Identification of initiator B cells, a novel subset of activation-induced deaminase-dependent B-1-like cells that mediate initiation of contact sensitivity

Journal of Immunology

Volumn 181, Issue 3, 2008, Pages 1717-1727

  Kerfoot, Steven M ^a   Szczepanik, Marian ^b   Tung, James W ^c,d   Askenase, Philip W ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NEVADA CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; B LYMPHOCYTE RECEPTOR; CD19 ANTIGEN; CD5 ANTIGEN; IMMUNOGLOBULIN D; IMMUNOGLOBULIN M; THY 1 ANTIGEN; AICDA (ACTIVATION INDUCED CYTIDINE DEAMINASE); AICDA (ACTIVATION-INDUCED CYTIDINE DEAMINASE); ANTIGEN; CYTIDINE DEAMINASE;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CELL SUBPOPULATION; CONTACT SENSITIVITY; CONTROLLED STUDY; GENE ISOLATION; GENE MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SOMATIC HYPERMUTATION; WILD TYPE; ANIMAL; CELL DIFFERENTIATION; CONTACT DERMATITIS; CYTOLOGY; DISEASE MODEL; ENZYMOLOGY; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT; PHENOTYPE; SENSITIVITY AND SPECIFICITY;

ANIMALS; ANTIGENS; B-LYMPHOCYTES; CELL DIFFERENTIATION; CYTIDINE DEAMINASE; DERMATITIS, CONTACT; DISEASE MODELS, ANIMAL; IMMUNITY, NATURAL; IMMUNOGLOBULIN D; IMMUNOGLOBULIN M; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; PHENOTYPE; SENSITIVITY AND SPECIFICITY; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN;

EID: 49649091123     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.3.1717     Document Type: Article

References (44)

1. + NKT cells and B-1 B cells. Trends Immunol. 25: 441-449.
2. Campos, R. A., M. Szczepanik, A. Itakura, M. Akahira-Azuma, S. Sidobre, M. Kronenberg, and P. W. Askenase. 2003. Cutaneous immunization rapidly activates liver invariant Vα14 NKT cells stimulating B-1 B cells to initiate T cell recruitment for elicitation of contact sensitivity. J. Exp. Med. 198: 1785-1796.
3. Itakura, A., M. Szczepanik, R. A. Campos, V. Paliwal, M. Majewska, H. Matsuda, K. Takatsu, and P. W. Askenase. 2005. An hour after immunization peritoneal B-1 cells are activated to migrate to lymphoid organs where within 1 day they produce IgM antibodies that initiate elicitation of contact sensitivity. J. Immunol. 175: 7170-7178.
4. Tsuji, R. F., M. Szczepanik, I. Kawikova, V. Paliwal, R. A. Campos, A. Itakura, M. Akahira-Azuma, N. Baumgarth, L. A. Herzenberg, and P. W. Askenase. 2002. B cell-dependent T cell responses: IgM antibodies are required to elicit contact sensitivity. J. Exp. Med. 196: 1277-1290.
5. Kawahara, T., H. Ohdan, G. Zhao, Y. G. Yang, and M. Sykes. 2003. Peritoneal cavity B cells are precursors of splenic IgM natural antibody-producing cells. J. Immunol. 171: 5406-5414.
6. Yang, Y., J. W. Tung, E. E. B. Ghosn, L. A. Herzenberg, and L. A. Herzenberg. 2007. Division and differentiation of natural antibody-producing cells in mouse spleen. Proc. Natl. Acad. Sci. USA 104: 4542-4546.
7. Szczepanik, M., M. Akahira-Azuma, K. Bryniarski, R. F. Tsuji, I. Kawikova, W. Ptak, C. Kiener, R. A. Campos, and P. W. Askenase. 2003. B-1 B cells mediate required early T cell recruitment to elicit protein-induced delayed-type hypersensitivity. J. Immunol. 171: 6225-6235.
8. Harari, O. A., J. F. McHale, D. Marshall, S. Ahmed, D. Brown, P. W. Askenase, and D. O. Haskard. 1999. Endothelial cell E- and P-selectin up-regulation in murine contact sensitivity is prolonged by distinct mechanisms occurring in sequence. J. Immunol. 163: 6860-6866.
9. + lymphocyte homing and initiation of late-phase inflammation in contact sensitivity. J. Exp. Med. 199: 1223-1234.
10. Thiriot, A., A. M. Drapier, P. Vieira, C. Fitting, J. M. Cavaillon, P. A. Cazenave, and D. Rueff-Juy. 2007. The Bw cells, a novel B cell population conserved in the whole genus Mus. J. Immunol. 179: 6568-6578.
11. Berland, R., and H. H. Wortis. 2002. Origins and functions of B-1 cells with notes on the role of CD5. Annu. Rev. Immunol. 20: 253-300.
12. Wortis, H. H., and R. Berland. 2001. Cutting edge commentary: origins of B-1 cells. J. Immunol. 166: 2163-2166.
13. Baumgarth, N., J. W. Tung, and L. A. Herzenberg. 2005. Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion. Springer Semin. Immunopathol. 26: 347-362.
14. Hardy, R. R. 2006. B-1 B cell development. J. Immunol. 177: 2749-2754.
15. Askenase, P. W., and G. L. Asherson. 1972. Contact sensitivity to oxazolone in the mouse: VIII. Demonstration of several classes of antibody in the sera of contact sensitized and unimmunized mice by a simplified antiglobulin assay. Immunology 23: 289-298.
16. Alugupalli, K. R., J. M. Leong, R. T. Woodland, M. Muramatsu, T. Honjo, and R. M. Gerstein. 2004. B1b lymphocytes confer T cell-independent long-lasting immunity. Immunity 21: 379-390.
17. Haas, K. M., J. C. Poe, D. A. Steeber, and 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.
18. Campos, R. A., M. Szczepanik, M. Lisbonne, A. Itakura, M. Leite-de-Moraes, and P. W. Askenase. 2006. Invariant NKT cells rapidly activated via immunization with diverse contact antigens collaborate in vitro with B-1 cells to initiate contact sensitivity. J. Immunol. 177: 3686-3694.
19. Paliwal, V., R. F. Tsuji, M. Szczepanik, I. Kawikova, R. A. Campos, M. Kneilling, M. Rocken, J. Schuurman, F. A. Redegeld, F. P. Nijkamp, and P. W. Askenase. 2002. Subunits of IgM reconstitute defective contact sensitivity in B-1 cell-deficient xid mice: κ light chains recruit T cells independent of complement. J. Immunol. 169: 4113-4123.
20. Petersen-Mahrt, S. 2005. DNA deamination in immunity. Immunol. Rev. 203: 80-97.
21. Pham, P., R. Bransteitter, and M. F. Goodman. 2005. Reward versus risk: DNA cytidine deaminases triggering immunity and disease. Biochemistry 44: 2703-2715.
22. Park, S. R., H. A. Kim, S. K. Chun, J. B. Park, and P. H. Kim. 2005. Mechanisms underlying the effects of LPS and activation-induced cytidine deaminase on IgA isotype expression. Mol. Cells 19: 445-451.
23. Cattoretti, G., M. Buttner, R. Shaknovich, E. Kremmer, B. Alobeid, and G. Niedobitek. 2006. Nuclear and cytoplasmic AID in extrafollicular and germinal center B cells. Blood 107: 3967-3975.
24. Ueda, Y., D. Liao, K. Yang, A. Patel, and G. Kelsoe. 2007. T-independent activation-induced cytidine deaminase expression, class-switch recombination, and antibody production by immature/transitional 1 B cells. J. Immunol. 178: 3593-3601.
25. Han, J. H., S. Akira, K. Calame, B. Beutler, E. Selsing, and T. Imanishi-Kari. 2007. Class switch recombination and somatic hypermutation in early mouse B cells are mediated by B cell and Toll-like receptors. Immunity 27: 64-75.
26. Szczepanik, M., K. Bryniarski, M. Tutaj, M. Ptak, J. Skrzeczynska, P. W. Askenase, and W. Ptak. 2005. Epicutaneous immunization induces αβ T-cell receptor CD4 CD8 double-positive non-specific suppressor T cells that inhibit contact sensitivity via transforming growth factor-β. Immunology 115: 42-54.
27. Wofsy, L., C. Henry, J. Kimura, and J. North. 1980. Modification and use of antibodies to label cell surface antigens. In Selected Methods in Cellular Immunology. B. B. Mishell and S. M. Shiigi, eds. Freeman, San Francisco, pp. 287-304.
28. Herzenberg, L. A., J. Tung, W. A. Moore, L. A. Herzenberg, and D. R. Parks. 2006. Interpreting flow cytometry data: a guide for the perplexed. Nat. Immunol. 7: 681-685.
29. Roederer, M., A. B. Kantor, D. R. Parks, and L. A. Herzenberg. 1996. Cy7PE and Cy7APC: bright new probes for immunofluorescence. Cytometry 24: 191-197.
30. Jolly, C. J., N. Klix, and M. S. Neuberger. 1997. Rapid methods for the analysis of immunoglobulin gene hypermutation: application to transgenic and gene targeted mice. Nucleic Acids Res. 25: 1913-1919.
31. 4-specific DTH-initiating cells with an unusual mixed phenotype for an antigen-specific cell. Cell. Immunol. 161: 244-255.
32. -, and expresses IL-3 receptors, but no IL-2 receptors. J. Immunol. 143: 3125-3133.
33. +). J. Invest Dermatol. 102: 321-327.
34. Snapper, C. M., J. J. Hooley, S. Barbieri, and F. D. Finkelman. 1990. Murine B cells expressing Thy-1 after in vivo immunization selectively secrete IgE. J. Immunol. 144: 2940-2945.
35. - CS-initiating cell: in vitro desensitization with hapten-amino acid or hapten-Ficoll conjugates, versus hapten-protein conjugates, suggests different antigen receptors on the immune cells that mediate the early and late components of murine contact sensitivity. J. Immunol. 153: 32-44.
36. Baumgarth, N., O. C. Herman, G. C. Jager, L. E. Brown, L. A. Herzenberg, and J. Chen. 2000. B-1 and B-2 cell-derived immunoglobulin M antibodies are non-redundant components of the protective response to influenza virus infection. J. Exp. Med. 192: 271-280.
37. + B) cells make somatically hypermutated high affinity IgM rheumatoid factors. J. Immunol. 151: 473-488.
38. Schettino, E. W., S. K. Chai, M. T. Kasaian, H. W. Schroeder, Jr., and P. Casali. 1997. VHDJH gene sequences and antigen reactivity of monoclonal antibodies produced by human B-1 cells: evidence for somatic selection. J. Immunol. 158: 2477-2489.
39. Hayakawa, K., and R. R. Hardy. 2000. Development and function of B-1 cells. Curr. Opin. Immunol. 12: 346-353.
40. Weller, S., M. C. Braun, B. K. Tan, A. Rosenwald, C. Cordier, M. E. Conley, A. Plebani, D. S. Kumararatne, D. Bonnet, O. Tournilhac, G. Tchernia, B. Steiniger, L. M. Staudt, J. L. Casanova, C. A. Reynaud, and J. C. Weill. 2004. Human blood IgM "memory" B cells are circulating splenic marginal zone B cells harboring a prediversified immunoglobulin repertoire. Blood 104: 3647-3654.
41. Reynaud, C. A., V. Dufour, and J. C. Weill. 1997. Generation of diversity in mammalian gut-associated lymphoid tissues: restricted V gene usage does not preclude complex V gene organization. J. Immunol. 159: 3093-3095.
42. Montecino-Rodriguez, E., H. Leathers, and K. Dorshkind. 2006. Identification of a B-1 B cell-specified progenitor. Nat. Immunol. 7: 293-301.
43. Alugupalli, K. R., J. M. Leong, R. T. Woodland, M. Muramatsu, T. Honjo, and R. M. Gerstein. 2004. B1b lymphocytes confer T cell-independent long-lasting immunity. Immunity 21: 379-390.
44. Alugupalli, K. R., and R. M. Gerstein. 2005. Divide and conquer: division of labor by B-1 B cells. Immunity 23: 1-2.