Preferential use of DH reading frame 2 alters B cell development and antigen-specific antibody production

Journal of Immunology

Volumn 181, Issue 12, 2008, Pages 8409-8415

  Schelonka, Robert L ^a   Zemlin, Michael ^a,b   Kobayashi, Ryoki ^a   Ippolito, Gregory C ^a   Zhuang, Yingxin ^a   Gartland, G Larry ^a   Szalai, Alex ^a   Fujihashi, Kohtaro ^a   Rajewsky, Klaus ^c   Schroeder Jr , Harry W ^a  

^a University of Alabama at Birmingham   (United States)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; IMMUNOGLOBULIN HEAVY CHAIN; EPITOPE;

AMINO ACID COMPOSITION; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE DIFFERENTIATION; BONE MARROW CELL; CONTROLLED STUDY; FLOW CYTOMETRY; FRAMESHIFT MUTATION; IMMUNOGLOBULIN HEAVY CHAIN GENE; MOUSE; NONHUMAN; PERITONEAL CAVITY; PRIORITY JOURNAL; SPLEEN CELL; ANIMAL; ANTIBODY SPECIFICITY; B LYMPHOCYTE; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL DIFFERENTIATION; COMPARATIVE STUDY; COMPLEMENTARITY DETERMINING REGION; FEMALE; GENE REARRANGEMENT; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; NUCLEOTIDE SEQUENCE; PATHOLOGY;

ANIMALS; ANTIBODY DIVERSITY; B-LYMPHOCYTE SUBSETS; CELL DIFFERENTIATION; COMPLEMENTARITY DETERMINING REGIONS; EPITOPES, B-LYMPHOCYTE; FEMALE; FRAMESHIFT MUTATION; GENE REARRANGEMENT, B-LYMPHOCYTE, HEAVY CHAIN; IMMUNOGLOBULIN HEAVY CHAINS; MICE; MICE, INBRED BALB C; MICE, MUTANT STRAINS; READING FRAMES;

EID: 58849120982     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.12.8409     Document Type: Article

References (40)

1. Tonegawa, S. 1983. Somatic generation of antibody diversity. Nature 302: 575-581.
2. Alt, F. W., and D. Baltimore. 1982. Joining of immunoglobulin heavy chain gene segments: implications from a chromosome with evidence of three D-J heavy fusions. Proc. Nat. Acad. Sci. USA 79: 4118-4122.
3. Rajewsky, K. 1996. Clonal selection and learning in the antibody system. Nature 381: 751-758. (Pubitemid 26243107)
4. Kabat, E. A., T. T. Wu, H. M. Perry, K. S. Gottesman, and C. Foeller. 1991. Sequences of Proteins of Immunological Interest, 5th Ed., U.S. Department of Health and Human Services, Bethesda, MD.
5. Padlan, E. A. 1994. Anatomy of the antibody molecule. Mol. Immunol. 31: 169-217.
6. H is sufficient for most antibody specificities. Immunity 13: 37-45.
7. Reth, M. G., and F. W. Alt. 1984. Novel immunoglobulin heavy chains are produced from DJH gene segment rearrangements in lymphoid cells. Nature 312: 418-423.
8. Gu, H., D. Kitamura, and K. Rajewsky. 1991. B cell development regulated by gene rearrangement: arrest of maturation by membrane-bound Dμ protein and selection of DH element reading frames. Cell 65: 47-54. (Pubitemid 121001212)
9. 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.
10. H reading frame preference. J. Immunol. 181: 8416-8424.
11. Cohn, M. 2008. A hypothesis accounting for the paradoxical expression of the D gene segment in the BCR and the TCR. Eur. J. Immunol. 38: 1779-1787.
12. 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.
13. Bibollet-Ruche, F., L. Hui, J. M. Decker, P. A. Goepfert, B. H. Hahn, E. Delaporte, M. Peeters, S. Allen, E. Hunter, J. Robinson, et al. 2006. Detection of novel neutralizing antibody responses to the membrane proximal external region (MPER) of gp41 following infection by HIV-1 subtypes A, B, C, D, F, G, H, CRF01, CRF02, or CRF11. Keystone Symposium on HIV Vaccines (X6), March 27-April 2, 2006, Abstract Book. Keystone Symposia, Silverthorne, CO.
14. Yuste, E., H. B. Sanford, J. Carmody, J. Bixby, S. Little, M. B. Zwick, T. Greenough, D. R. Burton, D. D. Richman, R. C. Desrosiers, and W. E. Johnson. 2006. Simian immunodeficiency virus engrafted with human immunodeficiency virus type 1 (HIV-1)-specific epitopes: replication, neutralization, and survey of HIV-1-positive plasma. J. Virol. 80: 3030-3041.
15. Zwick, M. B., A. F. Labrijn, M. Wang, C. Spenlehauer, E. O. Saphire, J. M. Binley, J. P. Moore, G. Stiegler, H. Katinger, D. R. Burton, and P. W. I. Parren. 2001. Broadly neutralizing antibodies targeted to the membraneproximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J. Virol. 75: 10892-10905. (Pubitemid 33034579)
16. Cardoso, R. M. F., M. B. Zwick, R. L. Stanfield, R. Kunert, J. M. Binley, H. Katinger, D. R. Burton, and I. A. Wilson. 2005. Broadly neutralizing anti-HIV antibody 4E10 recognizes a helical conformation of a highly conserved fusionassociated motif in gp41. Immunity 22: 163-173.
17. Ofek, G., M. Tang, A. Sambor, H. Katinger, J. R. Mascola, R. Wyatt, and P. D. Kwong. 2004. Structure and mechanistic analysis of the anti-human immunodeficiency virus Type 1 antibody 2F5 in complex with its gp41 epitope. J. Virol. 78: 10724-10737. (Pubitemid 39258398)
18. Ivanov, I. I., R. L. Schelonka, Y. Zhuang, G. L. Gartland, M. Zemlin, and H. W. Schroeder, Jr. 2005. Development of the expressed immunoglobulin CDR-H3 repertoire is marked by focusing of constraints in length, amino acid utilization, and charge that are first established in early B cell progenitors. J. Immunol. 174: 7773-7780.
19. 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 DH gene segment is sufficient for B cell development and immune function. J. Immunol. 175: 6624-6632.
20. Hardy, R. R., and K. Hayakawa. 2001. B cell development pathways. Annu. Rev. Immunol. 19: 595-621.
21. Allman, D., R. C. Lindsley, W. DeMuth, K. Rudd, S. A. Shinton, and R. R. Hardy. 2001. Resolution of three nonproliferative immature splenic B cell subsets reveals multiple selection points during peripheral B cell maturation. J. Immunol. 167: 6834-6840. (Pubitemid 33144175)
22. Oliver, A. M., F. Martin, G. L. Gartland, R. H. Carter, and J. F. Kearney. 1997. Marginal zone B cells exhibit unique activation, proliferative and immunoglobulin secretory responses. Eur. J. Immunol. 27: 2366-2374.
23. Loder, F., B. Mutschler, R. J. Ray, C. J. Paige, P. Sideras, R. Torres, M. C. Lamers, and R. Carsetti. 1999. 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. 190: 75-89. (Pubitemid 29330125)
24. Blomberg, B., W. R. Geckeler, and M. Weigert. 1972. Genetics of the antibody response to dextran in mice. Science 177: 178-180.
25. Stohrer, R. C., and J. F. Kearney. 1983. Fine idiotype analysis of B cell precursors in the T-dependent and T-independent responses to α1-3 dextran in BALB/c mice. J. Exp. Med. 158: 2081-2094.
26. Imanishi-Kari, T., E. Rajnavolgyi, T. Takemori, R. S. Jack, and K. Rajewsky. 1979. The effect of light chain gene expression on the inheritance of an idiotype associated with primary anti-(4-hydroxy-3- nitrophenyl)acetyl(NP) antibodies. Eur. J. Immunol. 9: 324-331. (Pubitemid 9205198)
27. VanCott, J. L., H. F. Staats, D. W. Pascual, M. Roberts, S. N. Chatfield, M. Yamamoto, M. Coste, P. B. Carter, H. Kiyono, and J. R. McGhee. 1996. Regulation of mucosal and systemic antibody responses by T helper cell subsets, macrophages, and derived cytokines following oral immunization with live recombinant Salmonella. J. Immunol. 156: 1504-1514.
28. + T cells in nasopharyngeal- associated lymphoreticular tissue. J. Immunol. 170: 1754-1762.
29. Volk, W. A., B. Bizzini, R. M. Snyder, E. Bernhard, and R. R. Wagner. 1984. Neutralization of tetanus toxin by distinct monoclonal antibodies binding to multiple epitopes on the toxin molecule. Infect. Immun. 45: 604-609.
30. 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. 43-67.
31. Nguyen, H. H., M. Zemlin, H. L. Vu, I. I. Ivanov, J. Andrasi, C. Zemlin, R. L. Schelonka, H. W. Schroeder, Jr., and J. Mestecky. 2007. Heterosubtypic immunity to influenza A virus infection requires a properly diversified antibody repertoire. J. Virol. 81: 9331-9338.
32. Freitas, A. A., and B. Rocha. 2000. Population biology of lymphocytes: the flight for survival. Annu. Rev. Immunol. 18: 83-111.
33. 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.
34. Wang, H., and S. H. Clarke. 2004. Regulation of B-cell development by antibody specificity. Curr. Opin. Immunol. 16: 246-250. (Pubitemid 38332030)
35. Merrell, K. T., R. J. Benschop, S. B. Gauld, K. Aviszus, D. Decote-Ricardo, L. J. Wysocki, and J. C. Cambier. 2006. Identification of anergic B cells within a wild-type repertoire. Immunity 25: 953-962.
36. Zemlin, M., R. L. Schelonka, K. Bauer, and H. W. Schroeder, Jr. 2002. Regulation and chance in the ontogeny of B and T cell antigen receptor repertoires. Immunol. Res. 26: 265-278.
37. 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. (Pubitemid 19276688)
38. Corbett, S. J., I. M. Tomlinson, E. L. Sonnhammer, D. Buck, and G. Winter. 1997. Sequence of the human immunoglobulin diversity (D) segment locus: a systematic analysis provides no evidence for the use of DIR segments, inverted D segments, "minor" D segments or D-D recombination. J. Mol. Biol. 270: 587-597.
39. Alam, S. M., M. McAdams, D. Boren, M. Rak, R. M. Scearce, F. Gao, Z. T. Camacho, D. Gewirth, G. Kelsoe, P. Chen, and B. F. Haynes. 2007. The role of antibody polyspecificity and lipid reactivity in binding of broadly neutralizing anti-HIV-1 envelope human monoclonal antibodies 2F5 and 4E10 to glycoprotein 41 membrane proximal envelope epitopes. 178: 4424-4435.
40. Butler, J. E., C. D. Lemke, P. Weber, M. Sinkora, and K. M. Lager. 2007. Antibody repertoire development in fetal and neonatal piglets. XIX. Undiversified B cells with hydrophobic HCDR3s preferentially proliferate in the porcine reproductive and respiratory syndrome. J. Immunol. 178: 6320-6331.