Expression of human AID in yeast induces mutations in context similar to the context of somatic hypermutation at G-C pairs in immunoglobulin genes

BMC Immunology

Volumn 6, Issue , 2005, Pages

  Mayorov, Vladimir I ^a   Rogozin, Igor B ^b,c   Adkison, Linda R ^a   Frahm, Christin ^e   Kunkel, Thomas A ^d   Pavlov, Youri I ^e,f  

^a MERCER UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c INSTITUTE OF CYTOLOGY AND GENETICS   (Russian Federation)

^d NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^e UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^f UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; CYTOSINE; DEAMINASE; GUANINE; THYMINE; URACIL DNA GLYCOSYLTRANSFERASE; AICDA (ACTIVATION INDUCED CYTIDINE DEAMINASE); AICDA (ACTIVATION-INDUCED CYTIDINE DEAMINASE); AMINO ACID TRANSPORTER; CAN1 PROTEIN, S CEREVISIAE; CYTIDINE DEAMINASE; CYTOSINE DEAMINASE; SACCHAROMYCES CEREVISIAE PROTEIN;

BASE PAIRING; CODON; CONTROLLED STUDY; DEAMINATION; ENZYME SPECIFICITY; EXPRESSION VECTOR; GENE EXPRESSION; GENE INSERTION; HYPOTHESIS; IMMUNOGLOBULIN GENE; MOUSE STRAIN; MUTAGENESIS; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; PROTEIN EXPRESSION; REVIEW; SOMATIC HYPERMUTATION; SOMATIC MUTATION; WILD TYPE; YEAST; ARTICLE; GENETICS; HUMAN; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE; SUPPRESSOR GENE;

AMINO ACID TRANSPORT SYSTEMS, BASIC; BASE PAIRING; CODON; CYTIDINE DEAMINASE; CYTOSINE DEAMINASE; GENES, IMMUNOGLOBULIN; GENES, SUPPRESSOR; HUMANS; MUTAGENESIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN; SUBSTRATE SPECIFICITY;

EID: 26444443118     PISSN: 14712172     EISSN: 14712172     Source Type: Journal    
DOI: 10.1186/1471-2172-6-10     Document Type: Review

References (99)

1. Tonegawa S: Somatic generation of antibody diversity. Nature 1983, 302:575-581.
2. Honjo T, Nakai S, Nishida Y, Kataoka T, Yamawaki-Kataoka Y, Takahashi N, Obata M, Shimizu A, Yaoita Y, Nikaido T, Ishida N: Rearrangements of immunoglobulin genes during differentiation and evolution. Immunol Rev 1981, 59:33-67.
3. Alt FW, Blackwell TK, Yancopoulos GD: Development of the primary antibody repertoire. Science 1987, 238:1079-1087.
4. Honjo T, Kinoshita K, Muramatsu M: Molecular mechanism of class switch recombination: linkage with somatic hypermutation. Annu Rev Immunol 2002, 20:165-196.
5. Kinoshita K, Honjo T: Linking class-switch recombination with somatic hypermutation. Nat Rev Mol Cell Biol 2001, 2:493-503.
6. Milstein C, Rada C: The maturation of immune responce. London: Academic Press; 1995.
7. Rogozin IB, Kolchanov NA: Somatic hypermutagenesis in immunoglobulin genes. II. Influence of neighbouring base sequences on mutagenesis. Biochim Biophys Acta 1992, 1171:11-18.
8. Rogozin IB, Diaz M: 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 2004, 172:3382-3384.
9. Rogozin IB, Pavlov YI, Bebenek K, Matsuda T, Kunkel TA: Somatic mutation hotspots correlate with DNA polymerase eta error spectrum. Nat Immunol 2001, 2:530-536.
10. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T: Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 2000, 102:553-563.
11. 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 AG, Brousse N, Muramatsu M, Notarangelo LD, Kinoshita K, Honjo T, Fischer A, Durandy A: Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the Hyper-IgM syndrome (HIGM2). Cell 2000, 102:565-575.
12. Durandy A, Honjo T: Human genetic defects in class-switch recombination (hyper-IgM syndromes). Curr Opin Immunol 2001, 13:543-548.
13. Yoshikawa K, Okazaki IM, Eto T, Kinoshita K, Muramatsu M, Nagaoka H, Honjo T: AID enzyme-induced hypermutation in an actively transcribed gene in fibroblasts. Science 2002, 296:2033-2036.
14. Okazaki IM, Kinoshita K, Muramatsu M, Yoshikawa K, Honjo T: The AID enzyme induces class switch recombination in fibroblasts. Nature 2002, 416:340-345.
15. Arakawa H, Hauschild J, Buerstedde JM: Requirement of the activation-induced deaminase (AID) gene for immunoglobulin gene conversion. Science 2002, 295:1301-1306.
16. Di Noia JM, Neuberger MS: Immunoglobulin gene conversion in chicken DT40 cells largely proceeds through an abasic site intermediate generated by excision of the uracil produced by AID-mediated deoxycytidine deamination. Eur J Immunol 2004, 34:504-508.
17. Durandy A, Hivroz C, Mazerolles F, Schiff C, Bernard F, Jouanguy E, Revy P, DiSanto JP, Gauchat JF, Bonnefoy JY, Casanova JL, Fischer A: Abnormal CD40-mediated activation pathway in B lymphocytes from patients with hyper-IgM syndrome and normal CD40 ligand expression. J Immunol 1997, 158:2576-2584.
18. Kuppers R: Somatic hypermutation and B cell receptor selection in normal and transformed human B cells. Ann N Y Acad Sci 2003, 987:173-179.
19. Okazaki IM, Hiai H, Kakazu N, Yamada S, Muramatsu M, Kinoshita K, Honjo T: Constitutive expression of AID leads to tumorigenesis. J Exp Med 2003, 197:1173-1181.
20. Honjo T, Muramatsu M, Fagarasan S: AID: how does it aid antibody diversity? Immunity 2004, 20:659-668.
21. Doi T, Kinoshita K, Ikegawa M, Muramatsu M, Honjo T: De novo protein synthesis is required for the activation-induced cytidine deaminase function in class-switch recombination. Proc Natl Acad Sci U S A 2003, 100:2634-2638.
22. Ito S, Nagaoka H, Shinkura R, Begum N, Muramatsu M, Nakata M, Honjo T: Activation-induced cytidine deaminase shuttles between nucleus and cytoplasm like apolipoprotein B mRNA editing catalytic polypeptide 1. Proc Natl Acad Sci U S A 2004, 101:1975-1980.
23. Poltoratsky V, Goodman MF, Scharff MD: Error-prone candidates vie for somatic mutation. J Exp Med 2000, 192:F27-30.
24. Petersen-Mahrt SK, Harris RS, Neuberger MS: AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 2002, 418:99-103.
25. Pavlov YI, Rogozin IB, Galkin AP, Aksenova AY, Hanaoka F, Rada C, Kunkel TA: Correlation of somatic hypermutation specificity and A-T base pair substitution errors by DNA polymerase eta during copying of a mouse immunoglobulin kappa light chain transgene. Proc Natl Acad Sci U S A 2002, 99:9954-9959.
26. Rada C, Williams GT, Nilsen H, Barnes DE, Lindahl T, Neuberger MS: Immunoglobulin isotype switching is inhibited and somatic hypermutation perturbed in UNG-deficient mice. Curr Biol 2002, 12:1748-1755.
27. Storb U, Stavnezer J: Immunoglobulin genes: generating diversity with AID and UNG. Curr Biol 2002, 12:R725-727.
28. Diaz M, Storb U: A novel cytidine deaminase AIDs in the delivery of error-prone polymerases to immunoglobulin genes. DNA Repair (Amst) 2003, 2:623-627.
29. Neuberger MS, Harris RS, Di Noia J, Petersen-Mahrt SK: Immunity through DNA deamination. Trends Biochem Sci 2003, 28:305-312.
30. Li Z, Woo CJ, Iglesias-Ussel MD, Ronai D, Scharff MD: The generation of antibody diversity through somatic hypermutation and class switch recombination. Genes Dev 2004, 18:1-11.
31. Bhagwat AS: DNA-cytosine deaminases: from antibody maturation to antiviral defense. DNA Repair (Amst) 2004, 3:85-89.
32. Barreto VM, Ramiro AR, Nussenzweig MC: Activation-induced deaminase: controversies and open questions. Trends Immunol 2005, 26:90-96.
33. Pham P, Bransteitter R, Goodman MF: Reward versus Risk: DNA cytidine deaminases triggering immunity and disease. Biochemistry 2005, 44:2703-2715.
34. Luo Z, Ronai D, Scharff MD: The role of activation-induced cytidine deaminase in antibody diversification, immunodeficiency, and B-cell malignancies. J Allergy Clin Immunol 2004, 114:726-735; quiz 736.
35. Martin A, Bardwell PD, Woo CJ, Fan M, Shulman MJ, Scharff MD: Activation-induced cytidine deaminase turns on somatic hypermutation in hybridomas. Nature 2002, 415:802-806.
36. Beale RC, Petersen-Mahrt SK, Watt IN, Harris RS, Rada C, Neuberger MS: Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: correlation with mutation spectra in vivo. J Mol Biol 2004, 337:585-596.
37. Lindahl T: DNA glycosylases, endonucleases for apurinic/apyrimidinic sites, and base excision-repair. Prog Nucleic Acid Res Mol Biol 1979, 22:135-192.
38. Harris RS, Petersen-Mahrt SK, Neuberger MS: RNA editing enzyme APOBEC1 and some of its homologs can act as DNA mutators. Mol Cell 2002, 10:1247-1253.
39. Bransteitter R, Pham P, Scharff MD, Goodman MF: Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase. Proc Natl Acad Sci U S A 2003, 100:4102-4107.
40. Pham P, Bransteitter R, Petruska J, Goodman MF: Processive AID-catalysed cytosine deamination on single-stranded DNA simulates somatic hypermutation. Nature 2003, 424:103-107.
41. Dickerson SK, Market E, Besmer E, Papavasiliou FN: AID mediates hypermutation by deaminating single stranded DNA. J Exp Med 2003, 197:1291-1296.
42. Ramiro AR, Stavropoulos P, Jankovic M, Nussenzweig MC: Transcription enhances AID-mediated cytidine deamination by exposing single-stranded DNA on the nontemplate strand. Nat Immunol 2003, 4:452-456.
43. Sohail A, Klapacz J, Samaranayake M, Ullah A, Bhagwat AS: Human activation-induced cytidine deaminase causes transcription-dependent, strand-biased C to U deaminations. Nucleic Acids Res 2003, 31:2990-2994.
44. Shen HM, Storb U: Activation-induced cytidine deaminase (AID) can target both DNA strands when the DNA is supercoiled. Proc Natl Acad Sci U S A 2004, 101:12997-13002.
45. Bransteitter R, Pham P, Calabrese P, Goodman MF: Biochemical analysis of hyper-mutational targeting by wild type and mutant AID. J Biol Chem 2004, 279:51612-51621.
46. Yu K, Huang FT, Lieber MR: DNA substrate length and surrounding sequence affect the activation-induced deaminase activity at cytidine. J Biol Chem 2004, 279:6496-6500.
47. Milstein C, Neuberger MS, Staden R: Both DNA strands of antibody genes are hypermutation targets. Proc Natl Acad Sci U S A 1998, 95:8791-8794.
48. Poltoratsky VP, Wilson SH, Kunkel TA, Pavlov YI: Recombinogenic phenotype of human activation-induced cytosine deaminase. J Immunol 2004, 172:4308-4313.
49. Pavlov YI, Shcherbakova PV, Kunkel TA: In vivo consequences of putative active site mutations in yeast DNA polymerases alpha, epsilon, delta, and zeta. Genetics 2001, 159:47-64.
50. Pavlov YI, Newlon CS, Kunkel TA: Yeast origins establish a strand bias for replicational mutagenesis. Mol Cell 2002, 10:207-213.
51. Di Noia J, Neuberger MS: Altering the pathway of immunoglobulin hypermutation by inhibiting uracil-DNA glycosylase. Nature 2002, 419:43-48.
52. Rattray AJ, Shafer BK, McGill CB, Strathern JN: The roles of REV3 and RAD57 in doublestrand-break-repair-induced mutagenesis of Saccharomyces cerevisiae. Genetics 2002, 162:1063-1077.
53. Kunz BA, Ramachandran K, Vonarx EJ: DNA sequence analysis of spontaneous mutagenesis in Saccharomyces cerevisiae. Genetics 1998, 148:1491-1505.
54. Tishkoff DX, Filosi N, Gaida GM, Kolodner RD: A novel mutation avoidance mechanism dependent on S. cerevisiae RAD27 is distinct from DNA mismatch repair. Cell 1997, 88:253-263.
55. Niimi A, Limsirichaikul S, Yoshida S, Iwai S, Masutani C, Hanaoka F, Kool ET, Nishiyama Y, Suzuki M: Palm mutants in DNA polymerases alpha and eta alter DNA replication fidelity and translesion activity. Mol Cell Biol 2004, 24:2734-2746.
56. Kang XL, Yadao F, Gietz RD, Kunz BA: Elimination of the yeast RAD6 ubiquitin conjugase enhances base-pair transitions and G.C->T.A transversions as well as transposition of the Ty element: implications for the control of spontaneous mutation. Genetics 1992, 130:285-294.
57. Foster SJ, Dorner T, Lipsky PE: Somatic hypermutation of VkappaJkappa rearrangements: targeting of RGYW motifs on both DNA strands and preferential selection of mutated codons within RGYW motifs. Eur J Immunol 1999, 29:4011-4021.
58. Spencer J, Dunn M, Dunn-Walters DK: Characteristics of sequences around individual nucleotide substitutions in IgVH genes suggest different GC and AT mutators. J Immunol 1999, 162:6596-6601.
59. Boursier L, Su W, Spencer J: Analysis of strand biased 'G'.C hypermutation in human immunoglobulin V(lambda) gene segments suggests that both DNA strands are targets for deamination by activation-induced cytidine deaminase. Mol Immunol 2004, 40:1273-1278.
60. Impellizzeri KJ, Anderson B, Burgers PM: The spectrum of spontaneous mutations in a Saccharomyces cerevisiae uracil-DNA-glycosylase mutant limits the function of this enzyme to cytosine deamination repair. J Bacteriol 1991, 173:6807-6810.
61. Rogozin IB, Pavlov YI, Kunkel TA: Response 1 to 'Smaller role for pol ? Nature Immunology 2001, 2:983-984.
62. Coffman JA, Rai R, Cooper TG: Genetic evidence for Gln3p-independent, nitrogen catabolite repression-sensitive gene expression in Saccharomyces cerevisiae. J Bacteriol 1995, 177:6910-6918.
63. Rinckel LA, Garfinkel DJ: Influences of histone stoichiometry on the target site preference of retrotransposons Ty1 and Ty2 in Saccharomyces cerevisiae. Genetics 1996, 142:761-776.
64. van der Merwe GK, Cooper TG, van Vuuren HJ: Ammonia regulates VID30 expression and Vid30p function shifts nitrogen metabolism toward glutamate formation especially when Saccharomyces cerevisiae is grown in low concentrations of ammonia. J Biol Chem 2001, 276:28659-28666.
65. Chaudhuri J, Tian M, Khuong C, Chua K, Pinaud E, Alt FW: Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature 2003, 422:726-730.
66. Hanawalt PC: Subpathways of nucleotide excision repair and their regulation. Oncogene 2002, 21:8949-8956.
67. Rada C, Di Noia JM, Neuberger MS: Mismatch recognition and uracil excision provide complementary paths to both Ig switching and the A/T-focused phase of somatic mutation. Mol Cell 2004, 16:163-171.
68. Wilson TM, Vaisman A, Martomo SA, Sullivan P, Lan L, Hanaoka F, Yasui A, Woodgate R, Gearhart PJ: MSH2-MSH6 stimulates DNA polymerase eta, suggesting a role for A:T mutations in antibody genes. J Exp Med 2005, 201:637-645.
69. Matsuda T, Bebenek K, Masutani C, Rogozin IB, Hanaoka F, Kunkel TA: Error rate and specificity of human and murine DNA polymerase eta. J Mol Biol 2001, 312:335-346.
70. Zeng X, Winter DB, Kasmer C, Kraemer KH, Lehmann AR, Gearhart PJ: DNA polymerase eta is an A-T mutator in somatic hypermutation of immunoglobulin variable genes. Nat Immunol 2001, 2:537-541.
71. Chaudhuri J, Khuong C, Alt FW: Replication protein A interacts with AID to promote deamination of somatic hypermutation targets. Nature 2004, 430:992-998.
72. Kunkel TA, Pavlov YI, Bebenek K: Functions of human DNA polymerases eta, kappa and iota suggested by their properties, including fidelity with undamaged DNA templates. DNA Repair (Amst) 2003, 2:135-149.
73. Poltoratsky V, Woo CJ, Tippin B, Martin A, Goodman MF, Scharff MD: Expression of error-prone polymerases in BL2 cells activated for Ig somatic hypermutation. Proc Natl Acad Sci U S A 2001, 98:7976-7981.
74. Faili A, Aoufouchi S, Flatter E, Gueranger Q, Reynaud CA, Weill JC: Induction of somatic hypermutation in immunoglobulin genes is dependent on DNA polymerase iota. Nature 2002, 419:944-947.
75. McDonald JP, Frank EG, Plosky BS, Rogozin IB, Masutani C, Hanaoka F, Woodgate R, Gearhart PJ: 129-derived strains of mice are deficient in DNA polymerase iota and have normal immunoglobulin hypermutation. J Exp Med 2003, 198:635-643.
76. Tissier A, Frank EG, McDonald JP, Vaisman A, Fernandez de Henestrosa AR, Boudsocq F, McLenigan MP, Woodgate R: Biochemical characterization of human DNA polymerase iota provides clues to its biological function. Biochem Soc Trans 2001, 29(Pt 2):183-187.
77. Zan H, Komori A, Li Z, Cerutti A, Schaffer A, Flajnik MF, Diaz M, Casali P: The translesion DNA polymerase zeta plays a major role in Ig and bcl-6 somatic hypermutation. Immunity 2001, 14:643-653.
78. Goodman MF: Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu Rev Biochem 2002, 71:17-50.
79. Neuberger MS, Di Noia JM, Beale RC, Williams GT, Yang Z, Rada C: Somatic hypermutation at A.T pairs: polymerase error versus dUTP incorporation. Nat Rev Immunol 2005, 5:171-178.
80. Nilsen H, Rosewell I, Robins P, Skjelbred CF, Andersen S, Slupphaug G, Daly G, Krokan HE, Lindahl T, Barnes DE: Uracil-DNA glycosylase (UNG)-deficient mice reveal a primary role of the enzyme during DNA replication. Mol Cell 2000, 5:1059-1065.
81. Barnes DE, Lindahl T: Repair and Genetic Consequences of Endogenous DNA Base Damage in Mammalian Cells. Annu Rev Genet 2004, 38:445-476.
82. Woo CJ, Martin A, Scharff MD: Induction of somatic hypermutation is associated with modifications in immunoglobulin variable region chromatin. Immunity 2003, 19:479-489.
83. Bennetzen JL, Hall BD: Codon selection in yeast. J Biol Chem 1982, 257:3026-3031.
84. Jansen R, Bussemaker HJ, Gerstein M: Revisiting the codon adaptation index from a whole-genome perspective: analyzing the relationship between gene expression and codon occurrence in yeast using a variety of models. Nucleic Acids Res 2003, 31:2242-2251.
85. Pavlov YI, Nguyen D, Kunkel TA: Mutator effects of overproducing DNA polymerase eta (Rad30) and its catalytically inactive variant in yeast. Mutat Res 2001,478:129-139.
86. Shcherbakova PV, Noskov VN, Pshenichnov MR, Pavlov YI: Base analog 6-N-hydroxylaminopurine mutagenesis in the yeast Saccharomyces cerevisiae is controlled by replicative DNA polymerases. Mutat Res 1996, 369:33-44.
87. Shcherbakova PV, Pavlov YI: 3′-->5′ exonucleases of DNA polymerases epsilon and delta correct base analog induced DNA replication errors on opposite DNA strands in Saccharomyces cerevisiae. Genetics 1996, 142:717-726.
88. Calderon IL, Contopoulou CR, Mortimer RK: Isolation of a DNA fragment that is expressed as an amber suppressor when present in high copy number in yeast. Gene 1984, 29:69-76.
89. Achilli A, Matmati N, Casalone E, Morpurgo G, Lucaccioni A, Pavlov YI, Babudri N: The exceptionally high rate of spontaneous mutations in the polymerase delta proofreading exonuclease-deficient Saccharomyces cerevisiae strain starved for adenine. BMC Genet 2004, 5:34.
90. Shcherbakova PV, Kunkel TA: Mutator phenotypes conferred by MLH1 overexpression and by heterozygosity for mlh1 mutations. Mol Cell Biol 1999, 19:3177-3183.
91. Kozmin SG, Pavlov YI, Kunkel TA, Sage E: Roles of Saccharomyces cerevisiae DNA polymerases Poleta and Polzeta in response to irradiation by simulated sunlight. Nucleic Acids Res 2003, 31:4541-4552.
92. Betz AG, Rada C, Pannell R, Milstein C, Neuberger MS: Passenger transgenes reveal intrinsic specificity of the antibody hypermutation mechanism: clustering, polarity, and specific hot spots. Proc Natl Acad Sci U S A 1993, 90:2385-2388.
93. Gonzalez-Fernandez A, Milstein C: Analysis of somatic hypermutation in mouse Peyer's patches using immunoglobulin kappa light-chain transgenes. Proc Natl Acad Sci U S A 1993, 90:9862-9866.
94. Adams WT, Skopek TR: Statistical test for the comparison of samples from mutational spectra. J Mol Biol 1987, 194:391-396.
95. Khromov-Borisov NN, Rogozin IB, Pegas Henriques JA, de Serres FJ: Similarity pattern analysis in mutational distributions. Mutat Res 1999, 430:55-74.
96. Ng PC, Henikoff S: SIFT: Predicting amino acid changes that affect protein function. Nucleic Acids Res 2003, 31:3812-3814.
97. Glazko GV, Milanesi L, Rogozin IB: The subclass approach for mutational spectrum analysis: application of the SEM algorithm. J Theor Biol 1998, 192:475-487.
98. Rogozin IB, Kondrashov FA, Glazko GV: Use of mutation spectra analysis software. Hum Mutation 2001, 17:83-102.
99. Rogozin IB, Pavlov YI: Theoretical analysis of mutation hotspots and their DNA sequence context specificity. Mutat Res 2003, 544:65-85.