Reduced Switching in SCID B Cells Is Associated with Altered Somatic Mutation of Recombined S Regions

Journal of Immunology

Volumn 171, Issue 12, 2003, Pages 6556-6564

  Cook, Adam J L ^a   Oganesian, Liana ^a,b   Harumal, Pearly ^a   Basten, Antony ^a   Brink, Robert ^a   Jolly, Christopher J ^a  

^a Institute of Cancer Medicine and Cell Biology   (Australia)

^b CHILDREN'S MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CYTIDINE; CYTIDINE DEAMINASE; DNA; DNA DEPENDENT PROTEIN KINASE; DNA DEPENDENT PROTEIN KINASE CATALYTIC SUBUNIT PROTEIN; DOUBLE STRANDED DNA; HEN EGG LYSOZYME; HOMEODOMAIN PROTEIN; IMMUNOGLOBULIN CLASS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN M; LYSOZYME; PROTEIN; PROTEIN SERINE THREONINE KINASE; RAG 1 PROTEIN; RAG-1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL; ANIMAL CELL; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; BASE PAIRING; BIOSYNTHESIS; CELL CULTURE; CELL SURVIVAL; COMBINED IMMUNODEFICIENCY; CONTROLLED STUDY; CYTOLOGY; DEAMINATION; DNA STRAND BREAKAGE; DNA TEMPLATE; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVE SITE; GENE; GENE MUTATION; GENE REARRANGEMENT; GENE SWITCHING; GENETIC RECOMBINATION; GENETICS; IGH C GENE; IMMUNOGLOBULIN GENE; IMMUNOGLOBULIN V(D)J RECOMBINATION; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGY; METABOLISM; MOUSE; MOUSE MUTANT; MOUSE STRAIN; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRITIONAL DEFICIENCY; PHYSIOLOGY; POINT MUTATION; PRIORITY JOURNAL; RAG1 GENE; SCID CELL; SCID MOUSE; SOMATIC MUTATION; TRANSGENE; TRANSGENIC MOUSE;

EID: 0345735841     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.171.12.6556     Document Type: Article

References (66)

1. Williams, G. T., C. J. Jolly, J. Kohler, and M. S. Neuberger. 2000. The contribution of somatic hypermutation to the diversity of serum immunoglobulin: dramatic increase with age. Immunity 13:409.
2. Muramatsu, M., K. Kinoshita, S. Fagarasan, S. Yamada, Y. Shinkai, and T. Honjo. 2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102:553.
3. Petersen-Mahrt, S. K., R. S. Harris, and M. S. Neuberger. 2002. AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 418:99.
4. Di Noia, J., and M. S. Neuberger. 2002. Altering the pathway of immunoglobulin hypermutation by inhibiting uracil-DNA glycosylase. Nature 419:43.
5. Rada, C., G. T. Williams, H. Nilsen, D. E. Barnes, T. Lindahl, and M. S. Neuberger. 2002. Immunoglobulin isotype switching is inhibited and somatic hypermutation perturbed in UNG-deficient mice. Curr. Biol. 12:1748.
6. Zeng, X., D. B. Winter, C. Kasmer, K. H. Kraemer, A. R. Lehmann, and P. J. Gearhart. 2001. DNA polymerase η is an A-T mutator in somatic hypermutation of immunoglobulin variable genes. Nat. Immun. 2:537.
7. Zan, H., A. Komori, Z. Li, A. Cerutti, A. Schaffer, M. F. Flajnik, M. Diaz, and P. Casali. 2001. The translesion DNA polymerase ζ plays a major role in Ig and bcl-6 somatic hypermutation. Immunity 14:643.
8. Faili, A., S. Aoufouchi, E. Flatter, Q. Gueranger, C. A. Reynaud, and J. C. Weill. 2002. Induction of somatic hypermutation in immunoglobulin genes is dependent on DNA polymerase ι. Nature 419:944.
9. Wuerffel, R. A., J. Du, R. J. Thompson, and A. L. Kenter. 1997. Ig Sγ3 DNA-specific double strand breaks are induced in mitogen-activated B cells and are implicated in switch recombination. J. Immunol. 159:4139.
10. Chen, X., K. Kinoshita, and T. Honjo. 2001. Variable deletion and duplication at recombination junction ends: implication for staggered double-strand cleavage in class-switch recombination. Proc. Natl. Acad. Sci. USA 98:13860.
11. Petersen, S., R. Casellas, B. Reina-San-Martin, H. T. Chen, M. J. Difilippantonio, P. C. Wilson, L. Hanitsch, A. Celeste, M. Muramatsu, D. R. Pilch, et al. 2001. AID is required to initiate Nbs1/γ-H2AX focus formation and mutations at sites of class switching. Nature 414:660.
12. Papavasiliou, F. N., and D. G. Schatz. 2002. The activation-induced deaminase functions in a postcleavage step of the somatic hypermutation process. J. Exp. Med. 195:1193.
13. Bross, L., M. Muramatsu, K. Kinoshita, T. Honjo, and H. Jacobs. 2002. DNA double-strand breaks: prior to but not sufficient in targeting hypermutation. J. Exp. Med. 195:1187.
14. Iwasato, T., A. Shimizu, T. Honjo, and H. Yamagishi. 1990. Circular DNA is excised by immunoglobulin class switch recombination. Cell 62:143.
15. Matsuoka, M., K. Yoshida, T. Maeda, S. Usuda, and H. Sakano. 1990. Switch circular DNA formed in cytokine-treated mouse splenocytes: evidence for intramolecular DNA deletion in immunoglobulin class switching. Cell 62:135.
16. von Schwedler, U., H. M. Jack, and M. Wabl. 1990. Circular DNA is a product of the immunoglobulin class switch rearrangement. Nature 345:452.
17. Karran, P. 2000. DNA double strand break repair in mammalian cells. Curr. Opin. Genet. Dev. 10:144.
18. Khanna, K. K., and S. P. Jackson. 2001. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 27:247.
19. Manis, J. P., Y. Gu, R. Lansford, E. Sonoda, R. Ferrini, L. Davidson, K. Rajewsky, and F. W. Alt. 1998. Ku70 is required for late B cell development and immunoglobulin heavy chain class switching. J. Exp. Med. 187:2081.
20. Casellas, R., A. Nussenzweig, R. Wuerffel, R. Pelanda, A. Reichlin, H. Suh, X. F. Qin, E. Besmer, A. Kenter, K. Rajewsky, and M. C. Nussenzweig. 1998. Ku80 is required for immunoglobulin isotype switching. EMBO J. 17:2404.
21. Reina-San-Martin, B., S. Difilippantonio, L. Hanitsch, R. F. Masilamani, A. Nussenzweig, and M. C. Nussenzweig. 2003. H2AX is required for recombination between immunoglobulin switch regions but not for intra-switch region recombination or somatic hypermutation. J. Exp. Med. 197:1767.
22. Danska, J. S., D. P. Holland, S. Mariathasan, K. M. Williams, and C. J. Guidos. 1996. Biochemical and genetic defects in the DNA-dependent protein kinase in murine scid lymphocytes. Mol. Cell. Biol. 16:5507.
23. Smith, G. C., and S. P. Jackson. 1999. The DNA-dependent protein kinase. Genes Dev. 13:916.
24. DiBiase, S. J., Z. C. Zeng, R. Chen, T. Hyslop, W. J. Curran, Jr., and G. Iliakis. 2000. DNA-dependent protein kinase stimulates an independently active, non-homologous, end-joining apparatus. Cancer Res. 60:1245.
25. Fukumura, R., R. Araki, A. Fujimori, Y. Tsutsumi, A. Kurimasa, G. C. Li, D. J. Chen, K. Tatsumi, and M. Abe. 2000. Signal joint formation is also impaired in DNA-dependent protein kinase catalytic subunit knockout cells. J. Immunol. 165:3883.
26. Smith, J., E. Riballo, B. Kysela, C. Baldeyron, K. Manolis, C. Masson, M. R. Lieber, D. Papadopoulo, and P. Jeggo. 2003. Impact of DNA ligase IV on the fidelity of end joining in human cells. Nucleic Acids Res. 31:2157.
27. Manis, J. P., D. Dudley, L. Kaylor, and F. W. Alt. 2002. IgH class switch recombination to IgG1 in DNA-PKcs-deficient B cells. Immunity 16:607.
28. Bosma, G. C., J. Kim, T. Urich, D. M. Fath, M. G. Cotticelli, N. R. Ruetsch, M. Z. Radic, and M. J. Bosma. 2002. DNA-dependent protein kinase activity is not required for immunoglobulin class switching. J. Exp. Med. 196:1483.
29. Phan, T. G., M. Amesbury, S. Gardam, J. Crosbie, J. Hasbold, P. D. Hodgkin, A. Basten, and R. Brink. 2003. B cell receptor-independent stimuli trigger immunoglobulin (Ig) class switch recombination and production of IgG autoantibodies by anergic self-reactive B cells. J. Exp. Med. 197:845.
30. + transgenic T cells in spontaneous inflammatory bowel disease in lymphopenic mice. J. Immunol. 162:7208.
31. Razi-Wolf, Z., L. D. Falo, Jr., and H. Reiser. 1994. Expression and function of the costimulatory molecule B7 on murine Langerhans cells: evidence for an alternative CTLA-4 ligand. Eur. J. Immunol. 24:805.
32. Kirkham, P. A., L. Santos-Argumedo, M. M. Harnett, and R. M. Parkhouse. 1994. Murine B-cell activation via CD38 and protein tyrosine phosphorylation. Immunology 83:513.
33. 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, et al. 1988. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 334:676.
34. Kehry, M. R., and B. Castle. 1994. Regulation of CD40 ligand expression and use of recombinant CD40 ligand for studying B cell growth and differentiation. Semin. Immunol. 6:287.
35. Lyons, A. B., and C. R. Parish. 1994. Determination of lymphocyte division by flow cytometry. J. Immunol. Methods 171:131.
36. Hasbold, J., A. V. Gett, J. S. Rush, E. Deenick, D. Avery, J. Jun, and P. D. Hodgkin. 1999. Quantitative analysis of lymphocyte differentiation and proliferation in vitro using carboxyfluorescein diacetate succinimidyl ester. Immunol. Cell Biol. 77:516.
37. Blunt, T., N. J. Finnie, G. E. Taccioli, G. C. Smith, J. Demengeot, T. M. Gottlieb, R. Mizuta, A. J. Varghese, F. W. Alt, P. A. Jeggo, and S. P. Jackson. 1995. Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair defects associated with the murine scid mutation. Cell 80:813.
38. Araki, R., A. Fujimori, K. Hamatani, K. Mita, T. Saito, M. Mori, R. Fukumura, M. Morimyo, M. Muto, M. Itoh, et al. 1997. Nonsense mutation at Tyr-4046 in the DNA-dependent protein kinase catalytic subunit of severe combined immune deficiency mice. Proc. Natl. Acad. Sci. USA 94:2438.
39. Rolink, A., F. Melchers, and J. Andersson. 1996. The SCID but not the RAG-2 gene product is required for Sμ-Sε heavy chain class switching. Immunity 5:319.
40. Lansford, R., J. P. Manis, E. Sonoda, K. Rajewsky, and F. W. Alt. 1998. Ig heavy chain class switching in Rag-deficient mice. Int. Immunol. 10:325.
41. Lieber, M. R., J. E. Hesse, S. Lewis, G. C. Bosma, N. Rosenberg, K. Mizuuchi, M. J. Bosma, and M. Gellert. 1988. The defect in murine severe combined immune deficiency: joining of signal sequences but not coding segments in V(D)J recombination. Cell 55:7.
42. Oettinger, M. A., D. G. Schatz, C. Gorka, and D. Baltimore. 1990. RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J recombination. Science 248:1517.
43. Nemazee, D. 2000. Receptor selection in B and T lymphocytes. Annu. Rev. Immunol. 18:19.
44. Hodgkin, P. D., J. H. Lee, and A. B. Lyons. 1996. B cell differentiation and isotype switching is related to division cycle number. J. Exp. Med. 184:277.
45. Hasbold, J., A. B. Lyons, M. R. Kehry, and P. D. Hodgkin. 1998. Cell division number regulates IgG1 and IgE switching of B cells following stimulation by CD40 ligand and IL-4. Eur. J. Immunol. 28:1040.
46. Deenick, E. K., J. Hasbold, and P. D. Hodgkin. 1999. Switching to IgG3, IgG2b, and IgA is division linked and independent, revealing a stochastic framework for describing differentiation. J. Immunol. 163:4707.
47. Altschul, S. F., W. Gish, W. Miller, E. W. Meyers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403.
48. Ehrenstein, M. R., C. Rada, A. M. Jones, C. Milstein, and M. S. Neuberger. 2001. Switch junction sequences in PMS2-deficient mice reveal a microhomology-mediated mechanism of Ig class switch recombination. Proc. Natl. Acad. Sci. USA 98:14553.
49. Schrader, C. E., J. Vardo, and J. Stavnezer. 2002. Role for mismatch repair proteins Msh2, Mlhl1 and Pms2 in immunoglobulin class switching shown by sequence analysis of recombination junctions. J. Exp. Med. 195:367.
50. Pan, Q., C. Petit-Frere, A. Lahdesmaki, H. Gregorek, K. H. Chrzanowska, and L. Hammarstrom. 2002. Alternative end joining during switch recombination in patients with ataxia-telangiectasia. Eur. J. Immunol. 32:1300.
51. Nagaoka, H., M. Muramatsu, N. Yamamura, K. Kinoshita, and T. Honjo. 2002. Activation-induced deaminase (AID)-directed hypermutation in the immunoglobulin Sμ region: implication of AID involvement in a common step of class switch recombination and somatic hypermutation. J. Exp. Med. 195:529.
52. Bertocci, B., L. Quint, F. Delbos, C. Garcia, C. A. Reynaud, and J. C. Weill. 1998. Probing immunoglobulin gene hypermutation with microsatellites suggests a nonreplicative short patch DNA synthesis process. Immunity 9:257.
53. Frey, S., B. Bertocci, F. Delbos, L. Quint, J. C. Weill, and C. A. Reynaud. 1998. Mismatch repair deficiency interferes with the accumulation of mutations in chronically stimulated B cells and not with the hypermutation process. Immunity 9:127.
54. Rada, C., M. R. Ehrenstein, M. S. Neuberger, and C. Milstein. 1998. Hot spot focusing of somatic hypermutation in MSH2-deficient mice suggests two stages of mutational targeting. Proc. Natl. Acad. Sci. USA 95:6953.
55. Schrader, C. E., J. Vardo, and J. Stavnezer. 2003. Mlh1 can function in antibody class switch recombination independently of Msh2. J. Exp. Med. 197:1377.
56. Keohavong, P., and W. G. Thilly. 1989. Fidelity of DNA polymerases in DNA amplification. Proc. Natl. Acad. Sci. USA 86:9253.
57. Peterson, S., A. Kurimasa, M. Oshimura, W. Dynan, E. Bradbury, and D. Chen. 1995. Loss of the catalytic subunit of the DNA-dependent protein kinase in DNA double-strand-break-repair mutant mammalian cells. Proc. Natl. Acad. Sci. USA 92:3171.
58. Grawunder, U., N. Finnie, S. P. Jackson, B. Riwar, and R. Jessberger. 1996. Expression of DNA-dependent protein kinase holoenzyme upon induction of lymphocyte differentiation and V(D)J recombination. Eur J. Biochem. 241:931.
59. Beamish, H. J., R. Jessberger, E. Riballo, A. Priestley, T. Blunt, B. Kysela, and P. A. Jeggo. 2000. The C-terminal conserved domain of DNA-PKcs, missing in the SCID mouse, is required for kinase activity. Nucleic Acids Res. 28:1506.
60. Gao, Y., J. Chaudhuri, C. Zhu, L. Davidson, D. T. Weaver, and F. W. Alt. 1998. A targeted DNA-PKcs-null mutation reveals DNA-PK-independent functions for KU in V(D)J recombination. Immunity 9:367.
61. Taccioli, G. E., A. G. Amatucci, H. J. Beamish, D. Gell, X. H. Xiang, M. I. Torres Arzayus, A. Priestley, S. P. Jackson, A. Marshak Rothstein, P. A. Jeggo, and V. L. Herrera. 1998. Targeted disruption of the catalytic subunit of the DNA-PK gene in mice confers severe combined immunodeficiency and radiosensitivity. Immunity 9:355.
62. Kurimasa, A., H. Ouyang, L. J. Dong, S. Wang, X. Li, C. Cordon-Cardo, D. J. Chen, and G. C. Li. 1999. Catalytic subunit of DNA-dependent protein kinase: impact on lymphocyte development and tumorigenesis. Proc. Natl. Acad. Sci. USA 96:1403.
63. cs) or recombination-activating gene (RAG)-1 activity. J. Exp. Med. 192:1509.
64. Yu, K., F. Chedin, C. L. Hsieh, T. E. Wilson, and M. R. Lieber. 2003. R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nat. Immun. 4:442.
65. Bransteitter, R., P. Pham, M. D. Scharff, and M. F. Goodman. 2003. Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase. Proc. Natl. Acad. Sci. USA 100:4102.
66. Ramiro, A. R., P. Stavropoulos, M. Jankovic, and M. C. Nussenzweig. 2003. Transcription enhances AID-mediated cytidine deamination by exposing single-stranded DNA on the nontemplate strand. Nat. Immun. 4:452.