Adult BM generates CD5+ B1 cells containing abundant N-region additions

European Journal of Immunology

Volumn 39, Issue 9, 2009, Pages 2383-2394

  Holodick, Nichol E ^a,b   Repetny, Karen ^c,d   Zhong, Xuemei ^a   Rothstein, Thomas L ^b  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c Boston University   (United States)

^d MILLENNIUM PHARMACEUTICALS INC   (United States)

Author keywords

Antibodies; B cells; Cell differentiation; Repertoire development

Indexed keywords

ANNEXIN; CD11B ANTIGEN; CD5 ANTIGEN; GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN; PHORBOL ESTER; TRANSCRIPTION FACTOR PAX5; CARCINOGEN; CD5 PROTEIN, MOUSE;

ADOPTIVE TRANSFER; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; CELL POPULATION; CELL RENEWAL; CONTROLLED STUDY; GENETIC TRANSDUCTION; HOMEOSTASIS; IMMUNOGLOBULIN PRODUCTION; MITOGENESIS; MOUSE; MURINE STEM CELL VIRUS; NONHUMAN; PERITONEAL CAVITY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECIPIENT; RETROVIRUS; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; DRUG EFFECT; IMMUNOLOGY; MALE; METABOLISM;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD5; B-LYMPHOCYTE SUBSETS; BONE MARROW CELLS; CARCINOGENS; IMMUNOGLOBULINS; MALE; MICE; MICE, INBRED BALB C; PHORBOL ESTERS;

EID: 70349257845     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200838920     Document Type: Article

References (45)

1. Herzenberg, L. A., B-1 cells: the lineage question revisited. Immunol. Rev. 2000. 175: 9-22.
2. Hardy, R. R. and Hayakawa, K., B cell development pathways. Annu. Rev. Immunol. 2001. 19: 595-621.
3. Berland, R. andWortis, H. H., Origins and functions of B-1 cells with notes on the role of CD5. Annu. Rev. Immunol. 2002. 20: 253-300.
4. Rothstein, T. L., Cutting edge commentary: two B-1 or not to be one. J. Immunol. 2002. 168: 4257-4261.
5. Tumang, J. R., Hastings, W. D., Bai, C. and Rothstein, T. L., Peritoneal and splenic B-1 cells are separable by phenotypic, functional, and transcriptomic characteristics. Eur. J. Immunol. 2004. 34: 2158-2167.
6. Kantor, A. B., Stall, A. M., Adams, S. and Herzenberg, L. A., Differential development of progenitor activity for three B-cell lineages. Proc. Natl. Acad. Sci. USA 1992. 89: 3320-3324.
7. Tung, J. W., Mrazek, M. D., Yang, Y. and Herzenberg, L. A., Phenotypically distinct B cell development pathways map to the three B cell lineages in the mouse. Proc. Natl. Acad. Sci. USA 2006. 103: 6293-6298.
8. Alugupalli, K. R., Leong, J. M., Woodland, R. T., Muramatsu, M., Honjo, T. and Gerstein, R. M., B1b lymphocytes confer T cell-independent long-lasting immunity. Immunity 2004. 21: 379-390. (Pubitemid 39208339)
9. Haas, K. M., Poe, J. C., Steeber, D. A. and Tedder, T. F., 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.
10. Alugupalli, K. R., A distinct role for B1b lymphocytes in T cell-independent immunity. Curr. Top Microbiol. Immunol. 2008. 319: 105-130.
11. Tumang, J. R., Frances, R., Yeo, S. G. and Rothstein, T. L., Cutting edge: Spontaneously Ig-secreting B-1 cells violate the accepted paradigm for expression of differentiation-associated transcription factors. J. Immunol. 2005. 174: 3173-3177. (Pubitemid 40354018)
12. Hastings, W. D., Tumang, J. R., Behrens, T. W. and Rothstein, T. L., Peritoneal B-2 cells comprise a distinct B-2 cell population with B-1b-like characteristics. Eur. J. Immunol. 2006. 36: 1114-1123.
13. Frances, R., Tumang, J. R. and Rothstein, T. L., Extreme skewing of annexin II and S100A6 expression identified by proteomic analysis of peritoneal B-1 cells. Int. Immunol. 2007. 19: 59-65.
14. Rothstein, T. L. and Kolber, D. L., Peritoneal B cells respond to phorbol esters in the absence of co- mitogen. J. Immunol. 1988. 140: 2880-2885.
15. Tanguay, D. A., Colarusso, T. P., Pavlovic, S., Irigoyen, M., Howard, R. G., Bartek, J., Chiles, T. C. and Rothstein, T. L., Early induction of cyclin D2 expression in phorbol ester-responsive B-1 lymphocytes. J. Exp. Med. 1999. 189: 1685-1690.
16. Tanguay, D. A., Colarusso, T. P., Doughty, C., Pavlovic, S., Rothstein, T. L. and Chiles, T. C., Differences in the signaling requirements for activation of assembled cyclin D3-cdk4 complexes in B-1 and B-2 lymphocytes. J. Immunol. 2001. 166: 4273-4277. (Pubitemid 32233706)
17. Klinman, D. M. and Holmes, K. L., Differences in the repertoire expressed by peritoneal and splenic Ly-1 (CD5)1B cells. J. Immunol. 1990. 144: 4520-4525.
18. Sidman, C. L., Shultz, L. D., Hardy, R. R., Hayakawa, K. and Herzenberg, L. A., Production of immunoglobulin isotypes by Ly-11B cells in viable motheaten and normal mice. Science 1986. 232: 1423-1425.
19. Forster, I. and Rajewsky, K., Expansion and functional activity of Ly-1+B cells upon transfer of peritoneal cells into allotype-congenic, newborn mice. Eur. J. Immunol. 1987. 17: 521-528.
20. Ishida, H., Hastings, R., Kearney, J. and 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: 1213-1220.
21. +) B cells that recognize phosphatidyl choline. J. Exp. Med. 1989. 169: 1869-1877.
22. Pennell, C. A., Mercolino, T. J., Grdina, T. A., Arnold, L. W., Haughton, G. and Clarke, S. H., Biased immunoglobulin variable region gene expression by Ly-1 B cells due to clonal selection. Eur. J. Immunol. 1989. 19: 1289-1295.
23. H11 family. J. Immunol. 1989. 142: 3643-3651.
24. H12 B-cell repertoire towards a single B1 specificity with survival function. Immunol. Rev. 2004. 197: 51-59.
25. Boes, M., Prodeus, A. P., Schmidt, T., Carroll, M. C. and Chen, J., A critical role of natural immunoglobulin M in immediate defense against systemic bacterial infection. J. Exp. Med. 1998. 188: 2381-2386.
26. Ochsenbein, A. F., Fehr, T., Lutz, C., Suter, M., Brombacher, F., Hengartner, H. and Zinkernagel, R. M., Control of early viral and bacterial distribution and disease by natural antibodies. Science 1999. 286: 2156-2159. (Pubitemid 129516290)
27. Baumgarth, N., Herman, O. C., Jager, G. C., Brown, L. E., Herzenberg, L. A. and 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: 271-280.
28. Pennell, C. A., Arnold, L. W., Haughton, G. and Clarke, S. H., Restricted Ig variable region gene expression among Ly-1+ B cell lymphomas. J. Immunol. 1988. 141: 2788-2796. (Pubitemid 18263069)
29. Forster, I., Gu, H. and Rajewsky, K., Germline antibody V regions as determinants of clonal persistence and malignant growth in the B cell compartment. EMBO J. 1988. 7: 3693-3703.
30. Gu, H., Forster, I. and Rajewsky, K., Sequence homologies, N sequence insertion and JH gene utilization in VHDJH joining: implications for the 3joining mechanism and the ontogenetic timing of Ly1 B cell and B-CLL progenitor generation. EMBO J. 1990. 9: 2133-2140.
31. Kantor, A. B., V-gene usage and N-region insertions in B-1a, B-1b and conventional B cells. Semin. Immunol. 1996. 8: 29-35.
32. Tornberg, U. C. and Holmberg, D., 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. 1995. 14: 1680-1689.
33. Lalor, P. A., Herzenberg, L. A., Adams, S. and Stall, A. M., Feedback regulation of murine Ly-1 B cell development. Eur. J. Immunol. 1989. 19: 507-513.
34. Hayakawa, K., Hardy, R. R., Stall, A. M. and Herzenberg, L. A., Immunoglobulin-bearing B cells reconstitute and maintain the murine Ly- 1 B cell lineage. Eur. J. Immunol. 1986. 16: 1313-1316.
35. Montecino-Rodriguez, E., Leathers, H. and Dorshkind, K., Identification of a B-1 B cell-specified progenitor. Nat. Immunol. 2006. 7: 293-301.
36. Herzenberg, L. A. and Tung, J. W., B cell lineages: documented at last! Nat. Immunol. 2006. 7: 225-226.
37. Cong, Y. Z., Rabin, E. andWortis, H. H., Treatment of murine CD5- B cells with anti-Ig, but not LPS, induces surface CD5: two B-cell activation pathways. Int. Immunol. 1991. 3: 467-476.
38. Cherry, S. R., Biniszkiewicz, D., van Parijs, L., Baltimore, D. and Jaenisch, R., Retroviral expression in embryonic stem cells and hematopoietic stem cells. Mol. Cell. Biol. 2000. 20: 7419-7426.
39. Kantor, A. B., Merrill, C. E., Herzenberg, L. A. and Hillson, J. L., An unbiased analysis of V(H)-D-J(H) sequences from B-1a, B-1b, and conventional B cells. J. Immunol. 1997. 158: 1175-1186.
40. Rothstein, T. L., Kolber, D. L., Murphy, T. P. and Cohen, D. P., Induction of phorbol ester responsiveness in conventional B cells after activation via surface Ig. J. Immunol. 1991. 147: 3728-3735.
41. Hardy, R. R. and Hayakawa, K., A developmental switch in B lymphopoiesis. Proc. Natl. Acad. Sci. USA 1991. 88: 11550-11554.
42. + B cells. Eur. J. Immunol. 1996. 26: 2537-2540.
43. Hayakawa, K., Hardy, R. R. and Herzenberg, L. A., Progenitors for Ly-1 B cells are distinct from progenitors for other B cells. J. Exp. Med. 1985. 161: 1554-1568.
44. Naviaux, R. K., Costanzi, E., Haas, M. and Verma, I. M., The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol. 1996. 70: 5701-5705. (Pubitemid 26240755)
45. Frances, R., Tumang, J. R. and Rothstein, T. L., Cutting edge: B-1 cells are deficient in Lck: defective B cell receptor signal transduction in B-1 cells occurs in the absence of elevated Lck expression. J. Immunol. 2005. 175: 27-31. (Pubitemid 40884297)