Somatic mutations and activation-induced cytidine deaminase (AID) expression in established rheumatoid factor-producing lymphoblastoid cell line

Molecular Immunology

Volumn 44, Issue 4, 2007, Pages 494-505

  Gil, Yaniv ^a   Levy Nabot, Sarah ^a   Steinitz, Michael ^b   Laskov, Reuven ^a  

^a HEBREW UNIVERSITY   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

AID; B lymphocytes; Epstein Barr virus; Monoclonal antibodies; Rheumatoid factor; Somatic hypermutation

Indexed keywords

CYTIDINE DEAMINASE; RHEUMATOID FACTOR;

ANTIBODY SCREENING; ANTIGEN BINDING; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; EPSTEIN BARR VIRUS; GENE EXPRESSION; GENE IDENTIFICATION; GENE MUTATION; HUMAN; HUMAN CELL; LYMPHOBLASTOID CELL; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOMATIC MUTATION;

AMINO ACID SEQUENCE; CELL LINE, TRANSFORMED; CELL TRANSFORMATION, VIRAL; CYTIDINE DEAMINASE; ENZYME ACTIVATION; EPSTEIN-BARR VIRUS INFECTIONS; GENE REARRANGEMENT, B-LYMPHOCYTE; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNOGLOBULIN VARIABLE REGION; MOLECULAR SEQUENCE DATA; MUTATION; RHEUMATOID FACTOR; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN;

HUMAN HERPESVIRUS 4;

EID: 33748128977     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2006.02.012     Document Type: Article

References (58)

1. Albesiano E., Messmer B.T., Damle R.N., Allen S.L., Rai K.R., and Chiorazzi N. Activation-induced cytidine deaminase in chronic lymphocytic leukemia B cells: expression as multiple forms in a dynamic, variably sized fraction of the clone. Blood 102 (2003) 3333-3339
2. Allman D., Jain A., Dent A., Maile R.R., Selvaggi T., Kehry M.R., and Staudt L.M. BCL-6 expression during B-cell activation. Blood 87 (1996) 5257-5268
3. Altiok E., Klein G., Zech L., Uno M., Henriksson B.E., Battat S., Ono Y., and Ernberg I. Epstein-Barr virus-transformed pro-B cells are prone to illegitimate recombination between the switch region of the mu chain gene and other chromosomes. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 6333-6837
4. Bardwell P.D., Woo C.J., Wei K., Li Z., Martin A., Sack S.Z., Parris T., Edelmann W., and Scharff M.D. Altered somatic hypermutation and reduced class-switch recombination in exonuclease 1-mutant mice. Nat. Immunol. 5 (2004) 224-229
5. Berek C., and Milstein C. Mutation drift and repertoire shift in the maturation of the immune response. Immunol. Rev. 96 (1987) 23-41
6. Besmer E., Gourzi P., and Papavasiliou F.N. The regulation of somatic hypermutation. Curr. Opin. Immunol. 16 (2004) 241-245
7. Bransteitter R., Pham P., Scharff M.D., and Goodman M.F. Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 4102-4107
8. Cattoretti G., Chang C.C., Cechova K., Zhang J., Ye B.H., Falini B., Louie D.C., Offit K., Chaganti R.S., and Dalla-Favera R. BCL-6 protein is expressed in germinal-center B cells. Blood 86 (1995) 45-53
9. Chaudhuri J., Khuong C., and Alt F.W. Replication protein a interacts with AID to promote deamination of somatic hypermutation targets. Nature 430 (2004) 992-998
10. Chaudhuri J., Tian M., Khuong C., Chua K., Pinaud E., and Alt F.W. Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature 422 (2003) 726-730
11. Corper A.L., Sohi M.K., Bonagura V.R., Steinitz M., Jefferis R., Feinstein A., Beale D., Taussig M.J., and Sutton B.J. Structure of human IgM rheumatoid factor Fab bound to its autoantigen IgG Fc reveals a novel topology of antibody-antigen interaction. Nat. Struct. Biol. 4 (1997) 374-381
12. Denepoux S., Razanajaona D., Blanchard D., Meffre G., Capra J.D., Banchereau J., and Lebecque S. Induction of somatic mutation in a human B cell line in vitro. Immunity 6 (1997) 35-46
13. Dickerson S.K., Market E., Besmer E., and Papavasiliou F.N. AID mediates hypermutation by deaminating single stranded DNA. J. Exp. Med. 197 (2003) 1291-1296
14. Dorner T., Brezinschek H.P., Brezinschek R.I., Foster S.J., Domiati-Saad R., and Lipsky P.E. Analysis of the frequency and pattern of somatic mutations within nonproductively rearranged human variable heavy chain genes. J. Immunol. 158 (1997) 2779-2789
15. Fujita N., Jaye D.L., Geigerman C., Akyildiz A., Mooney M.R., Boss J.M., and Wade P.A. MTA3 and the Mi-2/NuRD complex regulate cell fate during B lymphocyte differentiation. Cell 119 (2004) 75-86
16. Geylis V., Kourilov V., Meiner Z., Nennesmo I., Bogdanovic N., and Steinitz M. Human monoclonal antibodies against amyloid-beta from healthy adults. Neurobiol. Aging 26 (2005) 597-606
17. Glasky M.S., and Reading C.L. Stability of specific immunoglobulin secretion by EBV-transformed lymphoblastoid cells and human-murine heterohybridomas. Hybridoma 8 (1989) 377-389
18. Harris R.S., Croom-Carter D.S., Rickinson A.B., and Neuberger M.S. Epstein-Barr virus and the somatic hypermutation of immunoglobulin genes in Burkitt's lymphoma cells. J. Virol. 75 (2001) 10488-10492
19. Harris R.S., Sale J.E., Petersen-Mahrt S.K., and Neuberger M.S. AID is essential for immunoglobulin V gene conversion in a cultured B cell line. Curr. Biol. 12 (2002) 435-438
20. He B., Raab-Traub N., Casali P., and Cerutti A. EBV-encoded latent membrane protein 1 cooperates with BAFF/BLyS and APRIL to induce T cell-independent Ig heavy chain class switching. J. Immunol. 171 (2003) 5215-5224
21. Kozbor D., and Roder J.C. Requirements for the establishment of high-titered human monoclonal antibodies against tetanus toxoid using the Epstein-Barr virus technique. J. Immunol. 127 (1981) 1275-1280
22. Kuppers R., Zhao M., Rajewsky K., and Hansmann M.L. Detection of clonal B cell populations in paraffin-embedded tissues by polymerase chain reaction. Am. J. Pathol. 143 (1993) 230-239
23. Levy S., Ben-Bassat H., Klein B., Rabinowitz R., Shlomai Z., Steinitz M., and Laskov FR. Expression of AID and BCL-6 genes in normal and EBV transformed B-lymphocytes. Proceedings of the 32th Meeting of the Israeli Immunological Society. Haifa, Israel (2003)
24. Li Z., Woo C.J., Iglesias-Ussel M.D., Ronai D., and Scharff M.D. The generation of antibody diversity through somatic hypermutation and class switch recombination. Genes Dev. 18 (2004) 1-11
25. Maizels N. Somatic hypermutation: how many mechanisms diversify V region sequences?. Cell 83 (1995) 9-12
26. Maniatis T., Fritch E.F., and Sambrook J. Molecular cloning: a laboratory manual. Cold spring Harbor laboratory (1989), Cold Spring Harbor, New York
27. Martin A., Bardwell P.D., Woo C.J., Fan M., Shulman M.J., and Scharff M.D. Activation-induced cytidine deaminase turns on somatic hypermutation in hybridomas. Nature 415 (2002) 802-806
28. McCarthy H., Wierda W.G., Barron L.L., Cromwell C.C., Wang J., Coombes K.R., Rangel R., Elenitoba-Johnson K.S., Keating M.J., and Abruzzo L.V. High expression of activation-induced cytidine deaminase (AID) and splice variants is a distinctive feature of poor-prognosis chronic lymphocytic leukemia. Blood 101 (2003) 4903-4908
29. Muramatsu M., Kinoshita K., Fagarasan S., Yamada S., Shinkai Y., and Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102 (2000) 553-563
30. Muramatsu M., Sankaranand V.S., Anant S., Sugai M., Kinoshita K., Davidson N.O., and Honjo T. Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells. J. Biol. Chem. 274 (1999) 18470-18476
31. Natvig J.B., Thompson K., Randen I., Steinitz M., Taussig M., Beale D., Barker P., Sletten K., Waalen K., and Forre O. Partial amino acid sequence analysis and variable subgroup determination (VH and VL) of a monoclonal rheumatoid factor derived from a rheumatoid arthritis patient. Scand. J. Rheumatol. 75 Suppl (1988) 127-132
32. Neuberger M.S., Di Noia J.M., Beale R.C., Williams G.T., Yang Z., and Rada C. Somatic hypermutation at A-T pairs: polymerase error versus dUTP incorporation. Nat. Rev. Immunol. 5 (2005) 171-178
33. Niedobitek G., Meru N., and Delecluse H.J. Epstein-Barr virus infection and human malignancies. Int. J. Exp. Pathol. 82 (2001) 149-170
34. Noguchi E., Shibasaki M., Inudou M., Kamioka M., Yokouchi Y., Yamakawa-Kobayashi K., Hamaguchi H., Matsui A., and Arinami T. Association between a new polymorphism in the activation-induced cytidine deaminase gene and atopic asthma and the regulation of total serum IgE levels. J. Allergy Clin. Immunol. 108 (2001) 382-386
35. Okazaki I.M., Hiai H., Kakazu N., Yamada S., Muramatsu M., Kinoshita K., and Honjo T. Constitutive expression of AID leads to tumorigenesis. J. Exp. Med. 197 (2003) 1173-1181
36. Onizuka T., Moriyama M., Yamochi T., Kuroda T., Kazama A., Kanazawa N., Sato K., Kato T., Ota H., and Mori S. BCL-6 gene product, a 92- to 98-kD nuclear phosphoprotein, is highly expressed in germinal center B cells and their neoplastic counterparts. Blood 86 (1995) 28-37
37. Pascual V., Victor K., Randen I., Thompson K., Steinitz M., Forre O., Fu S.M., Natvig J.B., and Capra J.D. Nucleotide sequence analysis of rheumatoid factors and polyreactive antibodies derived from patients with rheumatoid arthritis reveals diverse use of VH and VL gene segments and extensive variability in CDR-3. Scand. J. Immunol. 36 (1992) 349-362
38. Pasqualucci L., Neumeister P., Goossens T., Nanjangud G., Chaganti R.S., Kuppers R., and Dalla-Favera R. Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas. Nature 412 (2001) 341-346
39. Petersen-Mahrt S.K., Harris R.S., and Neuberger M.S. AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 418 (2002) 99-103
40. Rada C., Di Noia J.M., and Neuberger M.S. Mismatch recognition and uracil excision provide complementary paths to both Ig switching and the A/T-focused phase of somatic mutation. Mol. Cell. 16 (2004) 163-171
41. Ramiro A.R., Stavropoulos P., Jankovic M., and Nussenzweig M.C. Transcription enhances AID-mediated cytidine deamination by exposing single-stranded DNA on the nontemplate strand. Nat. Immunol. 4 (2003) 452-456
42. Revy P., Muto T., Levy Y., Geissmann F., Plebani A., Sanal O., Catalan N., Forveille M., Dufourcq-Labelouse R., Gennery A., Tezcan I., Ersoy F., Kayserili H., Ugazio A.G., Brousse N., Muramatsu M., Notarangelo L.D., Kinoshita K., Honjo T., Fischer A., and Durandy A. Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the Hyper-IgM syndrome (HIGM2). Cell 102 (2000) 565-575
43. Roder J.C., Cole S.P., and Kozbor D. The EBV-hybridoma technique. Meth. Enzymol. 121 (1986) 140-167
44. Rogozin I.B., and Diaz M. Cutting edge: DGYW/WRCH is a better predictor of mutability at G:C bases in Ig hypermutation than the widely accepted RGYW/WRCY motif and probably reflects a two-step activation-induced cytidine deaminase-triggered process. J. Immunol. 172 (2004) 3382-3384
45. Rosen A., and Klein G. UV light-induced immunoglobulin heavy-chain class switch in a human lymphoblastoid cell line. Nature 306 (1983) 189-190
46. Sale J.E., and Neuberger M.S. TdT-accessible breaks are scattered over the immunoglobulin V domain in a constitutively hypermutating B cell line. Immunity 9 (1998) 859-869
47. Shaffer A.L., Lin K.I., Kuo T.C., Yu X., Hurt E.M., Rosenwald A., Giltnane J.M., Yang L., Zhao H., Calame K., and Staudt L.M. Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity 17 (2002) 51-62
48. Sohi M.K., Corper A.L., Wan T., Steinitz M., Jefferis R., Beale D., He M., Feinstein A., Sutton B.J., and Taussig M.J. Crystallization of a complex between the Fab fragment of a human immunoglobulin M (IgM) rheumatoid factor (RF-AN) and the Fc fragment of human IgG4. Immunology 88 (1996) 636-641
49. Spillmann F.J., and Wabl M. Endogenous expression of activation-induced cytidine deaminase in cell line WEHI-231. J. Immunol. 173 (2004) 1858-1867
50. Steinitz M., Klein G., Koskimies S., and Makel O. EB virus-induced B lymphocyte cell lines producing specific antibody. Nature 269 (1977) 420-422
51. Steinitz M., and Tamir S. Human monoclonal autoimmune antibody produced in vitro: rheumatoid factor generated by Epstein-Barr virus-transformed cell line. Eur. J. Immunol. 12 (1982) 126-133
52. Steinitz M., Tamir S., Sela S.B., and Rosenmann E. The presence of non-isotype-specific antibodies in polyclonal anti-IgE reagents: demonstration of their binding to specifically selected Epstein-Barr virus-transformed cell lines. Cell. Immunol. 113 (1988) 10-19
53. Sugimoto M., Tahara H., Ide T., and Furuichi Y. Steps involved in immortalization and tumorigenesis in human B-lymphoblastoid cell lines transformed by Epstein-Barr virus. Cancer Res. 64 (2004) 3361-3364
54. Wabl M., Burrows P.D., von Gabain A., and Steinberg C. Hypermutation at the immunoglobulin heavy chain locus in a pre-B-cell line. Proc. Natl. Acad. Sci. U.S.A. 82 (1985) 479-482
55. Wabl M., Jack H.M., Meyer J., Beck-Engeser G., von Borstel R.C., and Steinberg C.M. Measurements of mutation rates in B lymphocytes. Immunol. Rev. 96 (1987) 91-107
56. Wu H., Pelkonen E., Knuutila S., and Kaartinen M. A human follicular lymphoma B cell line hypermutates its functional immunoglobulin genes in vitro. Eur. J. Immunol. 25 (1995) 3263-3269
57. Yoshikawa K., Okazaki I.M., Eto T., Kinoshita K., Muramatsu M., Nagaoka H., and Honjo T. AID enzyme-induced hypermutation in an actively transcribed gene in fibroblasts. Science 296 (2002) 2033-2036
58. Zan H., Cerutti A., Dramitinos P., Schaffer A., Li Z., and Casali P. Induction of Ig somatic hypermutation and class switching in a human monoclonal IgM + IgD + B cell line in vitro: definition of the requirements and modalities of hypermutation. J. Immunol. 162 (1999) 3437-3447