Peritoneal B-cell subsets in the genus Mus: Their role in innate immunity

Critical Reviews in Immunology

Volumn 28, Issue 4, 2008, Pages 341-361

  Thiriot, Aude ^a   Freitas, Antonio A ^a   Rueff Juy, Dominique ^a,b  

^a CNRS   (France)

^b INSTITUT PASTEUR   (France)

Author keywords

B cells; Innate immunity; Wild derived mouse strains

Indexed keywords

ANTIBODY; AUTOANTIBODY;

B LYMPHOCYTE; CELL POPULATION; EXPERIMENTAL MOUSE; IMMUNE SYSTEM; INNATE IMMUNITY; MEMORY CELL; MOUSE STRAIN; NONHUMAN; PERITONEUM CELL; PHENOTYPE; PRIORITY JOURNAL; REVIEW;

EID: 55349111133     PISSN: 10408401     EISSN: None     Source Type: Journal    
DOI: 10.1615/critrevimmunol.v28.i4.50     Document Type: Review

References (128)

1. Mestas J, Hughes CC. Of mice and not men: differences between mouse and human immunology. J Immunol. 2004;172:2731-8.
2. Payne KJ, Crooks GM. Immune-cell lineage commitment: translation from mice to humans. Immunity. 2007;26:674-7.
3. Guenet JL, Bonhomme F. Wild mice: an ever-increasing contribution to a popular mammalian model. Trends Genet. 2003;19:24-31.
4. Petkov PM, Ding Y, Cassell MA, Zhang W, Wagner G, Sargent EE, Asquith S, Crew V, Johnson KA, Robinson P, Scott VE, Wiles MV. An efficient SNP system for mouse genome scanning and elucidating strain relationships. Genome Res. 2004;14:1806-11.
5. Thiriot A, Drapier AM, Vieira P, Fitting C, Cavaillon JM, Cazenave PA, Rueff-Juy D. The Bw cells, a novel B cell population conserved in the whole genus Mus. J Immunol. 2007;179:6568-78.
6. Guenet JL, Bonhomme F. Origin of the laboratory mouse and related species. Chap 1. St. Louis (MO): Elsevier; 2004. p. 3-15.
7. Wade CM, Daly MJ. Genetic variation in laboratory mice. Nat Genet. 2005;37:1175-80.
8. Yang H, Bell TA, Churchill GA, Pardo-Manuel de Villena F. On the subspecific origin of the laboratory mouse. Nat Genet. 2007;39:1100-7.
9. Frazer KA, Eskin E, Kang HM, Bogue MA, Hinds DA, Beilharz EJ, Gupta RV, Montgomery J, Morenzoni MM, Nilsen GB, Pethiyagoda CL, Stuve LL, Johnson FM, Daly MJ, Wade CM, Cox DR. A sequence-based variation map of 8.27 million SNPs in inbred mouse strains. Nature. 2007;448:1050-3.
10. Ferris SD, Sage RD, Prager EM, Ritte U, Wilson AC. Mitochondrial DNA evolution in mice. Genetics. 1983;105:681-721.
11. Bishop CE, Boursot P, Baron B, Bonhomme F, Hatat D. Most classical Mus musculus domesticus laboratory mouse strains carry a Mus musculus musculus Y chromosome. Nature. 1985;315:70-2.
12. Potter M. Listing of stocks and strains of mice in the genus Mus derived from the feral state. Curr Top Microbiol Immunol. 1986;127:374-95.
13. Jouvin-Marche E, Morgado MG, Leguern C, Voegtle D, Bonhomme F, Cazenave PA. The mouse Igh-1a and Igh-1b H chain constant regions are derived from two distinct isotypic genes. Immunogenetics. 1989;29:92-7.
14. Sangster MY, Mackenzie JS, Shellam GR. Genetically determined resistance to flavivirus infection in wild Mus musculus domesticus and other taxonomic groups in the genus Mus. Arch Virol. 1998;143:697-715.
15. Sebastiani G, Blais V, Sancho V, Vogel SN, Stevenson MM, Gros P, Lapointe J M, Rivest S, Malo D. Host immune response to Salmonella enterica serovar Typhimurium infection in mice derived from wild strains. Infect Immun. 2002;70:1997-2009.
16. Turcotte K, Loredo-Osti JC, Fortin P, Schurr E, Morgan K, Gros P. Complex genetic control of susceptibility to Mycobacterium bovis (Bacille Calmette-Guerin) infection in wild-derived Mus spretus mice. Genes Immunol. 2006;7:684-7.
17. Bagot S, Campino S, Penha-Goncalves C, Pied S, Cazenave PA, Holmberg D. Identification of two cerebral malaria resistance loci using an inbred wild-derived mouse strain. Proc Natl Acad Sci U S A. 2002;99:9919-23.
18. Campino S, Bagot S, Bergman ML, Almeida P, Sepulveda N, Pied S, Penha-Goncalves C, Holmberg D, Cazenave PA. Genetic control of parasite clearance leads to resistance to Plasmodium berghei ANKA infection and confers immunity. Genes Immunol. 2005;6:416-21.
19. Conner JR, Smirnova II, Poltorak A. Forward genetic analysis of Toll-like receptor responses in wild-derived mice reveals a novel antiinflammatory role for IRAK1BP1. J Exp Med. 2008;205:305-14.
20. Staelens J, Wielockx B, Puimege L, Van Roy F, Guenet JL, Libert C. Hyporesponsiveness of SPRET/Ei mice to lethal shock induced by tumor necrosis factor and implications for a TNF-based antitumor therapy. Proc Natl Acad Sci U S A. 2002;99:9340-5.
21. Melanitou E, Joly F, Lathrop M, Boitard C, Avner P. Evidence for the presence of insulin-dependent diabetes-associated alleles on the distal part of mouse chromosome 6. Genome Res. 1998;8:608-20.
22. Juy D, Drapier AM, Guenet JL, Cazenave PA. Idiotypic characteristics of lambda 1-bearing anti-alpha(1-3)dextran response in wild mice: high frequency of responder strains and co-expression of IdI 558 and IdI 104 on the same molecule. Eur J Immunol. 1987;17:1757-62.
23. Cazenave PA, Marche PN, Jouvin-Marche E, Voegtle D, Bonhomme F, Bandeira A, Coutinho A. 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. 1990;63:717-28.
24. Rueff-Juy D, Marche PN, Drapier AM, Cazenave P-A. Junctional diversity of H and L chains allows the coexpression of two mutually exclusive idiotopes (IdI104 and IdI558). J Immunol. 1991;146:4024-30.
25. Thiriot A, Drapier AM, Mémet S, Fitting C, Sturny-Leclere A, Cavaillon JM, Cazenave PA, Freitas AA, Rueff-Juy D. Wild-derived mouse strains, a valuable model to study B cell responses. Mol Immunol. In press 2008.
26. Heinzel FP, Sadick MD, Holaday BJ, Coffman RL, Locksley RM. Reciprocal expression of interferon gamma or interleukin 4 during the resolution or progression of murine leishmaniasis. Evidence for expansion of distinct helper T cell subsets. J Exp Med. 1989;169:59-72.
27. Babay BE, Louzir H, Kebaier C, Boubaker S, Dellagi K, Cazenave PA. Inbred strains derived from feral mice reveal new pathogenic mechanisms of experimental leishmaniasis due to Leishmania major. Infect Immun. 2004;72:4603-11.
28. Burgio G, Szatanik M, Guenet JL, Arnau MR, Panthier JJ, Montagutelli X. Interspecific re-combinant congenic strains between C57BL/6 and mice of the Mus spretus species: a powerful tool to dissect genetic control of complex traits. Genetics. 2007;177:2321-33.
29. Martin F, Kearney JF. CD21high IgMhigh splenic B cells enriched in the marginal zone: distinct phenotypes and functions. Curr Top Microbiol Immunol. 1999;246:45-50.
30. Stall AM, Adams S, Herzenberg LA, Kantor AB. Characteristics and development of the murine B-1b (Ly-1 B sister) cell population. Ann N Y Acad Sci. 1992;651:33-43.
31. Cariappa A, Boboila C, Moran ST, Liu H, Shi HN, Pillai S. The recirculating B cell pool contains two functionally distinct, long-lived, posttransitional, follicular B cell populations. J Immunol. 2007;179:2270-81.
32. Cariappa A, Mazo IB, Chase C, Shi HN, Liu H, Li Q, Rose H, Leung H, Cherayil BJ, Russell P, von Andrian U, Pillai S. Perisinusoidal B cells in the bone marrow participate in T-independent responses to blood-borne microbes. Immunity. 2005;23:397-407.
33. Allman D, Pillai S. Peripheral B cell subsets. Curr Opin Immunol. 2008;20:149-57.
34. Gray D, MacLennan IC, Bazin H, Khan M. Migrant mu+ delta+ and static mu+ delta- B lymphocyte subsets. Eur J Immunol. 1982;12:564-9.
35. Martin F, Kearney JF. B-cell subsets and the mature preimmune repertoire. Marginal zone and B1 B cells as part of a "natural immune memory." Immunol Rev. 2000;175:70-9.
36. Weller S, Braun MC, Casanova JL, Reynaud CA, Weill JC. Human blood IgM "memory" B cells are circulating splenic marginal zone B cells harboring a pre-diversified immunoglobulin repertoire. Blood. 2004;104:3647-54.
37. Oliver AM, Martin F, Kearney JF. IgMhigh CD21high lymphocytes enriched in the splenic marginal zone generate effector cells more rapidly than the bulk of follicular B cells. J Immunol. 1999;162:7198-207.
38. Weller S, Reynaud CA, Weill JC. Vaccination against encapsulated bacteria in humans: paradoxes. Trends Immunol. 2005;26:85-9.
39. Loder F, Mutschler B, Ray RJ, Paige CJ, Sideras P, Torres R, Lamers MC, Carsetti R. B cell development in the spleen takes place in discrete steps and is determined by the quality of B cell receptor-derived signals. J Exp Med. 1999;190:75-89.
40. Allman D, Lindsley RC, DeMuth W, Rudd K, Shinton SA, Hardy RR. Resolution of three nonproliferative immature splenic B cell subsets reveals multiple selection points during peripheral B cell maturation. J Immunol. 2001;167:6834-40.
41. Merrell KT, Benschop RJ, Gauld SB, Aviszus K, Decote-Ricardo D, Wysocki LJ, Cambier JC. Identification of anergic B cells within a wild-type repertoire. Immunity. 2006;25:953-62.
42. Hayakawa K, Hardy RR, Herzenberg LA. Peritoneal Ly-1 B cells: genetic control, autoantibody production, increased lambda light chain expression. Eur J Immunol. 1986;16:450-6.
43. Hayakawa K, Hardy RR, Parks DR, Herzenberg LA. The "Ly-1 B" cell subpopulation in normal immunodefective, and autoimmune mice. J Exp Med. 1983;157:202-18.
44. Cong YZ, Rabin E, Wortis HH. Treatment of murine CD5- B cells with anti-Ig, but not LPS, induces surface CD5: two B-cell activation pathways. Int Immunol. 1991;3:467-76.
45. Hillion S, Saraux A, Youinou P, Jamin C. Expression of RAGs in peripheral B cells outside germinal centers is associated with the expression of CD5. J Immunol. 2005;174:5553-61.
46. Martin F, Oliver AM, Kearney JF. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity. 2001;14:617-29.
47. Baumgarth N, Tung JW, Herzenberg LA. Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion. Springer Semin Immunopathol. 2005;26:347-62.
48. Carsetti R, Rosado MM, Wardmann H. Peripheral development of B cells in mouse and man. Immunol Rev. 2004;197:179-91.
49. Haas KM, Poe JC, Steeber DA, Tedder TF. B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity. 2005;23:7-18.
50. Alugupalli KR, Leong JM, Woodland RT, Muramatsu M, Honjo T, Gerstein RM. B1b lymphocytes confer T cell-independent long-lasting immunity. Immunity. 2004;21:379-90.
51. Khan WN, Alt FW, Gerstein RM, Malynn BA, Larsson I, Rathbun G, Davidson L, Muller S, Kantor AB, Herzenberg LA. Defective B cell development and function in Btk-deficient mice. Immunity. 1995;3:283-99.
52. Berland R, Wortis HH. Origins and functions of B-1 cells with notes on the role of CD5. Annu Rev Immunol. 2002;20:253-300.
53. Berberich S, Dahne S, Schippers A, Peters T, Muller W, Kremmer E, Forster R, Pabst O. Differential molecular and anatomical basis for B cell migration into the peritoneal cavity and omental milky spots. J Immunol. 2008;180:2196-203.
54. Nisitani S, Murakami M, Akamizu T, Okino T, Ohmori K, Mori T, Imamura M, Honjo T. Preferential localization of human CD5+ B cells in the peritoneal cavity. Scand J Immunol. 1997;46:541-5.
55. Tumang JR, Hastings WD, Bai C, Rothstein TL. Peritoneal and splenic B-1 cells are separable by phenotypic, functional, and transcriptomic characteristics. Eur J Immunol. 2004;34:2158-67.
56. Kretschmer K, Jungebloud A, Stopkowicz J, Stoermann B, Hoffmann R, Weiss S. Antibody repertoire and gene expression profile: implications for different developmental and functional traits of splenic and peritoneal B-1 lymphocytes. J Immunol. 2003;171:1192-201.
57. Kerfoot SM, Szczepanik M, Tung JW, Askenase PW. Identification of initiator B cells, a novel subset of activation-induced deaminase-dependent B-1-like cells that mediate initiation of contact sensitivity. J Immunol. 2008;181:1717-27.
58. Yang Y, Tung JW, Ghosn EE, Herzenberg LA, Herzenberg LA. Division and differentiation of natural antibody-producing cells in mouse spleen. Proc Natl Acad Sci U S A. 2007;104:4542-6.
59. Balabanian K, Foussat A, Bouchet-Delbos L, Couderc J, Krzysiek R, Amara A, Baleux F, Portier A, Galanaud P, Emilie D. Interleukin-10 modulates the sensitivity of peritoneal B lymphocytes to chemokines with opposite effects on stromal cell-derived factor-1 and B-lymphocyte chemoattractant. Blood. 2002;99:427-36.
60. Cyster JG. Chemokines, sphingosine-1-phosphate, and cell migration in secondary lymphoid organs. Annu Rev Immunol. 2005;23:127-59.
61. Berberich S, Forster R, Pabst O. The peritoneal micromilieu commits B cells to home to body cavities and the small intestine. Blood. 2007;109:4627-34.
62. Ansel KM, Harris RB, Cyster JG. CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity. Immunity. 2002;16:67-76.
63. Hastings WD, Tumang JR, Behrens TW, Rothstein TL. Peritoneal B-2 cells comprise a distinct B-2 cell population with B-1b-like characteristics. Eur J Immunol. 2006;36:1114-23.
64. Kantor AB, Merrill CE, Herzenberg LA, Hillson JL. An unbiased analysis of V(H)-D-J(H) sequences from B-1a, B-1b, and conventional B cells. J Immunol. 1997;158:1175-86.
65. Kantor AB, Stall AM, Adams S, Herzenberg LA. Differential development of progenitor activity for three B-cell lineages. Proc Natl Acad Sci U S A. 1992;89:3320-4.
66. Herzenberg LA. B-1 cells: the lineage question revisited. Immunol Rev. 2000;175:9-22.
67. Chumley MJ, Dal Porto JM, Kawaguchi S, Cambier JC, Nemazee D, Hardy RR. A VH11V kappa 9 B cell antigen receptor drives generation of CD5+ B cells both in vivo and in vitro. J Immunol. 2000;164:4586-93.
68. Montecino-Rodriguez E, Leathers H, Dorshkind K. Identification of a B-1 B cell-specified progenitor. Nat Immunol. 2006;7:293-301.
69. Tung JW, Mrazek MD, Yang Y, Herzenberg LA. Phenotypically distinct B cell development pathways map to the three B cell lineages in the mouse. Proc Natl Acad Sci U S A. 2006;103:6293-8.
70. Tung JW, Herzenberg LA. Unraveling B-1 progenitors. Curr Opin Immunol. 2007;19:150-5.
71. Montecino-Rodriguez E, Dorshkind K. New perspectives in B-1 B cell development and function. Trends Immunol. 2006;27:428-33.
72. Rothstein TL. Cutting edge commentary: two B-1 or not to be one. J Immunol. 2002;168:4257-61.
73. Ishida H, Hastings R, Kearney J, Howard M. Continuous anti-interleukin 10 antibody administration depletes mice of Ly-1 B cells but not conventional B cells. J Exp Med. 1992;175:1213-20.
74. Berland R, Wortis HH. Normal B-1a cell development requires B cell-intrinsic NFATc1 activity. Proc Natl Acad Sci U S A. 2003;100:13459-64.
75. Ye M, Ermakova O, Graf T. PU.1 is not strictly required for B cell development and its absence induces a B-2 to B-1 cell switch. J Exp Med. 2005;202:1411-22.
76. Lopes-Carvalho T, Kearney JF. Development and selection of marginal zone B cells. Immunol Rev. 2004;197:192-205.
77. Hayakawa K, Hardy RR. Development and function of B-1 cells. Curr Opin Immunol. 2000;12:346-53.
78. -/- mice. J Exp Med. 2001;194:1141-50.
79. O'Garra A, Chang R, Go N, Hastings R, Haughton G, Howard M. Ly-1 B (B-1) cells are the main source of B cell-derived interleukin 10. Eur J Immunol. 1992;22:711-7.
80. Genestier L, Taillardet M, Mondiere P, Gheit H, Bella C, Defrance T. TLR agonists selectively promote terminal plasma cell differentiation of B cell subsets specialized in thymus-independent responses. J Immunol. 2007;178:7779-86.
81. Amsbaugh DF, Hansen CT, Prescott B, Stashak PW, Barthold DR, Baker PJ. 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. 1972;136:931-49.
82. Briles DE, Nahm M, Schroer K, Davie J, Baker P, Kearney J, Barletta R. Antiphosphocholine antibodies found in normal mouse serum are protective against intravenous infection with type 3 streptococcus pneumoniae. J Exp Med. 1981;153:694-705.
83. Quintans J, Quan ZS, Arias MA. Mice with the xid defect have helper cells for T15 idiotypedominant anti-phosphorylcholine primary and secondary plaque-forming cell responses. J Exp Med. 1982;155:1245-50.
84. Caroff M, Karibian D, Cavaillon JM, Haeffner-Cavaillon N. Structural and functional analyses of bacterial lipopolysaccharides. Microbes Infect. 2002;4:915-26.
85. Chang MK, Bergmark C, Laurila A, Horkko S, Han KH, Friedman P, Dennis EA, Witztum JL. Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: evidence that oxidation-specific epitopes mediate macrophage recognition. Proc Natl Acad Sci U S A. 1999;96:6353-8.
86. Garcia de Vinuesa C, O'Leary P, Sze DM, Toellner KM, MacLennan IC. T-independent type 2 antigens induce B cell proliferation in multiple splenic sites, but exponential growth is confined to extrafollicular foci. Eur J Immunol. 1999;29:1314-23.
87. Snapper CM, Shen Y, Khan AQ, Colino J, Zelazowski P, Mond JJ, Gause WC, Wu ZQ. Distinct types of T-cell help for the induction of a humoral immune response to Streptococcus pneumoniae. Trends Immunol. 2001;22:308-11.
88. Sen G, Khan AQ, Chen Q, Snapper CM. In vivo humoral immune responses to isolated pneumococcal polysaccharides are dependent on the presence of associated TLR ligands. J Immunol. 2005;175:3084-91.
89. Masmoudi H, Mota-Santos T, Huetz F, Coutinho A, Cazenave P-A. All T15 Id-positive antibodies (but not the majority of VHT15+ antibodies) are produced by peritoneal CD5+ B lymphocytes. Intern Immunol. 1990;2:515-20.
90. Claflin LJ, Lieberman R, Davie JM. Clonal nature of immune response to phosphorylcholine. I. Specificity, class and idiotope of phosphorylcholine- binding receptors on lymphoid cells. J Exp Med. 1974;139:58-68.
91. Kroese FG, Butcher EC, Stall AM, Lalor PA, Adams S, Herzenberg LA. Many of the IgA producing plasma cells in murine gut are derived from self-replenishing precursors in the peritoneal cavity. Int Immunol. 1989;1:75-84.
92. Stoel M, Jiang HQ, van Diemen CC, Bun JC, Dammers PM, Thurnheer MC, Kroese FG, Cebra JJ, Bos NA. Restricted IgA repertoire in both B-1 and B-2 cell-derived gut plasmablasts. J Immunol. 2005;174:1046-54.
93. Bos NA, Cebra JJ, Kroese FG. B-1 cells and the intestinal microflora. Curr Top Microbiol Immunol. 2000;252:211-20.
94. Macpherson AJ, Hunziker L, McCoy K, Lamarre A. IgA responses in the intestinal mucosa against pathogenic and non-pathogenic microorganisms. Microbes Infect. 2001;3:1021-35.
95. Jerne NK. The somatic generation of immune recognition. Eur J Immunol. 1971;1:1-9.
96. Jerne NK, Roland J, Cazenave PA. Recurrent idiotopes and internal images. EMBO J. 1982;1:243-7.
97. von Boehmer H, Aifantis I, Gounari F, Azogui O, Haughn L, Apostolou I, Jaeckel E, Grassi F, Klein L. Thymic selection revisited: how essential is it? Immunol Rev. 2003;191:62-78.
98. Janeway CA Jr. How the immune system works to protect the host from infection: a personal view. Proc Natl Acad Sci U S A. 2001;98:7461-8.
99. Avrameas S. Natural autoantibodies: from 'horror autotoxicus' to 'gnothi seauton.' Immunol Today. 1991;12:154-9.
100. Coutinho A, Kazatchkine MD, Avrameas S. Natural autoantibodies. Curr Opin Immunol. 1995;7:812-8.
101. Hayakawa K, Hardy RR, Honda M, Herzenberg LA, Steinberg AD. Ly-1 B cells: functionally distinct lymphocytes that secrete IgM autoantibodies. Proc Natl Acad Sci U S A. 1984;81:2494-8.
102. Baumgarth N, Herman OC, Jager GC, Brown LE, Herzenberg LA, Chen J. B-1 and B-2 cell-derived immunoglobulin M antibodies are nonredundant components of the protective response to influenza virus infection. J Exp Med. 2000;192:271-80.
103. Hardy RR. B-1 B cells: development, selection, natural autoantibody and leukemia. Curr Opin Immunol. 2006;18:547-55.
104. Freitas AA, Viale AC, Sundblad A, Heusser C, Coutinho A. Normal serum immunoglobulins participate in the selection of peripheral B-cell repertoires. Proc Natl Acad Sci U S A. 1991;88:5640-4.
105. Baker N, Ehrenstein MR. Cutting edge: selection of B lymphocyte subsets is regulated by natural IgM. J Immunol. 2002;169:6686-90.
106. Nobrega A, Haury M, Grandien A, Malanchere E, Sundblad A, Coutinho A. Global analysis of antibody repertoires. II. Evidence for specificity, self-selection and the immunological "homunculus" of antibodies in normal serum. Eur J Immunol. 1993;23:2851-9.
107. Ochsenbein AF, Zinkernagel RM. Natural antibodies and complement link innate and acquired immunity. Immunol Today. 2000;21:624-30.
108. Ochsenbein AF, Fehr T, Lutz C, Suter M, Brombacher F, Hengartner H, Zinkernagel RM. Control of early viral and bacterial distribution and disease by natural antibodies. Science. 1999;286:2156-9.
109. Kearney JF. Innate-like B cells. Springer Semin Immunopathol. 2005;26:377-83.
110. Binder CJ, Horkko S, Dewan A, Chang MK, Kieu EP, Goodyear CS, Shaw PX, Palinski W, Witztum JL, Silverman GJ. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat Med. 2003;9:736-43.
111. Binder CJ, Silverman GJ. Natural antibodies and the autoimmunity of atherosclerosis. Springer Semin Immunopathol. 2005;26:385-404.
112. Bendelac A, Bonneville M, Kearney JF. Autoreactivity by design: innate B and T lymphocytes. Nat Rev Immunol. 2001;1:177-86.
113. Casola S, Otipoby KL, Alimzhanov M, Humme S, Uyttersprot N, Kutok JL, Carroll MC, Rajewsky K. B cell receptor signal strength determines B cell fate. Nat Immunol. 2004;5:317-27.
114. Hardy RR. B-1 B cell development. J Immunol. 2006;177:2749-54.
115. Pillai S, Cariappa A, Moran ST. Positive selection and lineage commitment during peripheral B-lymphocyte development. Immunol Rev. 2004;197:206-18.
116. Chen X, Martin F, Forbush KA, Perlmutter RM, Kearney JF. Evidence for selection of a population of multi-reactive B cells into the splenic marginal zone. Int Immunol. 1997;9:27-41.
117. Shaw PX, Goodyear CS, Chang MK, Witztum JL, Silverman GJ. The autoreactivity of antiphosphorylcholine antibodies for atherosclerosis- associated neo-antigens and apoptotic cells. J Immunol. 2003;170:6151-7.
118. Monafo WJ, Greenspan NS, Cebra-Thomas JA, Davie JM. Modulation of the murine immune response to streptococcal group A carbohydrate by immunization with monoclonal anti-idiotope. J Immunol. 1987;139:2702-7.
119. Gaudin E, Hao Y, Rosado MM, Chaby R, Girard R, Freitas AA. Positive selection of B cells expressing low densities of self-reactive BCRs. J Exp Med. 2004;199:843-53.
120. McHeyzer-Williams LJ, McHeyzer-Williams MG. Antigen-specific memory B cell development. Annu Rev Immunol. 2005;23:487-513.
121. Guigou V, Guilbert B, Moinier D, Tonnelle C, Boubli L, Avrameas S, Fougereau M, Fumoux F. Ig repertoire of human polyspecific antibodies and B cell ontogeny. J Immunol. 1991;146:1368-74.
122. Merbl Y, Zucker-Toledano M, Quintana FJ, Cohen IR. Newborn humans manifest autoantibodies to defined self molecules detected by antigen microarray informatics. J Clin Invest. 2007;117:712-8.
123. Cohen IR. Biomarkers, self-antigens and the immunological homunculus. J Autoimmun. 2007;29:246-9.
124. Kasaian MT, Ikematsu H, Casali P. Identification and analysis of a novel human surface CD5-B lymphocyte subset producing natural antibodies. J Immunol. 1992;148:2690-702.
125. Martin M, Strasser A, Baumgarth N, Cicuttini FM, Welch K, Salvaris E, Boyd AW. A novel cellular model (SPGM 1) of switching between the pre-B cell and myelomonocytic lineages. J Immunol. 1993;150:4395-406.
126. Cumano A, Paige CJ, Iscove NN, Brady G. Bipotential precursors of B cells and macrophages in murine fetal liver. Nature. 1992;356:612-5.
127. Montecino-Rodriguez E, Leathers H, Dorshkind K. Bipotential B-macrophage progenitors are present in adult bone marrow. Nat Immunol. 2001;2:83-8.
128. Li J, Barreda DR, Zhang YA, Boshra H, Gelman AE, Lapatra S, Tort L, Sunyer JO. B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat Immunol. 2006;7:1116-24.