Natural and induced B-1 cell immunity to infections raises questions of nature versus nurture

Annals of the New York Academy of Sciences

Volumn 1362, Issue 1, 2015, Pages 188-199

  Baumgarth, Nicole ^a   Waffarn, Elizabeth E ^a   Nguyen, Trang T T ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

B cell subsets; IgM; Influenza virus infections; Natural antibodies

Indexed keywords

IMMUNOGLOBULIN M;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BONE MARROW; CELL MATURATION; CELLULAR IMMUNITY; CONTROLLED STUDY; FEMALE; INFECTION; LYMPHOCYTE SUBPOPULATION; LYMPHOID TISSUE; MALE; MOUSE; NATURAL SCIENCE; NONHUMAN; PERITONEAL CAVITY; SPLEEN LYMPHOCYTE; 129 MOUSE; ANIMAL; BONE MARROW CELL; C57BL MOUSE; COMMUNICABLE DISEASE; CYTOLOGY; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; SPLEEN;

ANIMALS; B-LYMPHOCYTE SUBSETS; BONE MARROW CELLS; COMMUNICABLE DISEASES; FEMALE; IMMUNITY, CELLULAR; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; SPLEEN;

EID: 84959473198     PISSN: 00778923     EISSN: 17496632     Source Type: Journal    
DOI: 10.1111/nyas.12804     Document Type: Article

References (73)

1. Baumgarth, N. 2011. The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat. Rev. Immunol. 11: 34-46.
2. Berland, R. & H.H. Wortis. 2002. Origins and functions of B-1 cells with notes on the role of CD5. Annu. Rev. Immunol. 20: 253-300.
3. Hooijkaas, H., R. Benner, J. Pleasants & B. Wostmann. 1984. Isotypes and specificities of immunoglobulins produced by germ-free mice fed chemically defined ultrafiltered "antigen-free" diet. Eur. J. Immunol. 14: 1127-1130.
4. Alugupalli, K.R. et al. 2004. B1b lymphocytes confer T cell-independent long-lasting immunity. Immunity 21: 379-390.
5. Baumgarth, N., J. Chen, O.C. Herman, et al. 2000. The role of B-1 and B-2 cells in immune protection from influenza virus infection. Curr. Top Microbiol. Immunol. 252: 163-169.
6. Ochsenbein, A.F. et al. 1999. Control of early viral and bacterial distribution and disease by natural antibodies. Science 286: 2156-2159.
7. Ehrenstein, M.R. & C.A. Notley. 2010. The importance of natural IgM: scavenger, protector and regulator. Nat. Rev. Immunol. 10: 778-786.
8. Silverman, G.J., C. Gronwall, J. Vas & Y. Chen. 2009. Natural autoantibodies to apoptotic cell membranes regulate fundamental innate immune functions and suppress inflammation. Discov. Med. 8: 151-156.
9. Fahey, J.L. & S. Sell. 1965. The immunoglobulins of mice. V. The metabolic (catabolic) properties of five immunoglobulin classes. J. Exp. Med. 122: 41-58.
10. Nisitani, S., T. Tsubata, M. Murakami & T. Honjo. 1995. Administration of interleukin-5 or -10 activates peritoneal B-1 cells and induces autoimmune hemolytic anemia in anti-erythrocyte autoantibody-transgenic mice. Eur. J. Immunol. 25: 3047-3052.
11. Kawahara, T., H. Ohdan, G. Zhao, Y.G. Yang & M. Sykes. 2003. Peritoneal cavity B cells are precursors of splenic IgM natural antibody-producing cells. J. Immunol. 171: 5406-5414.
12. Ha, S.A. et al. 2006. Regulation of B1 cell migration by signals through Toll-like receptors. J. Exp. Med. 203: 2541-2550.
13. Haas, K.M., J.C. Poe, D.A. Steeber & T.F. Tedder. 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.
14. Alugupalli, K.R. et al. 2003. The resolution of relapsing fever borreliosis requires IgM and is concurrent with expansion of B1b lymphocytes. J. Immunol. 170: 3819-3827.
15. Cole, L.E. et al. 2009. Antigen-specific B-1a antibodies induced by Francisella tularensis LPS provide long-term protection against F. tularensis LVS challenge. Proc. Natl. Acad. Sci. U.S.A. 106: 4343-4348.
16. Choi, Y.S. & N. Baumgarth. 2008. Dual role for B-1a cells in immunity to influenza virus infection. J. Exp. Med. 205: 3053-3064.
17. Baumgarth, N., O.C. Herman, G.C. Jager, L. Brown & L.A. Herzenberg. 1999. Innate and acquired humoral immunities to influenza virus are mediated by distinct arms of the immune system. Proc. Natl. Acad. Sci. U.S.A. 96: 2250-2255.
18. Choi, Y.S., J.A. Dieter, K. Rothaeusler, Z. Luo & N. Baumgarth. 2012. B-1 cells in the bone marrow are a significant source of natural IgM. Eur. J. Immunol. 42: 120-129.
19. Kroese, F.G. et al. 1989. Many of the IgA producing plasma cells in murine gut are derived from self-replenishing precursors in the peritoneal cavity. Int. Immunol. 1: 75-84.
20. Rosado, M.M. et al. 2009. From the fetal liver to spleen and gut: the highway to natural antibody. Mucosal. Immunol. 2: 351-361.
21. Tung, J.W., D.R. Parks, W.A. Moore, L.A. Herzenberg & L.A. Herzenberg. 2004. Identification of B-cell subsets: an exposition of 11-color (Hi-D) FACS methods. Methods Mol. Biol. 271: 37-58.
22. Gil-Cruz, C. et al. 2009. The porin OmpD from nontyphoidal Salmonella is a key target for a protective B1b cell antibody response. Proc. Natl. Acad. Sci. U.S.A. 106: 9803-9808.
23. Yang, Y., J.W. Tung, E.E. Ghosn & L.A. Herzenberg. 2007. Division and differentiation of natural antibody-producing cells in mouse spleen. Proc. Natl. Acad. Sci. U.S.A. 104: 4542-4546.
24. Jacobson, A.C., K.M. Roundy, J.J. Weis & J.H. Weis. 2009. Regulation of murine splenic B cell CR3 expression by complement component 3. J. Immunol. 183: 3963-3970.
25. Abram, C.L. & C.A. Lowell. 2009. The ins and outs of leukocyte integrin signaling. Annu. Rev. Immunol. 27: 339-362.
26. Ansel, K.M., R.B. Harris & J.G. Cyster. 2002. CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity. Immunity 16: 67-76.
27. Watanabe, N. et al. 2000. Migration and differentiation of autoreactive B-1 cells induced by activated gamma/delta T cells in antierythrocyte immunoglobulin transgenic mice. J. Exp. Med. 192: 1577-1586.
28. + B cells. J. Immunol. 144: 4520-4525.
29. Kretschmer, K. et al. 2003. Antibody repertoire and gene expression profile: implications for different developmental and functional traits of splenic and peritoneal B-1 lymphocytes. J. Immunol. 171: 1192-1201.
30. Stoermann, B., K. Kretschmer, S. Duber, & S. Weiss. 2007. B-1a cells are imprinted by the microenvironment in spleen and peritoneum. Eur. J. Immunol. 37: 1613-1620.
31. Hayakawa, K., R.R. Hardy, D.R. Parks, & L.A. Herzenberg. 1983. The "Ly-1 B" cell subpopulation in normal immunodefective, and autoimmune mice. J. Exp. Med. 157: 202-218.
32. Hayakawa, K., R.R. Hardy, & L.A. Herzenberg. 1985. Progenitors for Ly-1 B cells are distinct from progenitors for other B cells. J. Exp. Med. 161: 1554-1568.
33. Lalor, P.A., L.A. Herzenberg, S. Adams, & A.M. Stall. 1989. Feedback regulation of murine Ly-1 B cell development. Eur. J. Immunol. 19: 507-513.
34. Lalor, P.A., A.M. Stall, S. Adams, & L.A. Herzenberg. 1989. Permanent alteration of the murine Ly-1 B repertoire due to selective depletion of Ly-1 B cells in neonatal animals. Eur. J. Immunol. 19: 501-506.
35. Stall, A.M., S.M. Wells, & K.P. Lam. 1996. B-1 cells: unique origins and functions. Semin. Immunol. 8: 45-59.
36. VanOudenaren, A., J.J. Haaijman, & R. Benner. 1984. Frequencies of background cytoplasmic Ig-containing cells in various lymphoid organs of athymic and euthymic mice as a function of age and immune status. Immunology 51: 735-742.
37. Murakami, M. et al. 1994. Oral administration of lipopolysaccharides activates B-1 cells in the peritoneal cavity and lamina propria of the gut and induces autoimmune symptoms in an autoantibody transgenic mouse. J. Exp. Med. 180: 111-121.
38. Ohdan, H. et al. 2000. Mac-1-negative B-1b phenotype of natural antibody-producing cells, including those responding to Gal alpha 1, 3Gal epitopes in alpha 1, 3-galactosyltransferase-deficient mice. J. Immunol. 165: 5518-5529.
39. +) B cells. Activated peritoneal macrophages release prostaglandin E2, which inhibits IgM secretion by peritoneal B-1a cells. J. Immunol. 154: 5630-5636.
40. + B lymphocytes. Int. Immunol. 2: 515-520.
41. Tumang, J.R., R. Frances, S.G. Yeo, & T.L. Rothstein. 2005. Spontaneously Ig-secreting B-1 cells violate the accepted paradigm for expression of differentiation-associated transcription factors. J. Immunol. 174: 3173-3177.
42. Holodick, N.E., J.R. Tumang, & T.L. Rothstein. 2010. Immunoglobulin secretion by B1 cells: differential intensity and IRF4-dependence of spontaneous IgM secretion by peritoneal and splenic B1 cells. Eur. J. Immunol. 40: 3007-3016.
43. Fairfax, K.A. et al. 2007. Different kinetics of Blimp-1 induction in B cell subsets revealed by reporter gene. J. Immunol. 178: 4104-4111.
44. + peritoneal B cells express high levels of membrane, but not secretory, C mu mRNA. J. Immunol. 146: 3639-3645.
45. Nguyen, T.T., R.A. Elsner, & N. Baumgarth. 2015. Natural IgM prevents autoimmunity by enforcing B cell central tolerance induction. J. Immunol. 194: 1489-1502.
46. Boes, M. et al. 1998. Enhanced B-1 cell development, but impaired IgG antibody responses in mice deficient in secreted IgM. J. Immunol. 160: 4776-4787.
47. Ehrenstein, M.R., T.L. O'Keefe, S.L. Davies, & M.S. Neuberger. 1998. Targeted gene disruption reveals a role for natural secretory IgM in the maturation of the primary immune response. Proc. Natl. Acad. Sci. U.S.A. 95: 10089-11093.
48. Boes, M. et al. 2000. Accelerated development of IgG autoantibodies and autoimmune disease in the absence of secreted IgM. Proc. Natl. Acad. Sci. U.S.A. 97: 1184-1189.
49. Wardemann, H., T. Boehm, N. Dear, & R. Carsetti. 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: 771-780.
50. Kantor, A.B. 1991. The development and repertoire of B-1 cells (CD5 B cells). Immunol. Today 12: 389-391.
51. Montecino-Rodriguez, E. & K. Dorshkind. 2012. B-1 B cell development in the fetus and adult. Immunity 36: 13-21.
52. Castro, C.D., Y. Ohta, H. Dooley, & M.F. Flajnik. 2013. Noncoordinate expression of J-chain and Blimp-1 define nurse shark plasma cell populations during ontogeny. Eur. J. Immunol. 43: 3061-3075.
53. Hooijkaas, H., R. Benner, J.R. Pleasants, & B.S. Wostmann. 1984. Isotypes and specificities of immunoglobulins produced by germ-free mice fed chemically defined ultrafiltered "antigen-free" diet. Eur. J. Immunol. 14: 1127-1130.
54. Baumgarth, N., J.W. Tung, & L.A. Herzenberg. 2005. Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion. Springer Semin. Immunopathol. 26: 347-362.
55. Zhou, Z.H. et al. 2007. The broad antibacterial activity of the natural antibody repertoire is due to polyreactive antibodies. Cell Host Microbe 1: 51-61.
56. Moon, H., J.G. Lee, S.H. Shin, & T.J. Kim. 2012. LPS-induced migration of peritoneal B-1 cells is associated with upregulation of CXCR4 and increased migratory sensitivity to CXCL12. J. Korean Med. Sci. 27: 27-35.
57. Weber, G.F. et al. 2014. Pleural innate response activator B cells protect against pneumonia via a GM-CSF-IgM axis. J. Exp. Med. 211: 1243-1256.
58. Rothstein, T.L. & D.L. Kolber. 1988. Anti-Ig antibody inhibits the phorbol ester-induced stimulation of peritoneal B cells. J. Immunol. 141: 4089-4093.
59. Claflin, J.L. & J. Berry. 1988. Genetics of the phosphocholine-specific antibody response to Streptococcus pneumoniae. Germ-line but not mutated T15 antibodies are dominantly selected. J. Immunol. 141: 4012-4019.
60. Baumgarth, N. 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: 271-280.
61. Nair, N., R. Biswas, F. Gotz, & L. Biswas. 2014. Impact of Staphylococcus aureus on pathogenesis in polymicrobial infections. Infect. Immunol. 82: 2162-2169.
62. O'Garra, A. et al. 1992. Ly-1 B (B-1) cells are the main source of B cell-derived interleukin 10. Eur. J. Immunol. 22: 711-717.
63. Rauch, P.J. et al. 2012. Innate response activator B cells protect against microbial sepsis. Science 335: 597-601.
64. Weber, G.F. et al. 2015. Interleukin-3 amplifies acute inflammation and is a potential therapeutic target in sepsis. Science 347: 1260-1265.
65. + T-cell activation. Eur. J. Immunol. 43: 2317-2326.
66. Zhong, X. et al. 2007. Reciprocal generation of Th1/Th17 and T(reg) cells by B1 and B2 B cells. Eur. J. Immunol. 37: 2400-2404.
67. + T cells. J. Leukoc. Biol. 91: 525-536.
68. Chang, W.L. et al. 2007. Influenza virus infection causes global respiratory tract B cell response modulation via innate immune signals. J. Immunol. 178: 1457-1467.
69. Coro, E.S., W.L. Chang, & N. Baumgarth. 2006. Type I IFN receptor signals directly stimulate local B cells early following influenza virus infection. J. Immunol. 176: 4343-4351.
70. Gasteiger, G. & A.Y. Rudensky. 2014. Interactions between innate and adaptive lymphocytes. Nat. Rev. Immunol. 14: 631-639.
71. deWaard, R. et al. 1998. Presence of germline and full-length IgA RNA transcripts among peritoneal B-1 cells. Dev. Immunol. 6: 81-87.
72. Kroese, F.G., R. deWaard, & N.A. Bos. 1996. B-1 cells and their reactivity with the murine intestinal microflora. Semin. Immunol. 8: 11-18.
73. Savage, H.P. & N. Baumgarth. 2015. Characteristics of natural antibody-secreting cells. Ann. N.Y. Acad. Sci. 1362: 132-142.