The peritoneal cavity B-2 antibody repertoire appears to reflect many of the same selective pressures that shape the B-1a and B-1b repertoires

Journal of Immunology

Volumn 185, Issue 10, 2010, Pages 6085-6095

  Vale, Andre M ^a   Tanner, Jason M ^b   Schelonka, Robert L ^b,f   Zhuang, Yingxin ^a   Zemlin, Michael ^e   Gartland, G Larry ^a,c,d   Schroeder Jr , Harry W ^a  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c University of Alabama at Birmingham   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e PHILIPPS UNIVERSITY MARBURG   (Germany)

^f OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CDR 3 PROTEIN; IMMUNOGLOBULIN; NUCLEOTIDE; UNCLASSIFIED DRUG;

AMINO ACID COMPOSITION; AMINO ACID SEQUENCE; ANIMAL CELL; ANTIGEN BINDING; ARTICLE; B 1A CELL; B 1B CELL; B LYMPHOCYTE; BONE MARROW; CELL COMPARTMENTALIZATION; CELL SELECTION; HYDROPHOBICITY; LYMPHOCYTE; LYMPHOCYTE SUBPOPULATION; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PERITONEAL CAVITY; PRIORITY JOURNAL;

ANIMALS; ANTIBODY DIVERSITY; B-LYMPHOCYTE SUBSETS; B-LYMPHOCYTES; BASE SEQUENCE; CELL SEPARATION; COMPLEMENTARITY DETERMINING REGIONS; FLOW CYTOMETRY; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; PERITONEAL CAVITY; PRECURSOR CELLS, B-LYMPHOID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 78650657599     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001423     Document Type: Article

References (56)

1. Kabat, E. A., T. T. Wu, H. M. Perry, K. S. Gottesman, and C. Foeller. 1991. Sequences of Proteins of Immunological Interest. U. S. Department of Health and Human Services, Bethesda, MD.
2. Xu, J. L., and M. M. Davis. 2000. Diversity in the CDR3 region of V (H) is sufficient for most antibody specificities. Immunity 13:37-45.
3. Lafaille, J. J., A. DeCloux, M. Bonneville, Y. Takagaki, and S. Tonegawa. 1989. Junctional sequences of T cell receptor gamma delta genes: implications for gamma delta T cell lineages and for a novel intermediate of V-(D)-J joining. Cell 59:859-870.
4. Alt, F. W., and D. Baltimore. 1982. Joining of immunoglobulin heavy chain gene segments: implications from a chromosome with evidence of three D-JH fusions. Proc. Natl. Acad. Sci. USA 79:4118-4122.
5. Tonegawa, S. 1983. Somatic generation of antibody diversity. Nature 302:575-581.
6. Ivanov, I. I., R. L. Schelonka, Y. Zhuang, G. L. Gartland, M. Zemlin, and H. W. Schroeder, Jr. 2005. Development of the expressed Ig CDR-H3 repertoire is marked by focusing of constraints in length, amino acid use, and charge that are first established in early B cell progenitors. J. Immunol. 174:7773-7780.
7. Zemlin, M., M. Klinger, J. Link, C. Zemlin, K. Bauer, J. A. Engler, H. W. Schroeder, Jr., and P. M. Kirkham. 2003. Expressed murine and human CDR-H3 intervals of equal length exhibit distinct repertoires that differ in their amino acid composition and predicted range of structures. J. Mol. Biol. 334:733-749.
8. Ivanov, I. I., J. M. Link, G. C. Ippolito, and H. W. Schroeder, Jr. 2002. Constraints on hydropathicity and sequence composition of HCDR3 are conserved across evolution. In The Antibodies. M. Zanetti, and J. D. Capra, eds. Taylor and Francis Group, London, p. 43-67.
9. Perlmutter, R. M., J. F. Kearney, S. P. Chang, and L. E. Hood. 1985. Developmentally controlled expression of immunoglobulin VH genes. Science 227:1597-1601.
10. Alt, F. W., T. K. Blackwell, R. A. DePinho, M. G. Reth, and G. D. Yancopoulos. 1986. Regulation of genome rearrangement events during lymphocyte differentiation. Immunol. Rev. 89:5-30.
11. Schelonka, R. L., I. I. Ivanov, D. Jung, G. C. Ippolito, L. Nitschke, Y. Zhuang, G. L. Gartland, J. Pelkonen, F. W. Alt, K. Rajewsky, and H. W. Schroeder, Jr. 2005. A single D H gene segment creates its own unique CDR-H3 repertoire and is sufficient for B cell development and immune function. J. Immunol. 175:6624-6632.
12. Ippolito, G. C., R. L. Schelonka, M. Zemlin, I. I. Ivanov, R. Kobayashi, C. Zemlin, G. L. Gartland, L. Nitschke, J. Pelkonen, K. Fujihashi, et al. 2006. Forced usage of positively charged amino acids in immunoglobulin CDR-H3 impairs B cell development and antibody production. J. Exp. Med. 203:1567-1578.
13. Zemlin, M., R. L. Schelonka, G. C. Ippolito, C. Zemlin, Y. Zhuang, G. L. Gartland, L. Nitschke, J. Pelkonen, K. Rajewsky, and H. W. Schroeder, Jr. 2008. Regulation of repertoire development through genetic control of DH reading frame preference. J. Immunol. 181:8416-8424.
14. Schelonka, R. L., J. Tanner, Y. Zhuang, G. L. Gartland, M. Zemlin, and H. W. Schroeder, Jr. 2007. Categorical selection of the antibody repertoire in splenic B cells. Eur. J. Immunol. 37:1010-1021.
15. Schelonka, R. L., E. Szymanska, A. M. Vale, Y. Zhuang, G. L. Gartland, and H. W. Schroeder, Jr. 2010. D (H) and J (H) usage in murine fetal liver mirrors that of human fetal liver. Immunogenetics 62:653-666.
16. Schelonka, R. L., I. I. Ivanov, A. M. Vale, E. Szymanska, M. Zemlin, G. L. Gartland, and H. W. Schroeder, Jr. 2010. The CDR-H3 repertoire from TdT deficient adult bone marrow is a close, but not exact, homologue of the CDR-H3 repertoire from perinatal liver. J. Immunol. 185:6075-6084.
17. Herzenberg, L. A., and J. W. Tung. 2006. B cell lineages: documented at last! Nat. Immunol. 7:225-226.
18. Hayakawa, K., R. R. Hardy, L. A. Herzenberg, and L. A. Herzenberg. 1985. Progenitors for Ly-1 B cells are distinct from progenitors for other B cells. J. Exp. Med. 161:1554-1568.
19. Montecino-Rodriguez, E., H. Leathers, and K. Dorshkind. 2006. Identification of a B-1 B cell-specified progenitor. Nat. Immunol. 7:293-301.
20. Haughton, G., L. W. Arnold, A. C. Whitmore, and S. H. Clarke. 1993. B-1 cells are made, not born. Immunol. Today 14:84-87, discussion 87-91.
21. Lam, K. P., and K. Rajewsky. 1999. B cell antigen receptor specificity and surface density together determine B-1 versus B-2 cell development. J. Exp. Med. 190:471-477.
22. Shirai, H., A. Kidera, and H. Nakamura. 1996. Structural classification of CDR-H3 in antibodies. FEBS Lett. 399:1-8.
23. Shirai, H., A. Kidera, and H. Nakamura. 1999. H3-rules: identification of CDR-H3 structures in antibodies. FEBS Lett. 455:188-197.
24. Gu, H., I. Förster, and K. Rajewsky. 1990. Sequence homologies, N sequence insertion and JH gene utilization in VHDJH joining: implications for the joining mechanism and the ontogenetic timing of Ly1 B cell and B-CLL progenitor generation. EMBO J. 9:2133-2140.
25. Tornberg, U. C., and D. Holmberg. 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.
26. Kantor, A. B., C. E. Merrill, L. A. Herzenberg, and J. L. Hillson. 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.
27. Hardy, R. R., and K. Hayakawa. 2001. B cell development pathways. Annu. Rev. Immunol. 19:595-621.
28. Reininger, L., P. Ollier, P. Poncet, A. Kaushik, and J. C. Jaton. 1987. Novel V genes encode virtually identical variable regions of six murine monoclonal antibromelain-treated red blood cell autoantibodies. J. Immunol. 138:316-323.
29. Pennell, C. A., L. W. Arnold, G. Haughton, and S. H. Clarke. 1988. Restricted Ig variable region gene expression among Ly-1+ B cell lymphomas. J. Immunol. 141:2788-2796.
30. Feeney, A. J. 1991. Predominance of the prototypic T15 anti-phosphorylcholine junctional sequence in neonatal pre-B cells. J. Immunol. 147:4343-4350.
31. Feeney, A. J. 1990. Lack of N regions in fetal and neonatal mouse immunoglobulin V-D-J junctional sequences. J. Exp. Med. 172:1377-1390.
32. Yancopoulos, G. D., S. V. Desiderio, M. Paskind, J. F. Kearney, D. Baltimore, and F. W. Alt. 1984. Preferential utilization of the most JH-proximal VH gene segments in pre-B-cell lines. Nature 311:727-733.
33. Malynn, B. A., G. D. Yancopoulos, J. E. Barth, C. A. Bona, and F. W. Alt. 1990. Biased expression of JH-proximal VH genes occurs in the newly generated repertoire of neonatal and adult mice. J. Exp. Med. 171:843-859.
34. Viale, A. C., A. Coutinho, and A. A. Freitas. 1992. Differential expression of VH gene families in peripheral B cell repertoires of newborn or adult immunoglobulin H chain congenic mice. J. Exp. Med. 175:1449-1456.
35. Williams, G. S., A. Martinez, A. Montalbano, A. Tang, A. Mauhar, K. M. Ogwaro, D. Merz, C. Chevillard, R. Riblet, and A. J. Feeney. 2001. Unequal VH gene rearrangement frequency within the large VH7183 gene family is not due to recombination signal sequence variation, and mapping of the genes shows a bias of rearrangement based on chromosomal location. J. Immunol. 167:257-263.
36. Sen, R., and E. Oltz. 2006. Genetic and epigenetic regulation of IgH gene assembly. Curr. Opin. Immunol. 18:237-242.
37. Feeney, A. J. 1992. Predominance of VH-D-JH junctions occurring at sites of short sequence homology results in limited junctional diversity in neonatal antibodies. J. Immunol. 149:222-229.
38. Marshall, A. J., N. Doyen, L. A. Bentolila, C. J. Paige, and G. E. Wu. 1998. Terminal deoxynucleotidyl transferase expression during neonatal life alters D (H) reading frame usage and Ig-receptor-dependent selection of V regions. J. Immunol. 161:6657-6663.
39. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
40. Eisenberg, D. 1984. Three-dimensional structure of membrane and surface proteins. Annu. Rev. Biochem. 53:595-623.
41. Kantor, A. B., and L. A. Herzenberg. 1993. Origin of murine B cell lineages. Annu. Rev. Immunol. 11:501-538.
42. Tung, J. W., M. D. Mrazek, Y. Yang, L. A. Herzenberg, and L. A. Herzenberg. 2006. Phenotypically distinct B cell development pathways map to the three B cell lineages in the mouse. Proc. Natl. Acad. Sci. USA 103:6293-6298.
43. Carlsson, L., C. Overmo, and D. Holmberg. 1992. Selection against N-region diversity in immunoglobulin heavy chain variable regions during the development of pre-immune B cell repertoires. Int. Immunol. 4:549-553.
44. Avrameas, S. 1991. Natural autoantibodies: from 'horror autotoxicus' to 'gnothi seauton'. Immunol. Today 12:154-159.
45. Esplin, B. L., R. S. Welner, Q. Zhang, L. A. Borghesi, and P. W. Kincade. 2009. A differentiation pathway for B1 cells in adult bone marrow. Proc. Natl. Acad. Sci. USA 106:5773-5778.
46. Holodick, N. E., K. Repetny, X. Zhong, and T. L. Rothstein. 2009. Adult BM generates CD5+ B1 cells containing abundant N-region additions. Eur. J. Immunol. 39:2383-2394.
47. Kantor, A. B., A. M. Stall, S. Adams, and L. A. Herzenberg. 1992. Differential development of progenitor activity for three B-cell lineages. Proc. Natl. Acad. Sci. USA 89:3320-3324.
48. Carvalho, T. L., T. Mota-Santos, A. Cumano, J. Demengeot, and P. Vieira. 2001. Arrested B lymphopoiesis and persistence of activated B cells in adult interleukin 7(-/)-mice. J. Exp. Med. 194:1141-1150.
49. Hastings, W. D., J. R. Tumang, T. W. Behrens, and T. L. Rothstein. 2006. Peritoneal B-2 cells comprise a distinct B-2 cell population with B-1b-likecharacteristics. Eur. J. Immunol. 36:1114-1123.
50. Wardemann, H., T. Boehm, N. Dear, and 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.
51. Gu, H., D. Kitamura, and K. Rajewsky. 1991. DH reading frame bias: evolutionary selection, antigen selection or both? Evolutionary selection. Immunol. Today 12:420-421.
52. Ichihara, Y., H. Hayashida, S. Miyazawa, and Y. Kurosawa. 1989. Only DFL16, DSP2, and DQ52 gene families exist in mouse immunoglobulin heavy chain diversity gene loci, of which DFL16 and DSP2 originate from the same primordial DH gene. Eur. J. Immunol. 19:1849-1854.
53. Schelonka, R. L., M. Zemlin, R. Kobayashi, G. C. Ippolito, Y. Zhuang, G. L. Gartland, A. Szalai, K. Fujihashi, K. Rajewsky, and H. W. Schroeder, Jr. 2008. Preferential use of DH reading frame 2 alters B cell development and antigen-specific antibody production. J. Immunol. 181:8409-8415.
54. Tung, J. W., and L. A. Herzenberg. 2007. Unraveling B-1 progenitors. Curr. Opin. Immunol. 19:150-155.
55. Baumgarth, N., O. C. Herman, G. C. Jager, L. Brown, L. A. Herzenberg, and 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. USA 96:2250-2255.
56. 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 nonredundant components of the protective response to influenza virus infection. J. Exp. Med. 192:271-280.