Secondary rearrangements and hypermutation generate sufficient B cell diversity to mount protective antiviral immunoglobulin responses

Journal of Experimental Medicine

Volumn 189, Issue 11, 1999, Pages 1791-1798

  López Macías, Constantino ^a   Kalinke, Ulrich ^a   Cascalho, Marilia ^b   Wabl, Matthias ^b   Hengartner, Hans ^a   Zinkernagel, Rolf M ^a   Lamarre, Alain ^a  

^a INSTITUTE OF EXPERIMENTAL IMMUNOLOGY   (Switzerland)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Antibody diversity; B cell gene rearrangement; Mutation; Vesicular stomatitis virus; Viral antibodies

Indexed keywords

ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; GENE MUTATION; GENE REARRANGEMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; VESICULAR STOMATITIS VIRUS; VIRUS INFECTION;

ANIMALS; ANTIBODIES, VIRAL; ANTIBODY DIVERSITY; B-LYMPHOCYTES; BASE SEQUENCE; DNA; GENE REARRANGEMENT, B-LYMPHOCYTE; GENE TARGETING; MICE; MICE, INBRED C57BL; MUTATION; NEUTRALIZATION TESTS; SEQUENCE HOMOLOGY, NUCLEIC ACID; VESICULAR STOMATITIS-INDIANA VIRUS;

EID: 0344689840     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.189.11.1791     Document Type: Article

References (48)

1. Tonegawa, S. 1983. Somatic generation of antibody diversity. Nature. 302:575-581.
2. Gay, D., T. Saunders, S. Camper, and M. Weigert. 1993. Receptor editing: an approach by autoreactive B cells to escape tolerance J. Exp. Med. 177:999-1008.
3. Radic, M.Z., J. Erikson, S. Litwin, and M. Weigert. 1993. B lymphocytes may escape tolerance by revising their antigen receptors. J. Exp. Med. 177:1165-1173.
4. Tiegs, S.L., D.M. Russell, and D. Nemazee. 1993. Receptor editing in self-reactive bone marrow B cells. J. Exp. Med. 177:1009-1020.
5. Chen, C., Z. Nagy, E.L. Prak, and M. Weigert. 1995. Immunoglobulin heavy chain gene replacement: a mechanism of receptor editing. Immunity. 3:747-755.
6. Lang, J., M. Jackson, L. Teyton, A. Brunmark, K. Kane, and D. Nemazee. 1996. B cells are exquisitely sensitive to central tolerance and receptor editing induced by ultralow affinity, membrane-bound antigen. J. Exp. Med. 184:1685-1697.
7. Chen, C., E.L. Prak, and M. Weigert. 1997. Editing disease-associated autoantibodies. Immunity. 6:97-105.
8. Pelanda, R., S. Schwers, E. Sonoda, R.M. Torres, D. Nemazee, and K. Rajewsky. 1997. Receptor editing in a transgenic mouse model: site, efficiency, and role in B cell tolerance and antibody diversification, Immunity. 7:765-775.
9. Fang, W., B.C. Weintraub, B. Dunlap, P. Garside, K.A. Pape, M.K. Jenkins, C.C. Goodnow, D.L. Mueller, and T.W. Behrens. 1998. Self-reactive B lymphocytes overexpressing Bcl-xL escape negative selection and are tolerized by clonal anergy and receptor editing. Immunity. 9:35-15.
10. Han, S., S.R. Dillon, B. Zheng, M. Shimoda, M.S. Schlissel, and G. Kelsoe. 1997. V(D)J recombinase activity in a subset of germinal center B lymphocytes. Science. 278:301-305.
11. Papavasiliou, F., R. Casellas, H. Suh, X.F. Qin, E. Besmer, R. Pelanda, D. Nemazee, K. Rajewsky, and M.C. Nussenzweig. 1997. V(D)J recombination in mature B cells: a mechanism for altering antibody responses. Science. 278:298-301.
12. Hertz, M., V. Kouskoff, T. Nakamura, and D. Nemazee. 1998. V(D)J recombinase induction in splenic B lymphocytes is inhibited by antigen-receptor signalling. Nature. 394:292-295.
13. Meffre, E., F. Papavasiliou, P. Cohen, O. de Bouteiller, D. Bell, H. Karasuyama, C. Schiff, J. Banchereau, Y.J. Liu, and M.C. Nussenzweig. 1998. Antigen receptor engagement turns off the V(D)J recombination machinery in human tonsil B cells. J. Exp. Med. 188:765-772.
14. Cascalho, M., A. Ma, S. Lee, L. Masat, and M. Wabl. 1996. A quasi-monoclonal mouse. Science. 272:1649-1652.
15. Cascalho, M., J. Wong, and M. Wabl. 1997. VH gene replacement in hyperselected B cells of the quasimonoclonal mouse. J. Immunol. 159:5795-5801.
16. Bertrand, F.E., R. Golub, and G.E. Wu. 1998. V(H) gene replacement occurs in the spleen and bone marrow of non-autoimmune quasi-monoclonal mice. Eur. J. Immunol. 28: 3362-3370.
17. Charan, S., and R.M. Zinkernagel. 1986. Antibody mediated suppression of secondary IgM response in nude mice against vesicular stomatitis virus. J. Immunol. 136:3057-3061.
18. Battegay, M., S. Cooper, A. Althage, J. Baenziger, H. Hengartner, and R.M. Zinkernagel. 1991. Quantification of lymphocytic choriomeningitis virus with an immunological focus assay in 24-or 96-well plates. J. Virol. Methods. 33:191-198.
19. Matsuura, Y., R.D. Possee, H.A. Overton, and D.H. Bishop. 1987. Baculovirus expression vectors: the requirements for high level expression of proteins, including glycoproteins. J. Gen. Virol. 68:1233-1250.
20. Battegay, M., D. Moskophidis, H. Waldner, M.A. Brundler, W.-P. Fung-Leung, T.W. Mak, H. Hengartner, and R.M. Zinkernagel. 1993. Impairment and delay of neutralizing antiviral antibody responses by virus-specific cytotoxic T cells. J. Immunol. 151:5408-5415.
21. Krebber, A., S. Bomhauser, J. Burmester, A. Honegger, J. Willuda, H.R. Bosshard, and A. Plückthun. 1997. Reliable cloning of functional antibody variable domains from hybridomas and spleen cell repertoires employing a reengineered phage display system. J. Immunol. Methods. 201:35-55.
22. Wagner, R.R. 1987. The Rhabdoviruses. Plenum Press, New York. 544 pp.
23. Lefrancois, L. 1984. Protection against lethal viral infection by neutralizing and nonneutralizing monoclonal antibodies: distinct mechanisms of action in vivo. J. Virol. 51:208-214.
24. Bachmann, M.F., T.M. Kündig, C.P. Kalberer, H. Hengartner, and R.M. Zinkernagel. 1994. How many specific B cells are needed to protect against a virus? J. Immunol. 152:4235-4241.
25. Roost, H.-P., M.F. Bachmann, A. Haag, U. Kalinke, V. Pliska, H. Hengartner, and R.M. Zinkernagel. 1995. Early high-affinity neutralizing anti-viral IgG responses without further overall improvements of affinity. Proc. Natl. Acad. Sci. USA. 92:1257-1261.
26. Roost, H.-P., A. Haag, C. Burkhart, R.M. Zinkernagel, and H. Hengartner. 1996. Mapping of the dominant neutralizing antigenic site of a virus using infected cells. J. Immunol. Methods. 189:233-242.
27. Kalinke, U., A. Krebber, C. Krebber, E. Bucher, A. Plückthun, R.M. Zinkernagel, and H. Hengartner. 1996. Monovalent single-chain Fv fragments and bivalent miniantibodies bound to vesicular stomatitis virus (VSV) protect against lethal infection. Eur. J. Immunol. 26:2801-2806.
28. Burns, W., L.C. Billups, and A.L. Notkins. 1975. Thymus dependence of viral antigens. Nature. 256:654-656.
29. Charan, S., H. Hengartner, and R.M. Zinkernagel. 1987. Antibodies against the two serotypes of vesicular stomatitis virus measured by enzyme-linked immunosorbent assay: immunodominance of serotype-specific determinants and induction of asymmetrically cross-reactive antibodies. J. Virol. 61:2509-2514.
30. Leist, T.P., S.P. Cobbold, H. Waldmann, M. Aguet, and R.M. Zinkernagel. 1987. Functional analysis of T lymphocyte subsets in antiviral host defense. J. Immunol. 138:2278-2281.
31. Takeda, S., Y.R. Zou, H. Bluethmann, D. Kitamura, U. Muller, and K. Rajewsky. 1993. Deletion of the immunoglobulin kappa chain intron enhancer abolishes kappa chain gene rearrangement in cis but not lambda chain gene rearrangement in trans. EMBO (Eur. Mol. Biol. Organ.) J. 12: 2329-2336.
32. Kalinke, U., E.M. Bucher, A. Oxenius, B. Ernst, H.-P. Roost, S. Geley, R. Kofler, R.M. Zinkernagel, and H. Hengartner. 1996. The role of somatic mutation in the generation of the protective humoral immune response against vesicular stomatitis virus (VSV). Immunity. 5:639-652.
33. Kagi, D., B. Ledermann, K. Bürki, P. Seiler, B. Odermatt, K.J. Olsen, E.R. Podack, R.M. Zinkernagel, and H. Hengartner. 1994. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature. 369:31-37.
34. Zinkernagel, R.M., T. Leist, H. Hengartner, and A. Althage. 1985. Susceptibility to lymphocytic choriomeningitis virus isolates correlates directly with early and high cytotoxic T cell activity, as well as with footpad swelling reaction, and all three are regulated by H-2D. J. Exp. Med. 162:2125-2141.
35. Kimmig, B. and F. Lehmann-Grube. 1979. The immune response of the mouse to lymphocytic choriomeningitis virus. I. Circulating antibodies. J. Gen. Virol. 45:703-710.
36. Moskophidis, D., S.P. Cobbold, H. Waldmann, and F. Lehmann-Grube. 1987. Mechanism of recovery from acute virus infection: treatment of lymphocytic choriomeningitis virus-infected mice with monoclonal antibodies reveals that Lyt-2+ T lymphocytes mediate clearance of virus and regulate the antiviral antibody response. J. Virol. 61:1867-1874.
37. Bruns, M., J. Cihak, G. Muller, and F. Lehmann-Grube. 1983. Lymphocytic choriomeningitis virus. VI. Isolation of a glycoprotein mediating neutralization. Virology. 130:247-251.
38. Buchmeier, M.J., H.A. Lewicki, O. Tomori, and M.B.A. Oldstone. 1981. Monoclonal antibodies to lymphocytic choriomeningitis and pichinde viruses: generation, characterization, and cross-reactivity with other arenaviruses. Virology. 113:73-85.
39. Baldridge, J.R., and M.J. Buchmeier. 1992. Mechanisms of antibody-mediated protection against lymphocytic choriomeningitis virus infection: mother-to-baby transfer of humoral protection. J. Virol. 66:4252-4257.
40. Seiler, P., M.A. Brundler, C. Zimmermann, D. Weibel, M. Bruns, H. Hengartner, and R.M. Zinkernagel. 1998. Induction of protective cytotoxic T cell responses in the presence of high titers of virus-neutralizing antibodies: implications for passive and active immunization. J. Exp. Med. 187:649-654.
41. Wright, K.E., and M.J. Buchmeier. 1991. Antiviral antibodies attenuate T-cell-mediated immunopathology following acute lymphocytic choriomeningitis virus infection. J. Virol. 65:3001-3006.
42. Planz, O., P. Seiler, H. Hengartner, and R.M. Zinkernagel. 1996. Specific cytotoxic T cells eliminate cells producing neutralizing antibodies. Nature. 382:726-729.
43. Rueckert, R.R. 1990. Picornaviridae and their replication. In Virology. B.N. Fields and D.M. Knipe, editors. Raven Press, New York. 507-548.
44. Fehr, T., H.Y. Naim, M.F. Bachmann, A.F. Ochsenbein, P. Spielhofer, E. Bucher, H. Hengartner, M.A. Billeter, and R.M. Zinkernagel. 1998. T-cell independent IgM and enduring protective IgG antibodies induced by chimeric measles viruses. Nat. Med. 4:945-948.
45. Nussenzweig, M.C. 1998. Immune receptor editing: revise and select. Cell. 95:875-878.
46. Qin, X.F., S. Schwers, W. Yu, F. Papavasiliou, H. Suh, A. Nussenzweig, K. Rajewsky, and M.C. Nussenzweig. 1999. Secondary V(D)J recombination in B-1 cells. Nature. 397: 355-359.
47. Retter, M.W., and D. Nemazee. 1998. Receptor editing occurs frequently during normal B cell development. J. Exp. Med. 188:1231-1238.
48. de Wildt, R.M.T., R.M.A. Hoet, W.J. van Venrooij, I.M. Tomlinson, and G. Winter. 1999. Analysis of heavy and light chain pairings indicates that receptor editing shapes the human antibody repertoire. J. Mol. Biol. 285:895-901.