Increased negative selection impairs neonatal B cell repertoire but does not directly lead to generation of disease-associated IgM auto-antibodies

International Immunology

Volumn 18, Issue 5, 2006, Pages 661-669

  Cassady Cain, Robin L ^a   Kaushik, Azad K ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

B lymphocyte; IgM auto antibodies; Negative B cell selection; SHP 1; VHJ558 gene; VDJ rearrangement

Indexed keywords

AUTOANTIBODY; COMPLEMENTARY DNA; IMMUNOGLOBULIN M ANTIBODY; PROTEIN TYROSINE PHOSPHATASE SHP 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CELL SELECTION; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA LIBRARY; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENE MUTATION; GENE REARRANGEMENT; GENETIC PREDISPOSITION; GERM LINE; IMMUNE RESPONSE; LOGISTIC REGRESSION ANALYSIS; MOUSE; MOUSE STRAIN; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; ONTOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

ANIMALS; AUTOANTIBODIES; B-LYMPHOCYTES; DATA INTERPRETATION, STATISTICAL; GENE LIBRARY; GENOTYPE; IMMUNOGLOBULIN M; IMMUNOGLOBULIN MU-CHAINS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; PHYLOGENY; SELECTION (GENETICS);

EID: 33646882384     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxl003     Document Type: Article

References (64)

1. Shlomchik, M. J., Marshak-Rothstein, A., Wolfowicz, C. B., Rothstein, T. L. and Weigert, M. G. 1987. The role of clonal selection and somatic mutation in autoimmunity. Nature 328:805.
2. Adib, M., Ragimbeau, J., Avrameas, S. and Ternynck, T. 1990. IgG autoantibody activity in normal mouse serum is controlled by IgM. J. Immunol. 145:3807.
3. Kiely, J.-M., Braun, J. and Unonaue, E. R. 1985. Autoregulation of B cell growth by an immunoglobulin M autoantibody. J. Immunol. 135:1040.
4. Shultz, L. D., Coman, D. R., Beamer, W. G. and Sidman, C. L. 1984. 'Viable motheaten', a new allele at the motheaten locus I. Pathology. Am. J. Pathol. 116:179.
5. Matthews, R. J., Bowne, D. B., Flores, E. and Thomas, M. L. 1992. Characterization of hematopoietic intracellular protein tyrosine phosphatases: Description of a phosphatase containing an SH2 domain and another enriched in proline-, glutamic acid-, serine-, and threonine-rich sequences. Mol. Cell Biol. 12:2396.
6. v) mutant mice I. Analysis of development of prothymocytes, early B lineage cells and terminal deoxynucleotidyl transferase-positive cells. J. Exp. Med. 164:1129.
7. Shultz, L. D., Schweitzer, P. A., Rajan, T. V. et al. 1993. Mutations at the murine motheaten locus are within the hematopoietic cell protein-tyrosine phosphatase (Hcph) gene. Cell 73:1445.
8. Cyster, J. G. and Goodnow, C. C. 1995. Protein tyrosine phosphatase 1C negatively regulates antigen receptor signalling in B lymphocytes and determines thresholds for negative selection. Immunity 2:13.
9. Pani, G., Kozlowski, M., Cambier, J. C., Mills, G. B. and Siminovitch, K. A. 1995. Identification of the tyrosine phosphatase PTP1C as a B cell antigen receptor-associated protein involved in the regulation of B cell signalling. J. Exp. Med. 181:2077.
10. Zhang, J., Somany, A. K. and Siminovitch, K. A. 2000. Roles of the SHP-1 tyrosine phosphatase in the negative regulation of cell signalling. Semin. Immunol. 12:361.
11. Cornall, R. J., Goodnow, C. C. and Cyster, J. G. 1995. The regulation of self-reactive B cells. Curr. Opin. Immunol. 7:804.
12. Frearson, J. A. and Alexander, D. R. 1997. The role of phosphotyrosine phosphatases in haematopoietic cell signal transduction. Bioessays 19:417.
13. Sidman, C. L., Shultz, L. D., Hardy, R. R., Hayakawa, K. and Herzenberg, L. A. 1986. Production of immunoglobulin isotypes by Ly-1+ B cells in viable motheaten and normal mice. Science 232:1423.
14. Hayakawa, K., Hardy, R. R., Parks, D. R. and Harzenberg, L. A. 1983. The Ly-1B cell subpopulation in normal, immunodefective and autoimmune mice. J. Exp. Med. 157:202.
15. Hayakawa, K., Hardy, R. R., Honda, M., Harzenberg, L. A. and Steinberg, A. D. 1984. Ly-1 B cells: Functionally distinct lymphocytes that secrete IgM autoantibodies. Proc. Natl Acad. Sci. USA 81:2494.
16. Christianson, S. W., Greiner, D. L., Deluca, D. et al. 2002. T cell developmental defects in 'viable motheaten' mice deficient in SHP-1 protein-tyrosine phosphatase. Developmental defects are corrected in vitro in the presence of normal hematopoietic-origin stromal cells and in vivo by exogenous IL-7. J. Autoimmun. 18:119.
17. Kasturi, K., Mayer, R., Bona, C. A., Scott, V. E. and Sidman, C. L. 1990. Germline V genes encode viable motheaten mouse auto-antibodies against thymocytes and red blood cells. J. Immunol. 145:2304.
18. Shultz, L. D. and Zurier, R. B. 1978. "Motheaten": A single gene model for stem cell dysfunction and early onset autoimmunity. In Rose, N. R., Bigazzi, P. E. and Warner, N. L., eds, Genetic Control of Autoimmune Disease. Developments in Immunology, Vol. 1, p. 229. Elsevier, North Holland, Amsterdam.
19. Kovarik, J., Kuntz, L., Ryffel, B. and Borel, J. F. 1994. The viable motheaten (mev) mouse - a new model for arthritis. J. Autoimmun. 7:575.
20. + IgM autoantibodies in lupus prone motheaten mice. Int. Immunol. 9:655.
21. κ gene family expression and pairing occurs among B lymphocytes in autoimmune motheaten mice. Autoimmunity 21:185.
22. Pani, G., Siminovitch, K. A. and Paige, C. J. 1997. The motheaten mutation rescues B cell signalling and development in CD45-deficient mice. J. Exp. Med. 181:581.
23. Yancopoulos, G. D. and Alt, F. W. 1985. Developmentally controlled and tissue-specific expression of unrearranged VH gene segments. Cell 40:271.
24. Kabat, E. A., Wu, T. T., Perry, H. M., Gottesman, K. S. and Foeller, C. 1991. Sequences of proteins of immunological interest, 5th edition. National Institute of Health, USA.
25. Altschul, S. F., Madden, T. L., Schaffer, A. A. et al. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25:3389.
26. H and junctional diversity in the fetal, adult and aged B cell repertoires. J. Immunol. 146:1996.
27. Feeney, A. J. 1990. Lack of N regions in fetal and neonatal mouse immunoglobulin VDJ junctional sequences. J. Exp. Med. 172: 1377.
28. Kyte, J. and Doolittle, R. F. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105.
29. SAS Institute Inc. SAS/STAT software (1997): Changes and enhancements through release 6.12. SAS Institute Inc., Cary, North Carolina. p. 1167.
30. Gu, H., Tarlinton, D., Muller, W., Rajewsky, K. and Forster, I. 1991. Most peripheral B cells in mice are ligand selected. J. Exp. Med. 173:1357.
31. Bothwell, A. L. M., Paskind, M., Reth, M., Imanishi-Kari, T., Rajewsky, K. and Baltimore, D. 1981. Heavy chain variable region contribution to the b-NP family of antibodies: Somatic mutation evident in a gamma-2a variable region. Cell 24:625.
32. Maizels, N. and Bothwell, A. L. M. 1985. The T-cell-independent immune response to the hapten NP uses a large repertoire of heavy chain genes. Cell 43:715.
33. Winter, E., Radbruch, A. and Krawinkel, U. 1985. Member of novel VH gene families are found in VDJ regions of polyclonally activated B-lymphocytes. EMBO J. 4:2861.
34. Blankenstein, T., Zoebelein, G. and Krawinkel, U. 1984. Analysis of immunoglobulin heavy chain V-region genes belonging to the V NP-gene family. Nucleic Acids Res. 12:6887.
35. Kaartinen, M., Pelkonen, E., Even, J. and Makela, O. 1988. V genes of the primary antibody response of C57BL/10 mice to the hapten phenyloxazolone. Eur. J. Immunol. 18:1095.
36. Ono, M., Yamamoto, T., Kyogoku, M. and Nose, M. 1995. Sequence analysis of the germ-line VH gene corresponding to a nephritogenic antibody in MRL/lpr lupus mice. Clin. Exp. Immunol. 100:284.
37. Both, G. W., Taylor, L., Pollard, J. W. and Steele, E. J. 1990. Distribution of mutations around rearranged heavy-chain antibody variable-region genes. Mol. Cell Biol. 10:5187.
38. H rearrangement by promoter-enhancer approximation. Mol. Cell Biol. 11:2096.
39. Nitschke, L., Kestler, J., Tallone, T., Pelkonen, S. and Pelkonen, J. 2001. Deletion of the DQ52 element within the Ig heavy chain locus leads to a selective reduction in VDJ recombination and altered D gene usage. J. Immunol. 166:2540.
40. Tsukada, S., Sugiyama, H., Oka, Y. and Kishimito, S. 1990. Estimation of D segment usage in initial D to JH joinings in a murine immature B cell line. J. Immunol. 144:643.
41. H repertoires formed at different stages of ontogeny and under different selection pressures. EMBO J. 14:1680.
42. Kantor, A. B., Merrill, C. E., Herzenberg, L. A. and Hillson, L. L. 1997. An unbiased analysis of VH-D-JH sequences from B-1a, B-1b and conventional B cells. J. Immunol. 158:1175.
43. Santiago-Raber, M.-L., Laporte, C., Reninger, L. and Izui, S. 2004. Genetic basis of murine lupus. Autoimmun. Rev. 3:33.
44. Ivanov, I. I., Schelonka, R. L., Zhuang, Y., Gartland, G. L., Zemlin, M. and Schroder, H. W., 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.
45. Tillman, D. M., Jou, N. T., Hill, R. J. and Marion, T. N. 1992. Both IgM and IgG anti-DNA antibodies are the products of clonally selective B cell stimulation in (NZB × NZW)F1 mice. J. Exp. Med. 176:761.
46. Hentati, B., Payelle-Brogard, B., Jouanne, C., Avrameas, S. and Ternynck, T. 1994. Natural autoantibodies are involved in the haemolytic anaemia of NZB mice. J. Autoimmun. 7:425.
47. Matsiota, P., Druet, P., Dosquet, P., Guilbert, B. and Avrameas, S. 1987. Natural autoantibodies in systemic lupus erythematosus. Clin. Exp. Immunol. 69:79.
48. Chen, C., Stenzel-Poore, M. P. and Rittenberg, M. 1991. Natural auto- and polyreactive antibodies differing from antigen-induced antibodies in the H-chain CDR3. J. Immunol. 147:2359.
49. Dammers, P. M. and Kroese, G. M. 2005. Recruitment and selection of marginal zone B cells is independent of exogenous antigens. Eur. J. Immunol. 35:2089.
50. Haasner, D., Rolink, A. and Melchers, F. 1994. Influence of surrogate light chain on DHJH-reading frame 2 suppression in mouse precursor B cells. Int. Immunol. 6:21.
51. H rearrangements in newborn autoimmune MRL mice. J. Immunol. 162:1566.
52. Wang, C., Khalil, M., Ravetch, J. and Diamond, B. 2003. The naïve B cell repertoire predisposes to antigen induced systemic lupus erythematosus. J. Immunol. 170:4826.
53. Cancro, M. and Kearney, J. F. 2004. B cell positive selection: Roadmap to the primary repertoire? J. Immunol. 173:15.
54. Dorner, T., Farner, N. L. and Lipsky, P. E. 1999. Ig λ and heavy chain gene usage in early untreated systemic lupus erythematosus suggests intensive B cell stimulation. J. Immunol. 163:1027.
55. H gene rearrangements in a patient with systemic lupus erythematosus. Autoimmunity 33:61.
56. Dorner, T., Heimbacher, C., Farner, N. L. and Lipsky, P. E. 1999. Enhanced mutational activity of Vκ gene rearrangements in systemic lupus erythematosus. Clin. Immunol. 92:188.
57. Dorner, T., Kaschner, S., Hansen, A., Pruss, A. and Lipsky, P. E. 2001. Perturbations in the impact of mutational activity on Vλ genes in systemic lupus erythematosus. Arthritis Res. 3:368.
58. Bikah, G., Carey, J., Ciallella, J. R., Tarakhovsky, A. and Bondada, S. 1996. CD5-mediated negative regulation of antigen receptor-induced growth signals in B-1 B cells. Science 274:1906.
59. Sen, G., Bikah, G., Venkataraman, C. and Bondada, S. 1999. Negative regulation of antigen receptor-mediated signalling by constitutive association of CD5 with the SHP-1 protein tyrosine phosphatase in B-1 B cells. Eur. J. Immunol. 29:3319.
60. Joliat, M. J., Lang, P. A., Lyons, B. L. et al. 2002. Absence of CD5 dramatically reduces progression of pulmonary inflammatory lesions in SHP-1 protein-tyrosine phosphatase-deficient viable motheeaten mice. J. Autoimmun. 18:105.
61. Sen, G. H., Wu, H. J., Bikah, C. et al. 2002. Defective CD19-dependant signalling in B-1a and B-1b lymphocyte subpopulations. Mol. Immunol. 39:57.
62. Frances, R., Tumang, J. R. and Rothstein, L. 2005. 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. 175:27.
63. Pillai, S., Cariappa, A. and Moran, S. T. 2005. Marginal zone B cells. Annu. Rev. Immunol. 23:161.
64. Carter, J. D., Calabrese, G. M., Naganuma, M. and Lorenz, U. 2005. Deficiency of the Src homology region 2 domain-containing phosphatase 1 (SHP-1) causes enrichment of CD4+CD25+ regulatory T cells. J. Immunol. 174:6627.