B cell tolerance to a minor, but not to a major, antigenic surface of the self antigen, cytochrome c

Journal of Immunology

Volumn 161, Issue 6, 1998, Pages 2841-2847

  Jemmerson, Ronald ^a,d   Minnerath, Jeanne M ^a,e   Hedrick, Stephen M ^b   Oehen, Stephan ^c  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c INSTITUTE OF EXPERIMENTAL IMMUNOLOGY   (Switzerland)

^d Box 196 FUMC ^*  (United States)

^e SAINT MARY'S UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CYTOCHROME C; MONOCLONAL ANTIBODY; OVALBUMIN;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE; CELL DEATH; CONTROLLED STUDY; FEMALE; IMMUNOLOGICAL TOLERANCE; MALE; MOUSE; NONHUMAN; PIGEON; PRIORITY JOURNAL; T LYMPHOCYTE; THYMUS; TRANSGENIC MOUSE;

ANIMALS; ANTIBODIES, MONOCLONAL; B-LYMPHOCYTES; BINDING SITES, ANTIBODY; COLUMBIDAE; CYTOCHROME C GROUP; EPITOPES, B-LYMPHOCYTE; IMMUNE SERA; LYMPHOCYTE COUNT; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; SELF TOLERANCE; VARIATION (GENETICS);

EID: 0032531039     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (68)

1. Nossal, G. J. V. 1996. Clonal anergy of B cells: a flexible, reversible, and quantitative concept. J. Exp. Med. 183:1953.
2. Goodnow, C. C., J. Crosbie, S. Adelstein, T. B. Lavoie, S. J. Smith-Gill, R. A. Brink, H. Pritchard-Briscoe, J. S. Wotherspoon, R. H. Loblay, K. Raphael, R. J. Trent, and A. Basten. 1988. A transgenic mouse model of immunological tolerance: absence of secretion and altered surface expression of immunoglobulin in self-reactive B lymphocytes. Nature 334:676.
3. Nemazee, D. A., and K. Bürki. 1989. Clonal deletion of B lymphocytes in a transgenic mouse bearing anti-MHC class I antibody genes. Nature 337:562.
4. + thymocytes. Nature 333:742.
5. Adelstein, S., H. Pritchard-Briscoe, T. A. Anderson, J. Crosbie, G. Gammon, R. H. Loblay, A. Basten, and C. C. Goodnow. 1991. Induction of self-tolerance in T cells but not B cells of transgenic mice expressing little self antigen. Science 251:1223.
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.
7. Liu, G. Y., P. J. Fairchild, R. M. Smith, J. R. Prowle, D. Kioussels, and D. C. Wraith. 1995. Low avidity recognition of self-antigen by T cells permits escape from central tolerance. Immunity 3:407.
8. Goodnow, C. C. 1992. Transgenic mice and analysis of B-cell tolerance. Annu. Rev. Immunol. 10:489.
9. Ashton-Rickardt, P. G., A. Bandeira, J. R. Delaney, L. Van Kaer, H.-P. Pircher, R. Zinkemagel, and S. Tonegawa. 1994. Evidence for a differential avidity model of T cell selection in the thymus. Cell 76:651.
10. Sebzda, E., V. A. Wallace, J. Mayer, R. S. M. Yeung, T. W. Mak, and P. S. Ohashi. 1994. Positive and negative thymocyte selection induced by different concentrations of a single peptide. Science 263:1615.
11. Ashton-Rickardt, P. G., and S. Tonegawa. 1994. A differential avidity model of T cell selection. Immunol. Today 15:362.
12. Jameson, S. C., K. A. Hogquist, and M. J. Bevan. 1995. Positive selection of thymocytes. Annu. Rev. Immunol. 13:93.
13. Stollar, B. D. 1991. Autoantibodies and autoantigens: a conserved system that may shape a primary immunoglobulin gene pool. Mol. Immunol. 28:1399.
14. Avrameas, S., and T. Ternynck. 1993. The natural autoantibodies system: between hypotheses and facts. Mol. Immunol. 30:1133.
15. Shlomchik, M. J., D. Zharhary, T. Saunders, S. A. Camper, and M. G. Weigert. 1993. A rheumatoid factor transgenic mouse model of autoantibody regulation. Int. Immunol. 5:1329.
16. Hannum, L. G., D. Ni, A. M. Haberman, M. G. Weigert, and M. J. Shlomchik. 1996. A disease-related rheumatoid factor autoantibody is not tolerized in a normal mouse: implications for the origins of autoantibodies in autoimmune disease. J. Exp. Med. 184:1269.
17. Berneman, A., T. Ternynck, and S. Avrameas. 1992. Natural mouse IgG reacts with self antigens including molecules involved in the immune response. Eur. J. Immunol. 22:625.
18. Portnöi, D., A. Freitas, D. Holmberag, A. Bandeira, and A. Coutinho. 1986. Immunocompetent autoreactive B lymphocytes are activated cycling cells in normal mice. J. Exp. Med. 164:25.
19. Stewart, J. J., H. Agosto, S. Litwin, J. D. Welsh, M. Shlomchik, M. Weigert, and P. E. Seiden. 1997. A solution to the rheumatoid factor paradox: pathologic rheumatoid factors can be tolerized by competition with natural rheumatoid factors. J. Immunol. 159:1728.
20. Caton, A. J., J. R. Swartzentruber, A. L. Kuhl, S. R. Carding, and S. E. Stark. 1996. Activation and negative selection of functionally distinct subsets of antibody-secreting cells by influenza hemagglutinin as a viral and a neo-self antigen. J. Exp. Med. 183:13.
21. Sercarz, E. E., P. V. Lehmann, A. Ametani, G. Benichou, A. Miller, and K. Moudgil. 1993. Dominance and crypticity of T cell antigenic determinants. Annu. Rev. Immunol. 11:729.
22. Mamula, M. J. 1993. The inability to process a self-peptide allows autoreactive T cells to escape tolerance. J. Exp. Med. 177:567.
23. Jemmerson, R., and R. Blankenfeld. 1988. Clonal analysis of the BALB/c secondary B cell repertoire specific for a self-antigen, cytochrome c. J. Immunol. 140:1762.
24. Minnerath, J. M., B. L. Crump, E. Margoliash, and R. Jemmerson. 1995. Major and minor epitopes on the self antigen mouse cytochrome c mapped by site-directed mutagene: sis. Mol. Immunol. 32:795.
25. Jemmerson, R. 1987. Multiple overlapping epitopes in the three antigenic regions of horse cytochrome c. J. Immunol. 138:213.
26. H genes. Mol. Immunol. 34:843.
27. Oehen, S., L. Feng, Y. Xia, C. D. Surh, and S. M. Hedrick. 1996. Antigen compartmentation and T helper cell tolerance induction. J. Exp. Med. 183:2617.
28. Jemmerson, R. 1987. Antigenicity and native structure of globular proteins: low frequency of peptide reactive antibodies. Proc. Natl. Acad. Sci. USA 84:9180.
29. a Ia molecule. J. Immunol. 135:3314.
30. Nemazee, D. 1996. Antigen receptor 'capacity' and the sensitivity of self-tolerance. Immunol. Today 17:25.
31. Harmey, M. A., and W. Neupert. 1985. Synthesis and intracellular transport of mitochon-drial proteins. In The Enzymes of Biological Membranes, Vol. 4. A. N. Martonosi, ed. Plenum Press, New York, p. 431.
32. Hickey, D. R., K. Jayaraman, C. T. Goodhue, J. Shah, S. A. Fingar, J. M. Clements, Y. Hosokawa, S. Tsunasawa, and F. Sherman. 1991. Synthesis and expression of genes encoding tuna, pigeon, and horse cytochromes c in the yeast Saccharomyces cerevisiae. Gene 105:73.
33. Borden, D., and E. Margoliash. 1976. Amino acid sequences of proteins-eukaryotic cytochromes c. In Handbook of Biochemistry and Molecular Biology, Vol. 3: Proteins. G. D. Fasman, ed. The Chemical Rubber Co., Cleveland, p. 268.
34. Klinman, N. R. 1969. Antibody with homogeneous antigen binding produced by splenic foci in organ culture. Immunochemistry 6:757.
35. Klinman, N. R. 1971. The mechanism of antigen stimulation of primary and secondary clonal precursor cells. J. Exp. Med. 136:241.
36. Koshy, T. I., T. L. Luntz, E. A. E. Garber, and E. Margoliash. 1992. Expression of recombinant cytochromes c from various species in Saccharomyces cerevisiae: post-translational modifications. Protein Expression Purif. 3:441.
37. DeLange, R. J., A. N. Glazer, and E. L. Smith. 1970. Identification and location of a e-trimethyllysine in yeast cytochrome c. J. Biol. Chem. 245:3325.
38. Minnerath, J. M., L. P. Wakem, L. L. Comfort, F. Sherman, and R. Jemmerson. 1995. The BALB/c mouse B-cell response to pigeon cytochrome c initiates as a heteroclitic response specific for the self antigen mouse cytochrome c. Proc. Natl. Acad. Sci. USA 92:12379.
39. Klinman, N. R. 1976. The acquisition of B-cell competence and diversity. Am. J. Pathol. 85:694.
40. Carbone, F. R., and Y. Paterson. 1985. Monoclonal antibodies to horse cytochrome c expressing four distinct idiotypes distribute among two sites on the native protein. J. Immunol. 135:2609.
41. Bushnell, G. W., G. V. Louie, and G. D. Brayer. 1990. High-resolution three-dimensional structure of horse heart cytochrome c. J. Mol. Biol. 214:585.
42. Kraulis, P. J. 1991. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24:946.
43. Jemmerson, R., and E. Margoliash. 1979. Topographic antigenic determinants on cytochrome c: immunoadsorbent separation of the rabbit antibody populations directed against horse cytochrome c. J. Biol. Chem. 254:12706.
44. Altman, D. G. 1991. Practical Statistics for Medical Research. Chapman and Hall, London.
45. Benjamin, D. C., J. A. Berzofsky, I. J. East, F. R. N. Gurd, C. Hannum, S. J. Leach, E. Margoliash, J. G. Michael, A., Miller, E. M. Prager, M. Reichlin, E. E. Sercarz, S. J. Smith-Gill, P. E. Todd, and A. C. Wilson. 1984. The antigenic structure of proteins: a reappraisal. Annu. Rev. Immunol 2:67.
46. Nisonoff, A., E. Margoliash, and M. Reichlin. 1967. Antibodies to rabbit cytochrome c arising in rabbits. Science 153:1273.
47. Liu, X., C. N. Kim, J. Yang, R. Jemmerson, and X. Wang. 1996. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86:147.
48. Roder, H., G. A. Elove, and S. W. Englander. 1988. Structural characterization of folding intermediates in cytochrome c by H-exchange labeling and proton NMR. Nature 335:700.
49. Salemme, F. R. 1977. Structure and function of cytochromes c. Annu. Rev. Biochem. 46:299.
50. Schwab, C., A. Twardek, T. P. Lo., G. D. Brayer, and H. R. Bosshard. 1993. Mapping antibody binding sites on cytochrome c with synthetic peptides: are results representative of the antigenic structure of proteins'? Protein Sci. 2:175.
51. Metcalf, E. S., and N. R. Klinman. 1976. In vitro tolerance induction of neonatal murine B cells. J. Exp. Med. 143:1327.
52. Klinman, N. R., R. L. Riley, P. R. Morrow, R. R. Jemmerson, and J. M. Teale. 1985. Tolerance and B cell repertoire establishment. Fed. Proc. 44:2488.
53. Katz, D. H., T. Hamaoka, and B. Benacerraf. 1974. Immunological tolerance in bone marrow-derived lymphocytes. III. Tolerance induction in primed B cells by hapten conjugates of unrelated immunogenic or "nonimmunogenic" carriers. J. Exp. Med. 139:1464.
54. von Felton, A., and W. O. Weigle. 1975. The induction of immunological unresponsiveness in previously immunized mice. Cell. Immunol. 18:31.
55. Nemazee, D., D. Russell, B. Arnold, G. Haemmerling, J. Allison, J. F. A. P. Miller, G. Morahan, and K. Buerki. 1991. Clonal deletion of auto-specific B lymphocytes. Immunol. Rev. 122:117.
56. Linton, P.-J., A. Rudie, and N. R. Klinman. 1991. Tolerance susceptibility of newly generating memory B cells. J. Immunol. 146:4099.
57. Linton, P.-J., D. J. Decker, and N. R. Klinman. 1989. Primary antibody-forming cells and secondary B cells are generated from separate precursor cell subpopulations. Cell 59:1049.
58. Goshorn, S. C., E. Retzel, and R. Jemmerson. 1991. Common structural features among monoclonal antibodies binding the same antigenic region of cytochrome c. J. Biol. Chem. 266:2134.
59. Jemmerson, R. 1995. Effects of conformation, amino acid sequence, and carrier coupling on the immunological recognition of peptide and protein antigens. In Immunological Recognition of Peptides in Medicine and Biology. N. D. Zegers, W. J. A. Boersma, and E. Claassen, eds. CRC Press, Boca Raton, p. 213.
60. Yang, J., X. Liu, K. Bhalla, C. N. Kim, A. M. Ibrado, J. Cai, T.-I. Peng, D. P. Jones, and X. Wang. 1997. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275:1129.
61. Kluck, R. M., E. Blossy-Wetzel, D. R. Green, and D. D. Newmeyer 1997. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275:1132.
62. Zou, H., W. J. Henzel, X. Liu, A. Lutschg, and X. Wang. 1997. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90:405.
63. L as an inhibitor of cytosolic cytochrome c accumulation in DNA damage-induced apoptosis. Proc. Natl. Acad. Sci. USA 94:6939.
64. Mamula, M. J. 1995. Lupus autoimmunity: from peptides to particles. Immunol. Rev. 144:301.
65. Utz, P. J., M. Hottelet, P. H. Schur, and P. Anderson. 1997. Proteins phosphorylated during stress-induced apoptosis are common targets for autoantibody production in patients with systemic lupus erythematosus. J. Exp. Med. 185:843.
66. Mamula, M. J., R. Jemmerson, and J. A. Hardin. 1990. The specificity of human anti-cytochrome c autoantibodies that arise in autoimmune disease. J. Immunol. 144:1835.
67. Cunningham, A. J., and E. J. Steele. 1979. Antigens, self and foreign, as the educating force in the development of immune diversity. In B Lymphocytes in the Immune Response. M. Cooper, D. Mosier, A. Scher, and E. Vitetta, eds. Elsevier, North Holland, p. 187.
68. Rathmell, J. C., and C. C. Goodnow. 1994. Effects of the lpr mutation on elimination and inactivation of self-reactive B cells. J. Immunol 153:2831.