Advertisement

A Distinct Role for B1b Lymphocytes in T Cell-Independent Immunity

  • K. R. Alugupalli
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 319)

Abstract

Pathogenesis of infectious disease is not only determined by the virulence of the microbe but also by the immune status of the host. Vaccination is the most effective means to control infectious diseases. A hallmark of the adaptive immune system is the generation of B cell memory, which provides a long-lasting protective antibody response that is central to the concept of vaccination. Recent studies revealed a distinct function for B1b lymphocytes, a minor subset of mature B cells that closely resembles that of memory B cells in a number of aspects. In contrast to the development of conventional B cell memory, which requires the formation of germinal centers and T cells, the development of B1b cell-mediated long-lasting antibody responses occurs independent of T cell help. T cell-independent (TI) antigens are important virulence factors expressed by a number of bacterial pathogens, including those associated with biological threats. TI antigens cannot be processed and presented to T cells and therefore are known to possess restricted T cell-dependent (TD) immunogenicity. Nevertheless, specific recognition of TI antigens by B1b cells and the highly protective antibody responses mounted by them clearly indicate a crucial role for this subset of B cells. Understanding the mechanisms of long-term immunity conferred by B1b cells may lead to improved vaccine efficacy for a variety of TI antigens.

Keywords

Antibody Response Germinal Center Reaction Protective Antibody Response 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

AID

Activation-induced cytidinedeaminase

BCR

B cell antigen receptor

Btk

Bruton’s tyrosine kinase

CSR

Class switch-recombination

FO

Follicular

LPS

Lipopolysaccharide

NP

4-Hydroxy-3-Nitrophenyl-Acetyl

PerC

Peritoneal cavity

PS

Polysaccharide

Rag1

Recombination-activating gene 1

SHM

Somatic hypermutation

TD

T cell-dependent

TI

T cell-independent

TI-1

T cell-independent type 1

TI-2

T cell-independent type 2

TLR

Toll-like receptor

Xid

X-linked immunodeficiency

XLA

X-linked agammaglobulinemia

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alugupalli KR, Michelson AD, Barnard MR, Leong JM (2001a) Serial determinations of platelet counts in mice by flow cytometry. Thromb Haemost 86:668–671.PubMedGoogle Scholar
  2. Alugupalli KR, Michelson AD, Barnard MR, Robbins D, Coburn J, Baker EK, Ginsberg MH, Schwan TG, Leong JM (2001b) Platelet activation by a relapsing fever spirochete results in enhanced bacterium-platelet interaction via integrin tIIbI3 activation. Mol Microbiol 39:330–340.PubMedGoogle Scholar
  3. Alugupalli KR, Gerstein RM, Chen J, Szomolanyi-Tsuda E, Woodland RT, Leong JM (2003a) The resolution of relapsing fever Borreliosis requires IgM and is concurrent with expansion of B1b lymphocytes. J Immunol 170:3819–3827.PubMedGoogle Scholar
  4. Alugupalli KR, Michelson AD, Joris I, Schwan TG, Hodivala-Dilke K, Hynes RO, Leong JM (2003b) Spirochete-platelet attachment and thrombocytopenia in murine relapsing fever borreliosis. Blood 102:2843–2850.PubMedGoogle Scholar
  5. Alugupalli KR, Leong JM, Woodland RT, Muramatsu M, Honjo T, Gerstein RM (2004) B1b Lymphocytes confer T cell-independent long-lasting immunity. Immunity 21:379–390.PubMedGoogle Scholar
  6. Alugupalli KR, Akira S, Lien E, Leong JM (2007) MyD88- and Bruton’s tyrosine kinase-mediated signals are essential for T cell-independent pathogen-specific IgM responses. J Immunol 178:3740–3749.PubMedGoogle Scholar
  7. Amsbaugh DF, Hansen CT, Prescott B, Stashak PW, Barthold DR, Baker PJ (1972) Genetic control of the antibody response to type 3 pneumococcal polysaccharide in mice. I. Evidence that an X-linked gene plays a decisive role in determining responsiveness. J Exp Med 136:931–949.PubMedGoogle Scholar
  8. Andersson J, Sjoberg O, Moller G (1972) Induction of immunoglobulin and antibody synthesis in vitro by lipopolysaccharides. Eur J Immunol 2:349–353.PubMedGoogle Scholar
  9. Ansel KM, Harris RB, Cyster JG (2002) CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity. Immunity 16:67–76.PubMedGoogle Scholar
  10. Arimitsu Y, Akama K (1973) Characterization of protective antibodies produced in mice infected with Borrelia duttonii. Jpn J Med Sci Biol 26:229–237.PubMedGoogle Scholar
  11. Balasz M, Martin F, Zhou T, Kearney JF (2002) Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 17:341–352.Google Scholar
  12. Barbour AG (1990) Antigenic variation of a relapsing feverBorrelia species. Annu Rev Microbiol 44:155–171.PubMedGoogle Scholar
  13. Barbour AG, Bundoc V (2001) In vitro and in vivo neutralization of the relapsing fever agentBorrelia hermsii with serotype-specific immunoglobulin M antibodies. Infect Immun 69:1009–1015.PubMedGoogle Scholar
  14. Belperron AA, Dailey CM, Bockenstedt LK (2005) Infection-induced marginal zone B cell production ofBorrelia hermsii-specific antibody is impaired in the absence of CD1d. J Immunol 174:5681–5686.PubMedGoogle Scholar
  15. Berland R, Wortis HH (2002) Origins and functions of B-1 cells with notes on the role of CD5. Annu Rev Immunol 20:253–300.PubMedGoogle Scholar
  16. Bernasconi NL, Traggiai E, Lanzavecchia A (2002) Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298:2199–2202.PubMedGoogle Scholar
  17. Boes M (2000) Role of natural and immune IgM antibodies in immune responses. Mol Immunol 37:1141–1149.PubMedGoogle Scholar
  18. Bondada S, Wu H, Robertson DA, Chelvarajan RL (2000) Accessory cell defect in unresponsiveness of neonates and aged to polysaccharide vaccines. Vaccine 19:557–565.PubMedGoogle Scholar
  19. Breukels MA, Zandvoort A, Rijkers GT, Lodewijk ME, Klok PA, Harms G, Timens W (2005) Complement dependency of splenic localization of pneumococcal polysaccharide and conjugate vaccines. Scand J Immunol 61:322–328.PubMedGoogle Scholar
  20. Briles DE, Nahm M, Schroer K, Davie J, Baker P, Kearney J, Barletta R (1981) Anti-phosphocholine antibodies found in normal mouse serum are protective against intravenous infection with type 3 Streptococcus pneumoniae. J Exp Med 153:694–705.PubMedGoogle Scholar
  21. Cabatingan MS, Schmidt MR, Sen R, Woodland RT (2002) Naive B lymphocytes undergo homeostatic proliferation in response to B cell deficit. J Immunol 169:6795–6805.PubMedGoogle Scholar
  22. Cadavid D, Thomas DD, Crawley R, Barbour AG (1994) Variability of a bacterial surface protein and disease expression in a possible mouse model of systemic Lyme borreliosis. J Exp Med 179:631–642.PubMedGoogle Scholar
  23. Carter RH, Fearon DT (1989) Polymeric C3dg primes human B lymphocytes for proliferation induced by anti-IgM. J Immunol 143:1755–1760.PubMedGoogle Scholar
  24. Carter RH, Spycher MO, Ng YC, Hoffman R, Fearon DT (1988) Synergistic interaction between complement receptor type 2 and membrane IgM on B lymphocytes. J Immunol 141:457–463.PubMedGoogle Scholar
  25. Carvalho TL, Mota-Santos T, Cumano A, Demengeot J, Vieira P (2001) Arrested B lymphopoiesis and persistence of activated B cells in adult interleukin 7–/– mice. J Exp Med 194:1141–1150.PubMedGoogle Scholar
  26. Chelvarajan RL, Gilbert NL, Bondada S (1998) Neonatal murine B lymphocytes respond to polysaccharide antigens in the presence of IL-1 and IL-6. J Immunol 161:3315–3324.PubMedGoogle Scholar
  27. Chelvarajan RL, Raithatha R, Venkataraman C, Kaul R, Han SS, Robertson DA, Bondada S (1999) CpG oligodeoxynucleotides overcome the unresponsiveness of neonatal B cells to stimulation with the thymus-independent stimuli anti-IgM and TNP-Ficoll. Eur J Immunol 29:2808–2818.PubMedGoogle Scholar
  28. Chelvarajan RL, Collins SM, Doubinskaia IE, Goes S, Van Willigen J, Flanagan D, De Villiers WJ, Bryson JS, Bondada S (2004) Defective macrophage function in neonates and its impact on unresponsiveness of neonates to polysaccharide antigens. J Leukoc Biol 75:982–994.PubMedGoogle Scholar
  29. Chelvarajan RL, Collins SM, Van Willigen JM, Bondada S (2005) The unresponsiveness of aged mice to polysaccharide antigens is a result of a defect in macrophage function. J Leukoc Biol 77:503–512.PubMedGoogle Scholar
  30. Chelvarajan RL, Liu Y, Popa D, Getchell ML, Getchell TV, Stromberg AJ, Bondada S (2006) Molecular basis of age-associated cytokine dysregulation in LPS-stimulated macrophages. J Leukoc Biol 79:1314–1327.PubMedGoogle Scholar
  31. Chinen J, Shearer WT (2002) Molecular virology and immunology of HIV infection. J Allergy Clin Immunol 110:189–198.PubMedGoogle Scholar
  32. Chong Y, Ikematsu H, Kikuchi K, Yamamoto M, Murata M, Nishimura M, Nabeshima S, Kashiwagi S, Hayashi J (2004) Selective CD27+ (memory) B cell reduction and characteristic B cell alteration in drug-naive and HAART-treated HIV type 1-infected patients. AIDS Res Hum Retroviruses 20:219–226.PubMedGoogle Scholar
  33. Connolly SE, Benach JL (2001) The spirochetemia of murine relapsing fever is cleared by complement-independent bactericidal antibodies. J Immunol 167:3029–3032.PubMedGoogle Scholar
  34. Connolly SE, Thanassi DG, Benach JL (2004) Generation of a complement-independent bactericidal IgM against a relapsing fever Borrelia. J Immunol 172:1191–1197.PubMedGoogle Scholar
  35. Corley RB, Morehouse EM, Ferguson AR (2005) IgM accelerates affinity maturation. Scand J Immunol 62 [Suppl 1]:55–61.PubMedGoogle Scholar
  36. Couderc J, Fevrier M, Duquenne C, Sourbier P, Liacopoulos P (1987) Xid mouse lymphocytes respond to TI-2 antigens when co-stimulated by TI-1 antigens or lymphokines. Immunology 61:71–76.PubMedGoogle Scholar
  37. de Vinuesa CG, Cook MC, Ball J, Drew M, Sunners Y, Cascalho M, Wabl M, Klaus GG, MacLennan IC (2000) Germinal centers without T cells. J Exp Med 191:485–494.PubMedGoogle Scholar
  38. Dullforce P, Sutton DC, Heath AW (1998) Enhancement of T cell-independent immune responses in vivo by CD40 antibodies. Nat Med 4:88–91.PubMedGoogle Scholar
  39. Ellmeier W, Jung S, Sunshine MJ, Hatam F, Xu Y, Baltimore D, Mano H, Littman DR (2000) Severe B cell deficiency in mice lacking the Tec kinase family members Tec and Btk. J Exp Med 192:1611–1624.PubMedGoogle Scholar
  40. Fagarasan S, Honjo T (2000) T-Independent immune response: new aspects of B cell biology. Science 290:89–92.PubMedGoogle Scholar
  41. Faili A, Aoufouchi S, Gueranger Q, Zober C, Leon A, Bertocci B, Weill JC, Reynaud CA (2002) AID-dependent somatic hypermutation occurs as a DNA single-strand event in the BL2 cell line. Nat Immunol 3:815–821.PubMedGoogle Scholar
  42. Fehr T, Naim HY, Bachmann MF, Ochsenbein AF, Spielhofer P, Bucher E, Hengartner H, Billeter MA, Zinkernagel RM (1998) T-cell independent IgM and enduring protective IgG antibodies induced by chimeric measles viruses. Nat Med 4:945–948.PubMedGoogle Scholar
  43. Feng SH, Stein KE (1991) VH gene family expression in mice with thexid defect. J Exp Med 174:45–51.PubMedGoogle Scholar
  44. Fikrig E, Barthold SW, Chen M, Grewal IS, Craft J, Flavell RA (1996) Protective antibodies in murine Lyme disease arise independently of CD40 ligand. J Immunol 157:1–3.PubMedGoogle Scholar
  45. Garcia-Monco JC, Miller NS, Backenson PB, Anda P, Benach JL (1997) A mouse model ofBorrelia meningitis after intradermal injection. J Infect Dis 175:1243–1245.PubMedGoogle Scholar
  46. Gebbia JA, Monco JC, Degen JL, Bugge TH, Benach JL (1999) The plasminogen activation system enhances brain and heart invasion in murine relapsing fever borreliosis. J Clin Invest 103:81–87.PubMedGoogle Scholar
  47. Guinamard R, Okigaki M, Schlessinger J, Ravetch JV (2000) Absence of marginal zone B cells in Pyk-2-deficient mice defines their role in the humoral response. Nat Immunol 1:31–36.PubMedGoogle Scholar
  48. Ha SA, Tsuji M, Suzuki K, Meek B, Yasuda N, Kaisho T, Fagarasan S (2006) Regulation of B1 cell migration by signals through Toll-like receptors. J Exp Med 203:2541–2550.PubMedGoogle Scholar
  49. Haas KM, Poe JC, Steeber DA, Tedder TF (2005) B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity 23:7–18.PubMedGoogle Scholar
  50. Hiernaux JR, Jones JM, Rudbach JA, Rollwagen F, Baker PJ (1983) Antibody response of immunodeficient (xid) CBA/N mice toEscherichia coli 0113 lipopolysaccharide, a thymus-independent antigen. J Exp Med 157:1197–1207.PubMedGoogle Scholar
  51. Hopken UE, Achtman AH, Kruger K, Lipp M (2004) Distinct and overlapping roles of CXCR5 and CCR7 in B-1 cell homing and early immunity against bacterial pathogens. J Leukoc Biol 76:709–718.PubMedGoogle Scholar
  52. Hsu MC, Toellner KM, Vinuesa CG, Maclennan IC (2006) B cell clones that sustain long-term plasmablast growth in T-independent extrafollicular antibody responses. Proc Natl Acad Sci U S A 103:5905–5910.PubMedGoogle Scholar
  53. Janeway C, Travers P, Walport M, Shlomchik M (2004) Immunobiology: The immune system in health and disease, 6th edn. Garland Publishing, New York.Google Scholar
  54. Jefferies CA, O’Neill LA (2004) Bruton’s tyrosine kinase (Btk)–the critical tyrosine kinase in LPS signalling? Immunol Lett 92:15–22.PubMedGoogle Scholar
  55. Jefferies CA, Doyle S, Brunner C, Dunne A, Brint E, Wietek C, Walch E, Wirth T, O’Neill LA (2003) Bruton’s tyrosine kinase is a Toll/interleukin-1 receptor domain-binding protein that participates in nuclear factor kappaB activation by Toll-like receptor 4. J Biol Chem 278:26258–26264.PubMedGoogle Scholar
  56. Kantor AB, Stall AM, Adams S, Watanabe K, Herzenberg LA (1995) De novo development and self-replenishment of B cells. Int Immunol 7:55–68.PubMedGoogle Scholar
  57. Kantor AB, Merrill CE, Herzenberg LA, Hillson JL (1997) An unbiased analysis of V(H)-D-J(H) sequences from B-1a B-1b, and conventional B cells. J Immunol 158:1175–1186.PubMedGoogle Scholar
  58. Kawai T, Adachi O, Ogawa T, Takeda K, Akira S (1999) Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11:115–122.PubMedGoogle Scholar
  59. Kelly DF, Moxon ER, Pollard AJ (2004)Haemophilus influenzae type b conjugate vaccines. Immunology 113:163–174.PubMedGoogle Scholar
  60. Kelly DF, Pollard AJ, Moxon ER (2005) Immunological memory: the role of B cells in long-term protection against invasive bacterial pathogens. JAMA 294:3019–3023.PubMedGoogle Scholar
  61. Khan WN, Alt FW, Gerstein RM, Malynn BA, Larsson I, Rathbun G, Davidson L, Muller S, Kantor AB, Herzenberg LA et al (1995) Defective B cell development and function in Btk-deficient mice. Immunity 3:283–299.PubMedGoogle Scholar
  62. Khan WN, Nilsson A, Mizoguchi E, Castigli E, Forsell J, Bhan AK, Geha R, Sideras P, Alt FW (1997) Impaired B cell maturation in mice lacking Bruton’s tyrosine kinase (Btk) and CD40. Int Immunol 9:395–405.PubMedGoogle Scholar
  63. Knoops L, Louahed J, Renauld JC (2004) IL-9-induced expansion of B-1b cells restores numbers but not function of B-1 lymphocytes in xid mice. J Immunol 172:6101–6106.PubMedGoogle Scholar
  64. Kruetzmann S, Manuela Rosado M, Weber H, Germing U, Tournilhac O, Peter HH, Berner R, Peters A, Boehm T, Plebani A et al (2003) Human immunoglobulin M memory B cells controllingStreptococcus pneumoniae infections are generated in the spleen. J Exp Med 197:939–945.PubMedGoogle Scholar
  65. Kurt-Jones EA, Popova L, Kwinn L, Haynes LM, Jones LP, Tripp RA, Walsh EE, Freeman MW, Golenbock DT, Anderson LJ, Finberg RW (2000) Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat Immunol 1:398–401.PubMedGoogle Scholar
  66. Landers CD, Chelvarajan RL, Bondada S (2005) The role of B cells and accessory cells in the neonatal response to TI-2 antigens. Immunol Res 31:25–36.PubMedGoogle Scholar
  67. Leadbetter EA, Rifkin IR, Hohlbaum AM, Beaudette BC, Shlomchik MJ, Marshak-Rothstein A (2002) Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416:603–607.PubMedGoogle Scholar
  68. Lesinski GB, Westerink MA (2001) Novel vaccine strategies to T-independent antigens. J Microbiol Methods 47:135–149.PubMedGoogle Scholar
  69. MacLennan IC, Garcia de Vinuesa C, Casamayor-Palleja M (2000) B-cell memory and the persistence of antibody responses. Philos Trans R Soc Lond Biol Sci 355:345–350.Google Scholar
  70. Maizels N, Bothwell A (1985) The T-cell-independent immune response to the hapten NP uses a large repertoire of heavy chain genes. Cell 43:715–720.PubMedGoogle Scholar
  71. Maizels N, Lau JC, Blier PR, Bothwell A (1988) The T-cell independent antigen NP-Ficoll, primes for a high-affinity IgM anti-NP response. Mol Immunol 25:1277–1282.PubMedGoogle Scholar
  72. Malley R, Henneke P, Morse SC, Cieslewicz MJ, Lipsitch M, Thompson CM, Kurt-Jones E, Paton JC, Wessels MR, Golenbock DT (2003) Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. Proc Natl Acad Sci U S A 100:1966–1971.PubMedGoogle Scholar
  73. Martin F, Kearney JF (2000) B-cell subsets and the mature preimmune repertoire. Marginal zone and B1 B cells as part of a “natural immune memory”. Immunol Rev 175:70–79.PubMedGoogle Scholar
  74. Martin F, Kearney JF (2001) B1 cells: similarities and differences with other B cell subsets. Curr Opin Immunol 13:195–201.PubMedGoogle Scholar
  75. 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 14:617–629.PubMedGoogle Scholar
  76. McHeyzer-Williams LJ, Driver DJ, McHeyzer-Williams MG (2001) Germinal center reaction. Curr Opin Hematol 8:52–59.PubMedGoogle Scholar
  77. McHeyzer-Williams MG (2003) B cells as effectors. Curr Opin Immunol 15:354–361.PubMedGoogle Scholar
  78. Mizuno T, Rothstein TL (2003) Cutting edge: CD40 engagement eliminates the need for Bruton’s tyrosine kinase in B cell receptor signaling for NF-kappa B. J Immunol 170:2806–2810.PubMedGoogle Scholar
  79. Mizuno T, Rothstein TL (2005) B cell receptor (BCR) cross-talk: CD40 engagement creates an alternate pathway for BCR signaling that activates I kappa B kinase/I kappa B alpha/NF-kappa B without the need for PI3 K and phospholipase C gamma. J Immunol 174:6062–6070.PubMedGoogle Scholar
  80. Montecino-Rodriguez E, Dorshkind K (2006) New perspectives in B-1 B cell development and function. Trends Immunol 27:428–433.PubMedGoogle Scholar
  81. Montecino-Rodriguez E, Leathers H, Dorshkind K (2006) Identification of a B-1 B cell-specified progenitor. Nat Immunol 7:293–301.PubMedGoogle Scholar
  82. Mosier DE, Scher I, Paul WE (1976) In vitro responses of CBA/N mice: spleen cells of mice with an X-linked defect that precludes immune responses to several thymus-independent antigens can respond to TNP-lipopolysaccharide. J Immunol 117:1363–1369.PubMedGoogle Scholar
  83. Mosier DE, Zaldivar NM, Goldings E, Mond J, Scher I, Paul WE (1977) Formation of antibody in the newborn mouse: study of T-cell-independent antibody response. J Infect Dis Suppl 136:S14–S19.PubMedGoogle Scholar
  84. Muller G, Hopken UE, Lipp M (2003) The impact of CCR7 and CXCR5 on lymphoid organ development and systemic immunity. Immunol Rev 195:117–135.PubMedGoogle Scholar
  85. Muramatsu M, Kinoshita S, Fagarasan S, Yamada Y, Shinkai Y, Honjo T (2000) Class switch recombination and hypermutation require Activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102:553–563.PubMedGoogle Scholar
  86. Nagai Y, Akashi S, Nagafuku M, Ogata M, Iwakura Y, Akira S, Kitamura T, Kosugi A, Kimoto M, Miyake K (2002) Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nat Immunol 3:667–672.PubMedGoogle Scholar
  87. Obukhanych TV, Nussenzweig MC (2006) T-independent type II immune responses generate memory B cells. J Exp Med 203:305–310.PubMedGoogle Scholar
  88. Ochsenbein AF, Pinschewer DD, Odermatt B, Carroll MC, Hengartner H, Zinkernagel RM (1999) Protective T cell-independent antiviral antibody responses are dependent on complement. J Exp Med 190:1165–1174.PubMedGoogle Scholar
  89. Pinschewer DD, Ochsenbein AF, Satterthwaite AB, Witte ON, Hengartner H, Zinkernagel RM (1999) A Btk transgene restores the antiviral TI-2 antibody responses of xid mice in a dose-dependent fashion. Eur J Immunol 29:2981–2987.PubMedGoogle Scholar
  90. Satterthwaite AB, Cheroutre H, Khan WN, Sideras P, Witte ON (1997) Btk dosage determines sensitivity to B cell antigen receptor cross-linking. Proc Natl Acad Sci U S A 94:13152–13157.PubMedGoogle Scholar
  91. Scher I, Steinberg AD, Berning AK, Paul WE (1975) X-linked B-lymphocyte immune defect in CBA/N mice. II. Studies of the mechanisms underlying the immune defect. J Exp Med 142:637–650.PubMedGoogle Scholar
  92. Schnare M, Barton GM, Holt AC, Takeda K, Akira S, Medzhitov R (2001) Toll-like receptors control activation of adaptive immune responses. Nat Immunol 2:947–950.PubMedGoogle Scholar
  93. Schroder NW, Opitz B, Lamping N, Michelsen KS, Zahringer U, Gobel UB, Schumann RR (2000) Involvement of lipopolysaccharide binding protein CD14, and Toll-like receptors in the initiation of innate immune responses by Treponema glycolipids. J Immunol 165:2683–2693.PubMedGoogle Scholar
  94. Scorpio A, Chabot DJ, Day WA, O’Brien D, K, Vietri NJ, Itoh Y, Mohamadzadeh M, Friedlander AM (2007) Poly-gamma-glutamate capsule-degrading enzyme treatment enhances phagocytosis and killing of encapsulated Bacillus anthracis. Antimicrob Agents Chemother 51:215–222.PubMedGoogle Scholar
  95. Selinka HC, Bosing-Schneider R (1988) Xid mice fail to express an anti-dextran immune response but carry alpha(1–3) dextran-specific lymphocytes in their potential repertoire. Eur J Immunol 18:1727–1732.PubMedGoogle Scholar
  96. Shang ES, Skare JT, Exner MM, Blanco DR, Kagan BL, Miller JN, Lovett MA (1998) Isolation and characterization of the outer membrane of Borrelia hermsii. Infect Immun 66:1082–1091.PubMedGoogle Scholar
  97. Snapper CM, Rosas FR, Moorman MA, Mond JJ (1997) Restoration of T cell-independent type 2 induction of Ig secretion by neonatal B cells in vitro. J Immunol 158:2731–2735.PubMedGoogle Scholar
  98. Southern PM Jr, Sanford JP (1969) Relapsing fever–a clinical and microbiological review. Medicine 48:129–149.Google Scholar
  99. Stall AM, Adams S, Herzenberg LA, Kantor AB (1992) Characteristics and development of the murine B-1b (Ly-1 B sister) cell population. Ann N Y Acad Sci 651:33–43.PubMedGoogle Scholar
  100. Szomolanyi-Tsuda E, Welsh RM (1998) T-cell-independent antiviral antibody responses. Curr Opin Immunol 10:431–435.PubMedGoogle Scholar
  101. Szomolanyi-Tsuda E, Brien JD, Dorgan JE, Garcea RL, Woodland RT, Welsh RM (2001) Antiviral T-cell-independent type 2 antibody responses induced in vivo in the absence of T and NK cells. Virology 280:160–168.PubMedGoogle Scholar
  102. Szomolanyi-Tsuda E, Seedhom MO, Carroll MC, Garcea RL (2006) T cell-independent and T cell-dependent immunoglobulin G responses to polyomavirus infection are impaired in complement receptor 2-deficient mice. Virology 352:52–60.PubMedGoogle Scholar
  103. Takeda K, Akira S (2005) Toll-like receptors in innate immunity. Int Immunol 17:1–14.PubMedGoogle Scholar
  104. Tarlinton D (2006) B-cell memory: are subsets necessary? Nat Rev Immunol 6:785–790.PubMedGoogle Scholar
  105. Thomas JD, Sideras P, Smith CIE, Vorechovsky I, Chapman V, Paul WE (1993) Colocalization of X-linked agammaglobulinemia and X-linked Immunodeficiency genes. Science 261:355–358.PubMedGoogle Scholar
  106. Toellner KM, Jenkinson WE, Taylor DR, Khan M, Sze DM, Sansom DM, Vinuesa CG, MacLennan IC (2002) Low-level hypermutation in T cell-independent germinal centers compared with high mutation rates associated with T cell-dependent germinal centers. J Exp Med 195:383–389.PubMedGoogle Scholar
  107. Tornberg UC, Holmberg D (1995) B-1a B-1b and B-2 B cells display unique VHDJH repertoires formed at different stages of ontogeny and under different selection pressures. EMBO J 14:1680–1689.PubMedGoogle Scholar
  108. Toyama H, Okada S, Hatano M, Takahashi Y, Takeda N, Ichii H, Takemori T, Kuroda Y, Tokuhisa T (2002) Memory B cells without somatic hypermutation are generated from Bcl6-deficient B cells. Immunity 17:329–339.PubMedGoogle Scholar
  109. Tung JW, Mrazek MD, Yang Y, Herzenberg LA, Herzenberg LA (2006) Phenotypically distinct B cell development pathways map to the three B cell lineages in the mouse. Proc Natl Acad Sci U S A 103:6293–6298.PubMedGoogle Scholar
  110. Vink A, Warnier G, Brombacher F, Renauld JC (1999) Interleukin 9-induced in vivo expansion of the B-1 lymphocyte population. J Exp Med 189:1413–1423.PubMedGoogle Scholar
  111. Vinuesa CG, Sunners Y, Pongracz J, Ball J, Toellner KM, Taylor D, MacLennan IC, Cook MC (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 31:1340–1350.PubMedGoogle Scholar
  112. Vos Q, Lees A, Wu Z, Snapper CM, Mond JJ (2000) B-cell activation by T-cell-independent type 2 antigens as an integral part of the humoral immune response to pathogenic microorganisms. Immunol Rev 176:154–170.PubMedGoogle Scholar
  113. Wang TT, Lucas AH (2004) The capsule ofBacillus anthracis behaves as a thymus-independent type 2 antigen. Infect Immun 72:5460–5463.PubMedGoogle Scholar
  114. Watanabe N, Ikuta K, Fagarasan S, Yazumi S, Chiba T, Honjo T (2000) Migration and differentiation of autoreactive B-1 cells induced by activated gamma/delta T cells in anti-erythrocyte immunoglobulin transgenic mice. J Exp Med 192:1577–1586.PubMedGoogle Scholar
  115. Weller S, Faili A, Garcia C, Braun MC, Le Deist FF, de Saint Basile GG, Hermine O, Fischer A, Reynaud CA, Weill JC (2001) CD40-CD40L independent Ig gene hypermutation suggests a second B cell diversification pathway in humans. Proc Natl Acad Sci U S A 98:1166–1170.PubMedGoogle Scholar
  116. Woodland RT, Schmidt MR (2005) Homeostatic proliferation of B cells. Semin Immunol 17:209–217.PubMedGoogle Scholar
  117. Woodland RT, Schmidt MR, Korsmeyer SJ, Gravel KA (1996) Regulation of B cell survival in xid mice by the proto-oncogene bcl-2. J Immunol 156:2143–2154.PubMedGoogle Scholar
  118. Yan SR, Byers DM, Bortolussi R (2004a) Role of protein tyrosine kinase p53/56lyn in diminished lipopolysaccharide priming of formylmethionylleucyl-phenylalanine-induced superoxide production in human newborn neutrophils. Infect Immun 72:6455–6462.PubMedGoogle Scholar
  119. Yan SR, Qing G, Byers DM, Stadnyk AW, Al-Hertani W, Bortolussi R (2004b) Role of MyD88 in diminished tumor necrosis factor alpha production by newborn mononuclear cells in response to lipopolysaccharide. Infect Immun 72:1223–1229.PubMedGoogle Scholar
  120. Yokota M, Morshed MG, Nakazawa T, Konishi H (1997) Protective activity ofBorrelia duttonii-specific immunoglobulin subclasses in mice. J Med Microbiol 46:675–680.PubMedGoogle Scholar
  121. Yu PW, Tabuchi RS, Kato RM, Astrakhan A, Humblet-Baron S, Kipp K, Chae K, Ellmeier W, Witte ON, Rawlings DJ (2004) Sustained correction of B-cell development and function in a murine model of X-linked agammaglobulinemia (XLA) using retroviral-mediated gene transfer. Blood 104:1281–1290.PubMedGoogle Scholar
  122. Zandvoort A, Timens W (2002) The dual function of the splenic marginal zone: essential for initiation of anti-TI-2 responses but also vital in the general first-line defense against blood-borne antigens. Clin Exp Immunol 130:4–11.PubMedGoogle Scholar
  123. Zandvoort A, Lodewijk ME, de Boer NK, Dammers PM, Kroese FG, Timens W (2001) CD27 expression in the human splenic marginal zone: the infant marginal zone is populated by naive B cells. Tissue Antigens 58:234–242.PubMedGoogle Scholar
  124. Zinkernagel RM (2000) What is missing in immunology to understand immunity? Nat Immunol 1:181–185.PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • K. R. Alugupalli
    • 1
  1. 1.Department of Microbiology and Immunology, Kimmel Cancer CenterThomas Jefferson UniversityPhiladelphiaUSA

Personalised recommendations