Comparison of the Differential Context-dependence of DNA Deamination by APOBEC Enzymes: Correlation with Mutation Spectra in Vivo

Journal of Molecular Biology

Volumn 337, Issue 3, 2004, Pages 585-596

  Beale, Rupert C L ^a   Petersen Mahrt, Svend K ^a,b   Watt, Ian N ^a   Harris, Reuben S ^a,c   Rada, Cristina ^a   Neuberger, Michael S ^a  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

AID; AID, activation induced deaminase; Antibody hypermutation; Cancer; Deamination; Retrovirus; THU, tetrahydrouridine

Indexed keywords

ACTIVATED INDUCED DEAMINASE; ANTIBODY; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 1; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; CYTIDINE DEAMINASE; DEAMINASE; DNA; ENZYME; IMMUNOGLOBULIN; MUTAGENIC AGENT; NUCLEOTIDE; RECOMBINANT ENZYME; UNCLASSIFIED DRUG;

ARTICLE; ASSAY; BACILLUS SUBTILIS; COMPARATIVE STUDY; CORRELATION ANALYSIS; DEAMINATION; DNA DETERMINATION; DNA STRAND; ENZYME ACTIVITY; ENZYME SPECIFICITY; GENE; GENE INACTIVATION; GENE SEQUENCE; GENE TARGETING; HUMAN IMMUNODEFICIENCY VIRUS; IN VITRO STUDY; IN VIVO STUDY; LYMPHOID TISSUE; LYMPHOMA; MUTATION; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN FAMILY; RETROVIRUS; SACB GENE; TUMOR; TUMOR SUPPRESSOR GENE;

BACILLUS SUBTILIS; UNIDENTIFIED RETROVIRUS;

EID: 1542328859     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.01.046     Document Type: Article

References (57)

1. Lindahl T. Instability and decay of the primary structure of DNA. Nature. 362:1993;709-715.
2. Muramatsu M., Sankaranand V.S., Anant S., Sugai M., Kinoshita K., Davidson N.O., 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.
3. Neuberger M.S., Harris R.S., Di Noia J., Petersen-Mahrt S.K. Immunity through DNA deamination. Trends Biochem. Sci. 28:2003;305-312.
4. Harris R.S., Bishop K.N., Sheehy A.M., Craig H.M., Petersen-Mahrt S.K., Watt I.N., et al. DNA deamination mediates innate immunity to retroviral infection. Cell. 113:2003;803-809.
5. Lecossier D., Bouchonnet F., Clavel F., Hance A.J. Hypermutation of HIV-1 DNA in the absence of the Vif protein. Science. 300:2003;1112.
6. Mangeat B., Turelli P., Caron G., Friedli M., Perrin L., Trono D. Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature. 424:2003;99-103.
7. Mariani R., Chen D., Schrofelbauer B., Navarro F., Konig R., Bollman B., et al. Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell. 114:2003;21-31.
8. Zhang H., Yang B., Pomerantz R.J., Zhang C., Arunachalam S.C., Gao L. The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature. 424:2003;94-98.
9. Blanc V., Davidson N.O. C-to-U RNA editing: mechanisms leading to genetic diversity. J. Biol. Chem. 278:2003;1395-1398.
10. Harris R.S., Petersen-Mahrt S.K., Neuberger M.S. RNA editing enzyme APOBEC1 and some of its homologs can act as DNA mutators. Mol. Cell. 10:2002;1247-1253.
11. Petersen-Mahrt S.K., Neuberger M.S. In vitro deamination of cytosine to uracil in single-stranded DNA by apolipoprotein B editing complex catalytic subunit 1 (APOBEC1). J. Biol. Chem. 278:2003;19583-19586.
12. Jarmuz A., Chester A., Bayliss J., Gisbourne J., Dunham I., Scott J., Navaratnam N. An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22. Genomics. 79:2002;285-296.
13. Kuppers R., Dalla-Favera R. Mechanisms of chromosomal translocations in B cell lymphomas. Oncogene. 20:2001;5580-5594.
14. Yamanaka S., Balestra M.E., Ferrell L.D., Fan J., Arnold K.S., Taylor S., et al. Apolipoprotein B mRNA-editing protein induces hepatocellular carcinoma and dysplasia in transgenic animals. Proc. Natl Acad. Sci. USA. 92:1995;8483-8487.
15. Okazaki I.M., Hiai H., Kakazu N., Yamada S., Muramatsu M., Kinoshita K., Honjo T. Constitutive expression of AID leads to tumorigenesis. J. Expt. Med. 197:2003;1173-1181.
16. Petersen-Mahrt S.K., Harris R.S., Neuberger M.S. AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature. 418:2002;99-103.
17. Bransteitter R., Pham P., Scharff M.D., Goodman M.F. Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase. Proc. Natl Acad. Sci. USA. 100:2003;4102-4107.
18. Chaudhuri J., Tian M., Khuong C., Chua K., Pinaud E., Alt F.W. Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature. 422:2003;726-730.
19. Dickerson S.K., Market E., Besmer E., Papavasiliou F.N. AID mediates hypermutation by deaminating single stranded DNA. J. Expt. Med. 197:2003;1291-1296.
20. Pham P., Bransteitter R., Petruska J., Goodman M.F. Processive AID-catalysed cytosine deamination on single-stranded DNA simulates somatic hypermutation. Nature. 424:2003;103-107.
21. Lawes M., Maloy S. MudSacI, a transposon with strong selectable and counterselectable markers: use for rapid mapping of chromosomal mutations in Salmonella typhimurium. J. Bacteriol. 177:1995;1383-1387.
22. MacGinnitie A.J., Anant S., Davidson N.O. Mutagenesis of apobec-1, the catalytic subunit of the mammalian apolipoprotein B mRNA editing enzyme, reveals distinct domains that mediate cytosine nucleoside deaminase, RNA binding, and RNA editing activity. J. Biol. Chem. 270:1995;14768-14775.
23. Papavasiliou F.N., Schatz D.G. The activation-induced deaminase functions in a postcleavage step of the somatic hypermutation process. J. Expt. Med. 195:2002;1193-1198.
24. Ashley G.W., Bartlett P.A. Inhibition of Escherichia coli cytidine deaminase by a phosphapyrimidine nucleoside. J. Biol. Chem. 259:1984;13621- 13627.
25. Cohen R.M., Wolfenden R. Cytidine deaminase from Escherichia coli. Purification, properties and inhibition by the potential transition state analog 3,4,5,6-tetrahydrouridine. J. Biol. Chem. 245:1971;7561-7565.
26. Ramiro A.R., Stavropoulos P., Jankovic M., Nussenzweig M.C. Transcription enhances AID-mediated cytidine deamination by exposing single-stranded DNA on the nontemplate strand. Nature Immunol. 4:2003;452-456.
27. Sohail A., Klapacz J., Samaranayake M., Ullah A., Bhagwat A.S. Human activation-induced cytidine deaminase causes transcription-dependent, strand-biased C to U deaminations. Nucl. Acids Res. 31:2003;2990-2994.
28. Yamanaka S., Poksay K.S., Arnold K.S., Innerarity T.L. A novel translational repressor mRNA is edited extensively in livers containing tumors caused by the transgene expression of the apoB mRNAS-editing enzyme. Genes Dev. 11:1997;321-333.
29. Sowden M., Hamm J.K., Smith H.C. Overexpression of APOBEC-1 results in mooring sequence-dependent promiscuous RNA editing. J. Biol. Chem. 271:1996;3011-3017.
30. Vartanian J.P., Meyerhans A., Asjo B., Wain-Hobson S. Selection, recombination, and G→A hypermutation of human immunodeficiency virus type 1 genomes. J. Virol. 65:1991;1779-1788.
31. Vartanian J.P., Henry M., Wain-Hobson S. Sustained G→A hypermutation during reverse transcription of an entire human immunodeficiency virus type 1 strain Vau group O genome. J. Gen. Virol. 83:2002;801-805.
32. Fitzgibbon J.E., Mazar S., Dubin D.T. A new type of G→A hypermutation affecting human immunodeficiency virus. AIDS Res. Hum. Retroviruses. 9:1993;833-838.
33. Borman A.M., Quillent C., Charneau P., Kean K.M., Clavel F. A highly defective HIV-1 group O provirus: evidence for the role of local sequence determinants in G→A hypermutation during negative-strand viral DNA synthesis. Virology. 208:1995;601-609.
34. Janini M., Rogers M., Birx D.R., McCutchan F.E. Human immunodeficiency virus type 1 DNA sequences genetically damaged by hypermutation are often abundant in patient peripheral blood mononuclear cells and may be generated during near-simultaneous infection and activation of CD4(+) T cells. J. Virol. 75:2001;7973-7986.
35. Klarmann G.J., Chen X., North T.W., Preston B.D. Incorporation of uracil into minus strand DNA affects the specificity of plus strand synthesis initiation during lentiviral reverse transcription. J. Biol. Chem. 278:2003;7902-7909.
36. Wagner S.D., Milstein C., Neuberger M.S. Codon bias targets mutation. Nature. 376:1995;732.
37. Rogozin I.B., Kolchanov N.A. Somatic hypermutagenesis in immunoglobulin genes. II. Influence of neighbouring base sequences on mutagenesis. Biochim. Biophys. Acta. 1171:1992;11-18.
38. Betz A., Rada C., Pannell R., Milstein C., Neuberger M.S. Passenger transgenes reveal intrinsic specificity of the antibody hypermutation mechanism: clustering, polarity, and specific hot spots. Proc. Natl Acad. Sci. USA. 90:1993;2385-2388.
39. Ta V.T., Nagaoka H., Catalan N., Durandy A., Fischer A., Imai K., et al. AID mutant analyses indicate requirement for class-switch-specific cofactors. Nature Immunol. 4:2003;843-848.
40. Rabbitts T.H., Baer R., Hamlyn P.H. Altered nucleotide sequences of a translocated c-myc gene in Burkitt lymphoma. Nature. 306:1983;760-765.
41. Migliazza A., Martinotti S., Chen W., Fusco C., Ye B.H., Knowles D.M., et al. Frequent somatic hypermutation of the 5′ noncoding region of the BCL6 gene in B-cell lymphoma. Proc. Natl Acad. Sci. USA. 92:1995;12520-12524.
42. Pasqualucci L., Migliazza A., Fracchiolla N., William C., Neri A., Baldini L., et al. BCL-6 mutations in normal germinal center B cells: evidence of somatic hypermutation acting outside Ig loci. Proc. Natl Acad. Sci. USA. 95:1998;11816-11821.
43. Shen H.M., Peters A., Baron B., Zhu X., Storb U. Mutation of BCL-6 gene in normal B cells by the process of somatic hypermutation of Ig genes. Science. 280:1998;1750-1752.
44. Pasqualucci L., Neumeister P., Goossens T., Nanjangud G., Chaganti R.S., Kuppers R., Dalla-Favera R. Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas. Nature. 412:2001;341-346.
45. Colgin L.M., Hackmann A.F.M., Emond M.J., Monnat R.J. The unexpected landscape of in vivo somatic mutation in a human epithelial cell lineage. Proc. Natl Acad. Sci. USA. 99:2002;1437-1442.
46. Link A.J., Phillips D., Church G.M. Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization. J. Bacteriol. 179:1997;6228-6237.
47. Haldimann A., Prahalad M.K., Fisher S.L., Kim S.K., Walsh C.T., Wanner B.L. Altered recognition mutants of the response regulator PhoB: a new genetic strategy for studying protein-protein interactions. Proc. Natl Acad. Sci. USA. 93:1996;14361-14366.
48. Haldimann A., Wanner B.L. Conditional-replication, integration, excision, and retrieval plasmid-host systems for gene structure-function studies of bacteria. J. Bacteriol. 183:2001;6384-6393.
49. Neidhardt F.C., Bloch P.L., Smith D.F. Culture medium for enterobacteria. J. Bacteriol. 119:1974;736-747.
50. Holmes E.C., Zhang L.Q., Simmonds P., Ludlam C.A., Brown A.J. Convergent and divergent sequence evolution in the surface envelope glycoprotein of human immunodeficiency virus type 1 within a single infected patient. Proc. Natl Acad. Sci. USA. 89:1992;4835-4839.
51. Rada C.A., Ehrenstein M.R., Neuberger M.S., Milstein C. Hot spot focusing of somatic hypermutation in MSH2-deficient mice suggests two stages of mutational targeting. Immunity. 9:1998;135-141.
52. Rada C., Williams G.T., Nilsen H., Barnes D.E., Lindahl T., Neuberger M.S. Immunoglobulin isotype switching is inhibited and somatic hypermutation perturbed in UNG-deficient mice. Curr. Biol. 12:2002;1748-1755.
53. Rada C., Milstein C. The intrinsic hypermutability of antibody heavy and light chain genes decays exponentially. EMBO J. 20:2001;4570-4576.
54. Ehrenstein M.R., Rada C., Jones A.-M., Milstein C., Neuberger M.S. Switch junction sequences in PMS2-deficient mice reveal a microhomology- mediated mechanism of immunoglobulin class switch recombination. Proc. Natl Acad. Sci. USA. 98:2001;14553-14558.
55. Wagner S.D., Elvin J.G., Norris P., McGregor J.M., Neuberger M.S. Somatic hypermutation of Ig genes in patients with xeroderma pigmentosum (XP-D). Int. Immunol. 8:1996;701-705.
56. Milstein C., Neuberger M.S., Staden R. Both DNA strands of antibody genes are hypermutation targets. Proc. Natl Acad. Sci. USA. 95:1998;8791-8794.
57. Olivier M., Eeles R., Hollstein M., Khan M.A., Harris C.C., Hainaut P. The IARC TP53 database: new online mutation analysis and recommendations to users. Hum. Mutat. 19:2002;607-614.