, Highet PF, Inman JK (1995) Human B cell activation. Effect of T cell cytokines on the physicochemical binding requirements for achieving cell cycle progression via the membrane IgM signaling pathway. J Immunol 155:3385Google Scholar
  68. 68.
    Mongini PK, Liu Q, Vilensky MA, et al (1998) Evidence for an upper affinity threshold for anti-IgM-induced apoptosis in a human B-cell lymphoma. Blood 92:3756Google Scholar
  69. 69.
    Nahm MH, Kroese FG, Hoffmann JW (1992) The evolution of immune memory and germinal centers. Immunol Today 13:438Google Scholar
  70. 70.
    Newkirk MM, Rauch J, Mageed RA, et al (1993) Restricted immunoglobulin variable region gene usage by hybridoma rheumatoid factors from patients with systemic lupus erythematosus and rheumatoid arthritis. Mol Immunol 30:255Google Scholar
  71. 71.
    Ochsenbein AF, Fehr T, Lutz C, et al (1999) Control of early viral and bacterial distribution and disease by natural antibodies. Science 286:2156Google Scholar
  72. 72.
    Oliver AM, Martin F, Gartland GL, et al (1997) Marginal zone B cells exhibit unique activation, proliferative and immunoglobulin secretory responses. Eur J Immunol 27:2366Google Scholar
  73. 73.
    Oppezzo P, Dumas G, Bouvet JP, et al (2004) Somatic mutations can lead to a loss of superantigenic and polyreactive binding. Eur J Immunol 34:1423Google Scholar
  74. 74.
    Palmqvist N, Foster T, Tarkowski A, et al (2002) Protein A is a virulence factor in Staphylococcus aureus arthritis and septic death. Microb Pathog 33:239Google Scholar
  75. 75.
    Patel AH, Nowlan P, Weavers ED, et al (1987) Virulence of protein A-deficient and alpha-toxin-deficient mutants of Staphylococcus aureus isolated by allele replacement. Infect Immun 55:3103Google Scholar
  76. 76.
    Pecquet SS, Ehrat C, Ernst PB (1992) Enhancement of mucosal antibody responses to Salmonella typhimurium and the microbial hapten phosphorylcholine in mice with X-linked immunodeficiency by B-cell precursors from the peritoneal cavity. Infect Immun 60:503Google Scholar
  77. 77.
    Pepys MB (1976) Role of complement in the induction of immunological responses. Transplant Rev 32:93Google Scholar
  78. 78.
    Pozdnyakova O, Guttormsen HK, Lalani FN, et al (2003) Impaired antibody response to group B streptococcal type III capsular polysaccharide in C3- and complement receptor 2-deficient mice. J Immunol 170:84Google Scholar
  79. 79.
    Pullen AM, Wade T, Marrack P, et al (1990) Identification of the region of T cell receptor beta chain that interacts with the self-superantigen MIs-1a. Cell 61:1365Google Scholar
  80. 80.
    Pullen AM, Bill J, Kubo RT, et al (1991) Analysis of the interaction site for the self superantigen Mls-1a on T cell receptor V beta. J Exp Med 173:1183Google Scholar
  81. 81.
    Roark JH, Bussel JB, Cines DB, et al (2002) Genetic analysis of autoantibodies in idiopathic thrombocytopenic purpura reveals evidence of clonal expansion and somatic mutation. Blood 100:1388Google Scholar
  82. 82.
    Sasano M, Burton DR, Silverman GJ (1993) Molecular selection of human antibodies with an unconventional bacterial B cell antigen. J Immunol 151:5822Google Scholar
  83. 83.
    Sasso EH, Silverman GJ, Mannik M (1989) Human IgM molecules that bind staphylococcal protein A contain VHIII H chains. J Immunol 142:2778Google Scholar
  84. 84.
    Sasso EH, Silverman GJ, Mannik M (1991) Human IgA and IgG F(ab’)2 that bind to staphylococcal protein A belong to the VHIII subgroup. J Immunol 147:1877Google Scholar
  85. 85.
    Shaw DR, Kirkham P, Schroeder HW. J, et al (1995) Structure-function studies of human monoclonal antibodies to pneumococcus type 3 polysaccharide. Ann N Y Acad Sci 764:370Google Scholar
  86. 86.
    Shibuya A, Sakamoto N, Shimizu Y, et al (2000) Fc alpha/mu receptor mediates endocytosis of IgM-coated microbes. Nat Immunol 1:441Google Scholar
  87. 87.
    Shinkura R, Kitada K, Matsuda F, et al (1999) Alymphoplasia is caused by a point mutation in the mouse gene encoding NF-kappa B-inducing kinase. Nat Genet 22:74Google Scholar
  88. 88.
    Silverman GJ, Lucas AH (1991) Variable region diversity in human circulating antibodies specific for the capsular polysaccharide of Haemophilus influenzae type b. Preferential usage of two types of VH3 heavy chains. J Clin Invest 88:911Google Scholar
  89. 89.
    Silverman GJ, Rapaport E (1992) Variable region restriction in circulating human antibodies specific for pneumococcal capsular polysaccharides. FASEB J 6:A1223Google Scholar
  90. 90.
    Silverman GJ, Sasano M, Wormsley SB (1993) Age-associated changes in binding of human B lymphocytes to a VH3-restricted unconventional bacterial antigen. J Immunol 151:5840Google Scholar
  91. 91.
    Silverman GJ, Nayak JV, Warnatz K, et al (1998) The dual phases of the response to neonatal exposure to a VH family-restricted staphylococcal B-cell superantigen. J Immunol 161:5720Google Scholar
  92. 92.
    Silverman GJ, Cary SP, Dwyer DC, et al (2000) A B cell superantigen-induced persistent “Hole” in the B-1 repertoire. J Exp Med 192:87Google Scholar
  93. 93.
    Silverman GJ, Cary S, Graille M, et al (2000) A B-cell superantigen that targets B-1 lymphocytes. Curr Top Microbiol Immunol 252:251Google Scholar
  94. 94.
    Silverman GJ, Shaw PX, Luo L, et al (2000) Neo-self antigens and the expansion of B-1 cells: lessons from atherosclerosis-prone mice. Curr Top Microbiol Immunol 252:189Google Scholar
  95. 95.
    Silverman GJ (2001) Adoptive transfer of a superantigen-induced “hole” in the repertoire of natural IgM-secreting cells. Cell Immunol 209:76Google Scholar
  96. 96.
    Silverman GJ, Goodyear CS (2001) In vivo VH targeted B-cell apoptotic deletion in mice and non-human primates. FASEB J 15:A694, 533.22Google Scholar
  97. 97.
    Silverman GJ, Goodyear CS (2002) A model B-cell superantigen and the immunobiology of B lymphocytes. Clin Immunol 102:117Google Scholar
  98. 98.
    Silverman GJ, Goodyear CS, Siegel DL (in press) On the mechanism of stapylococcal protein A immunomodulation. TransfusionGoogle Scholar
  99. 99.
    Skvaril F (1976) The question of specificity in binding human IgG subclasses to protein A-sepharose. Immunochemistry 13:871Google Scholar
  100. 100.
    Thiebe R, Schable KF, Bensch A, et al (1999) The variable genes and gene families of the mouse immunoglobulin kappa locus. Eur J Immunol 29:2072Google Scholar
  101. 101.
    Tlaskalova-Hogenova H, Mandel L, Stepankova R, et al (1992) Autoimmunity: from physiology to pathology. Natural antibodies, mucosal immunity and development of B cell repertoire. Folia Biol (Praha) 38:202Google Scholar
  102. 102.
    Todo K, Goto T, Miyamoto K, et al (2002) Physical and genetic map of the Finegoldia magna (formerly Peptostreptococcus magnus) ATCC 29328 genome. FEMS Microbiol Lett 210:33Google Scholar
  103. 103.
    Tortorella D, Gewurz BE, Furman MH, et al (2000) Viral subversion of the immune system. Annu Rev Immunol 18:861Google Scholar
  104. 104.
    Uhlen M, Guss B, Nilsson B, et al (1984) Complete sequence of the staphylococcal gene encoding protein A. A gene evolved through multiple duplications. J Biol Chem 259:1695Google Scholar
  105. 105.
    Van den Brink EN, Bril WS, Turenhout EA, et al (2002) Two classes of germline genes both derived from the V(H)1 family direct the formation of human antibodies that recognize distinct antigenic sites in the C2 domain of factor VIII. Blood 99:2828Google Scholar
  106. 106.
    Van Rooijen N (1989) Are bacterial endotoxins involved in autoimmunity by CD5+ (Ly-1+) B cells? Immunol Today 10:334Google Scholar
  107. 107.
    Viau M, Cholley B, Bjorck L, et al (2004) Down-modulation of the antigen receptor by a superantigen for human B cells. Immunol Lett 92:91Google Scholar
  108. 108.
    Viau M, Longo NS, Lipsky PE, et al (2004) Specific in vivo deletion of B-cell subpopulations expressing human immunoglobulins by the B-cell superantigen protein L. Infect Immun 72:3515Google Scholar
  109. 109.
    Vinuesa CG, Sunners Y, Pongracz J, et al (2001) Tracking the response of Xid B cells in vivo: TI-2 antigen induces migration and proliferation but Btk is essential for terminal differentiation. Eur J Immunol 31:1340Google Scholar
  110. 110.
    Wardemann H, Boehm T, Dear N, et al (2002) B-1a B cells that link the innate and adaptive immune responses are lacking in the absence of the spleen. J Exp Med 195:771Google Scholar
  111. 111.
    Weller S, Braun MC, Tan BK, et al (2004) Human blood IgM “memory” B cells are circulating splenic marginal zone B cells harboring a pre-diversified immunoglobulin repertoire. Blood 104:3647Google Scholar
  112. 112.
    White J, Pullen A, Choi K, et al (1993) Antigen recognition properties of mutant V beta 3+ T cell receptors are consistent with an immunoglobulin-like structure for the receptor. J Exp Med 177:119Google Scholar
  113. 113.
    Wikstrom M, Drakenberg T, Forsen S, et al (1994) Three-dimensional solution structure of an immunoglobulin light chain-binding domain of protein L. Comparison with the IgG-binding domains of protein G. Biochemistry 33:14011Google Scholar
  114. 114.
    Wilson M, Hsu E, Marcuz A, et al (1992) What limits affinity maturation of antibodies in Xenopus—the rate of somatic mutation or the ability to select mutants? EMBO J 11:4337Google Scholar
  115. 115.
    Yoder BJ, Goodrum KJ (2001) Plasmodium chabaudi chabaudi: B-1 cell expansion correlates with semiresistance in BALB/cJ mice. Exp Parasitol 98:71Google Scholar
  116. 116.
    Young WW, Tamura Y, Wolock DM, et al (1984) Staphylococcal protein A binding to the Fab of mouse monoclonal antibodies. J Immunol 133:3163Google Scholar
  117. 117.
    Zou YR, Gu H, Rajewsky K (1993) Generation of a mouse strain that produces immunoglobulin kappa chains with human constant regions. Science 262:1271Google Scholar

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© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Rheumatic Disease Core Center, Department of MedicineUniversity of California San DiegoLa JollaUSA

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