Molecular mechanism and clinical impact of APOBEC3B-catalyzed mutagenesis in breast cancer

Breast Cancer Research

Volumn 17, Issue 1, 2015, Pages

  Harris, Reuben S ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 1; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; CYTOSINE DEAMINASE; DNA POLYMERASE; GENOMIC DNA; PROTEIN APOBEC3B; UNCLASSIFIED DRUG; APOBEC3B PROTEIN, HUMAN; CYTIDINE DEAMINASE;

BIOLOGICAL FUNCTIONS; BREAST CANCER; CANCER GROWTH; CANCER INCIDENCE; DEAMINATION; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA SEQUENCE; HUMAN; MUTAGENESIS; MUTATION RATE; REVIEW; BREAST NEOPLASMS; CATALYSIS; CELL TRANSFORMATION; DISEASE COURSE; FEMALE; GENETICS; INCIDENCE; METABOLISM; MULTIGENE FAMILY; MUTATION; PATHOLOGY; RADIATION RESPONSE;

BREAST NEOPLASMS; CATALYSIS; CELL TRANSFORMATION, NEOPLASTIC; CYTIDINE DEAMINASE; DISEASE PROGRESSION; DNA DAMAGE; FEMALE; HUMANS; INCIDENCE; MULTIGENE FAMILY; MUTAGENESIS; MUTATION;

EID: 84924303574     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/s13058-014-0498-3     Document Type: Review

References (72)

1. Stephens PJ, Tarpey PS, Davies H, Van Loo P, Greenman C, Wedge DC, Nik-Zainal S, Martin S, Varela I, Bignell GR, Yates LR, Papaemmanuil E, Beare D, Butler A, Cheverton A, Gamble J, Hinton J, Jia M, Jayakumar A, Jones D, Latimer C, Lau KW, McLaren S, McBride DJ, Menzies A, Mudie L, Raine K, Rad R, Chapman MS, Teague J, et al: The landscape of cancer genes and mutational processes in breast cancer. Nature 2012, 486:400-404.
2. Network CGA: Comprehensive molecular portraits of human breast tumours. Nature 2012, 490:61-70.
3. Ng CK, Pemberton HN, Reis-Filho JS: Breast cancer intratumor genetic heterogeneity: causes and implications. Expert Rev Anticancer Ther 2012, 12:1021-1032.
4. Hanahan D, Weinberg RA: Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
5. Couch FJ, Nathanson KL, Offit K: Two decades after BRCA: setting paradigms in personalized cancer care and prevention. Science 2014, 343:1466-1470.
6. Venkitaraman AR: Cancer suppression by the chromosome custodians, BRCA1 and BRCA2. Science 2014, 343:1470-1475.
7. Abdel-Rahman WM, Peltomaki P: Lynch syndrome and related familial colorectal cancers. Crit Rev Oncogenesis 2008, 14:1-22. discussion 23-31.
8. Kottemann MC, Smogorzewska A: Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature 2013, 493:356-363.
9. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz LA Jr, Kinzler KW: Cancer genome landscapes. Science 2013, 339:1546-1558.
10. Cleaver JE, Crowley E: UV damage, DNA repair and skin carcinogenesis. Front Biosci 2002, 7:d1024-d1043.
11. Hecht SS: Lung carcinogenesis by tobacco smoke. Int J Cancer 2012, 131:2724-2732.
12. Jia P, Pao W, Zhao Z: Patterns and processes of somatic mutations in nine major cancers. BMC Med Genomics 2014, 7:11.
13. Makridakis NM, Reichardt JK: Translesion DNA polymerases and cancer. Front Genet 2012, 3:174.
14. Yoon JH, Prakash L, Prakash S: Highly error-free role of DNA polymerase eta in the replicative bypass of UV-induced pyrimidine dimers in mouse and human cells. Proc Natl Acad Sci U S A 2009, 106:18219-18224.
15. Lehmann AR: DNA polymerases and repair synthesis in NER in human cells. DNA Repair (Amst) 2011, 10:730-733.
16. Di Noia JM, Neuberger MS: Molecular mechanisms of antibody somatic hypermutation. Annu Rev Biochem 2007, 76:1-22.
17. Burns MB, Lackey L, Carpenter MA, Rathore A, Land AM, Leonard B, Refsland EW, Kotandeniya D, Tretyakova N, Nikas JB, Yee D, Temiz NA, Donohue DE, McDougle RM, Brown WL, Law EK, Harris RS: APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 2013, 494:366-370.
18. Refsland EW, Harris RS: The APOBEC3 family of retroelement restriction factors. Curr Top Microbiol Immunol 2013, 371:1-27.
19. 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.
20. Petersen-Mahrt SK, Harris RS, Neuberger MS: AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 2002, 418:99-103.
21. Robbiani DF, Nussenzweig MC: Chromosome translocation, B cell lymphoma, and activation-induced cytidine deaminase. Annu Rev Pathol 2013, 8:79-103.
22. Blanc V, Davidson NO: C-to-U RNA editing: mechanisms leading to genetic diversity. J Biol Chem 2003, 278:1395-1398.
23. Rosenberg BR, Hamilton CE, Mwangi MM, Dewell S, Papavasiliou FN: Transcriptome-wide sequencing reveals numerous APOBEC1 mRNA-editing targets in transcript 3' UTRs. Nat Struct Mol Biol 2011, 18:230-236.
24. Petersen-Mahrt SK, Neuberger MS: In vitro deamination of cytosine to uracil in single-stranded DNA by apolipoprotein B editing complex catalytic subunit 1 (APOBEC1). J Biol Chem 2003, 278:19583-19586.
25. Koito A, Ikeda T: Intrinsic immunity against retrotransposons by APOBEC cytidine deaminases. Front Microbiol 2013, 4:28.
26. Yamanaka S, Balestra ME, Ferrell LD, Fan J, Arnold KS, Taylor S, Taylor JM, Innerarity TL: Apolipoprotein B mRNA-editing protein induces hepatocellular carcinoma and dysplasia in transgenic animals. Proc Natl Acad Sci U S A 1995, 92:8483-8487.
27. Saraconi G, Severi F, Sala C, Mattiuz G, Conticello SG: The RNA editing enzyme APOBEC1 induces somatic mutations and a compatible mutational signature is present in esophageal adenocarcinomas. Genome Biol 2014, 15:417.
28. Malim MH, Bieniasz PD: HIV restriction factors and mechanisms of evasion. Cold Spring Harb Perspectives Med 2012, 2:a006940.
29. Kunkel TA, Diaz M: Enzymatic cytosine deamination: friend and foe. Mol Cell 2002, 10:962-963.
30. 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.
31. Schumacher AJ, Nissley DV, Harris RS: APOBEC3G hypermutates genomic DNA and inhibits Ty1 retrotransposition in yeast. Proc Natl Acad Sci U S A 2005, 102:9854-9859.
32. Stephens P, Edkins S, Davies H, Greenman C, Cox C, Hunter C, Bignell G, Teague J, Smith R, Stevens C, O'Meara S, Parker A, Tarpey P, Avis T, Barthorpe A, Brackenbury L, Buck G, Butler A, Clements J, Cole J, Dicks E, Edwards K, Forbes S, Gorton M, Gray K, Halliday K, Harrison R, Hills K, Hinton J, Jones D, et al: A screen of the complete protein kinase gene family identifies diverse patterns of somatic mutations in human breast cancer. Nat Genet 2005, 37:590-592.
33. Sjöblom T, Jones S, Wood LD, Parsons DW, Lin J, Barber TD, Mandelker D, Leary RJ, Ptak J, Silliman N, Szabo S, Buckhaults P, Farrell C, Meeh P, Markowitz SD, Willis J, Dawson D, Willson JK, Gazdar AF, Hartigan J, Wu L, Liu C, Parmigiani G, Park BH, Bachman KE, Papadopoulos N, Vogelstein B, Kinzler KW, Velculescu VE: The consensus coding sequences of human breast and colorectal cancers. Science 2006, 314:268-274.
34. Wood LD, Parsons DW, Jones S, Lin J, Sjöblom T, Leary RJ, Shen D, Boca SM, Barber T, Ptak J, Silliman N, Szabo S, Dezso Z, Ustyanksky V, Nikolskaya T, Nikolsky Y, Karchin R, Wilson PA, Kaminker JS, Zhang Z, Croshaw R, Willis J, Dawson D, Shipitsin M, Willson JK, Sukumar S, Polyak K, Park BH, Pethiyagoda CL, Pant PV, et al: The genomic landscapes of human breast and colorectal cancers. Science 2007, 318:1108-1113.
35. Ehrlich M, Norris KF, Wang RY, Kuo KC, Gehrke CW: DNA cytosine methylation and heat-induced deamination. Biosci Rep 1986, 6:387-393.
36. Roberts SA, Sterling J, Thompson C, Harris S, Mav D, Shah R, Klimczak LJ, Kryukov GV, Malc E, Mieczkowski PA, Resnick MA, Gordenin DA: Clustered mutations in yeast and in human cancers can arise from damaged long single-strand DNA regions. Mol Cell 2012, 46:424-435.
37. Chan K, Sterling JF, Roberts SA, Bhagwat AS, Resnick MA, Gordenin DA: Base damage within single-strand DNA underlies in vivo hypermutability induced by a ubiquitous environmental agent. PLoS Genet 2012, 8:e1003149.
38. Nik-Zainal S, Alexandrov LB, Wedge DC, Van Loo P, Greenman CD, Raine K, Jones D, Hinton J, Marshall J, Stebbings LA, Menzies A, Martin S, Leung K, Chen L, Leroy C, Ramakrishna M, Rance R, Lau KW, Mudie LJ, Varela I, McBride DJ, Bignell GR, Cooke SL, Shlien A, Gamble J, Whitmore I, Maddison M, Tarpey PS, Davies HR, Papaemmanuil E, et al: Mutational processes molding the genomes of 21 breast cancers. Cell 2012, 149:979-993.
39. Nik-Zainal S, Van Loo P, Wedge DC, Alexandrov LB, Greenman CD, Lau KW, Raine K, Jones D, Marshall J, Ramakrishna M, Shlien A, Cooke SL, Hinton J, Menzies A, Stebbings LA, Leroy C, Jia M, Rance R, Mudie LJ, Gamble SJ, Stephens PJ, McLaren S, Tarpey PS, Papaemmanuil E, Davies HR, Varela I, McBride DJ, Bignell GR, Leung K, Butler AP, et al: The life history of 21 breast cancers. Cell 2012, 149:994-1007.
40. Bacolla A, Cooper DN, Vasquez KM: Mechanisms of base substitution mutagenesis in cancer genomes. Genes 2014, 5:108-146.
41. Burns MB, Temiz NA, Harris RS: Evidence for APOBEC3B mutagenesis in multiple human cancers. Nat Genet 2013, 45:977-983.
42. Lawrence MS, Stojanov P, Polak P, Kryukov GV, Cibulskis K, Sivachenko A, Carter SL, Stewart C, Mermel CH, Roberts SA, Kiezun A, Hammerman PS, McKenna A, Drier Y, Zou L, Ramos AH, Pugh TJ, Stransky N, Helman E, Kim J, Sougnez C, Ambrogio L, Nickerson E, Shefler E, Cortés ML, Auclair D, Saksena G, Voet D, Noble M, DiCara D, et al: Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 2013, 499:214-218.
43. Leonard B, Hart SN, Burns MB, Carpenter MA, Temiz NA, Rathore A, Vogel RI, Nikas JB, Law EK, Brown WL, Li Y, Zhang Y, Maurer MJ, Oberg AL, Cunningham JM, Shridhar V, Bell DA, April C, Bentley D, Bibikova M, Cheetham RK, Fan JB, Grocock R, Humphray S, Kingsbury Z, Peden J, Chien J, Swisher EM, Hartmann LC, Kalli KR, et al: APOBEC3B upregulation and genomic mutation patterns in serous ovarian carcinoma. Cancer Res 2013, 73:7222-7231.
44. Roberts SA, Lawrence MS, Klimczak LJ, Grimm SA, Fargo D, Stojanov P, Kiezun A, Kryukov GV, Carter SL, Saksena G, Harris S, Shah RR, Resnick MA, Getz G, Gordenin DA: An APOBEC cytidine deaminase mutagenesis pattern is widespread in human cancers. Nat Genet 2013, 45:970-976.
45. Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV, Bignell GR, Bolli N, Borg A, Børresen-Dale AL, Boyault S, Burkhardt B, Butler AP, Caldas C, Davies HR, Desmedt C, Eils R, Eyfjörd JE, Foekens JA, Greaves M, Hosoda F, Hutter B, Ilicic T, Imbeaud S, Imielinski M, Jäger N, Jones DT, Jones D, Knappskog S, Kool M, et al: Signatures of mutational processes in human cancer. Nature 2013, 500:415-421.
46. Henderson S, Chakravarthy A, Su X, Boshoff C, Fenton TR: APOBEC-mediated cytosine deamination links PIK3CA helical domain mutations to human papillomavirus-driven tumor development. Cell Rep 2014, 7:1833-1841.
47. TCGA: Comprehensive molecular characterization of urothelial bladder carcinoma. Nature 2014, 507:315-322.
48. Taylor BJ, Nik-Zainal S, Wu YL, Stebbings LA, Raine K, Campbell PJ, Rada C, Stratton MR, Neuberger MS: DNA deaminases induce break-associated mutation showers with implication of APOBEC3B and 3A in breast cancer kataegis. Elife 2013, 2:e00534.
49. Chan K, Resnick MA, Gordenin DA: The choice of nucleotide inserted opposite abasic sites formed within chromosomal DNA reveals the polymerase activities participating in translesion DNA synthesis. DNA Repair (Amst) 2013, 12:878-889.
50. Chen J, Miller BF, Furano AV: Repair of naturally occurring mismatches can induce mutations in flanking DNA. Elife (Cambridge) 2014, 3:e02001.
51. Friedman JI, Stivers JT: Detection of damaged DNA bases by DNA glycosylase enzymes. Biochemistry 2010, 49:4957-4967.
52. Drier Y, Lawrence MS, Carter SL, Stewart C, Gabriel SB, Lander ES, Meyerson M, Beroukhim R, Getz G: Somatic rearrangements across cancer reveal classes of samples with distinct patterns of DNA breakage and rearrangement-induced hypermutability. Genome Res 2013, 23:228-235.
53. Kidd JM, Newman TL, Tuzun E, Kaul R, Eichler EE: Population stratification of a common APOBEC gene deletion polymorphism. PLoS Genet 2007, 3:e63.
54. Nik-Zainal S, Wedge DC, Alexandrov LB, Petljak M, Butler AP, Bolli N, Davies HR, Knappskog S, Martin S, Papaemmanuil E, Ramakrishna M, Shlien A, Simonic I, Xue Y, Tyler-Smith C, Campbell PJ, Stratton MR: Association of a germline copy number polymorphism of APOBEC3A and APOBEC3B with burden of putative APOBEC-dependent mutations in breast cancer. Nat Genet 2014, 46:487-491.
55. Caval V, Suspene R, Shapira M, Vartanian JP, Wain-Hobson S: A prevalent cancer susceptibility APOBEC3A hybrid allele bearing APOBEC3B 3'UTR enhances chromosomal DNA damage. Nat Commun 2014, 5:5129.
56. Landry S, Narvaiza I, Linfesty DC, Weitzman MD: APOBEC3A can activate the DNA damage response and cause cell-cycle arrest. EMBO Rep 2011, 12:444-450.
57. Suspène R, Aynaud MM, Guetard D, Henry M, Eckhoff G, Marchio A, Pineau P, Dejean A, Vartanian JP, Wain-Hobson S: Somatic hypermutation of human mitochondrial and nuclear DNA by APOBEC3 cytidine deaminases, a pathway for DNA catabolism. Proc Natl Acad Sci U S A 2011, 108:4858-4863.
58. Aynaud MM, Suspene R, Vidalain PO, Mussil B, Guetard D, Tangy F, Wain-Hobson S, Vartanian JP: Human Tribbles 3 protects nuclear DNA from cytidine deamination by APOBEC3A. J Biol Chem 2012, 287:39182-39192.
59. Carpenter MA, Li M, Rathore A, Lackey L, Law EK, Land AM, Leonard B, Shandilya SM, Bohn MF, Schiffer CA, Brown WL, Harris RS: Methylcytosine and normal cytosine deamination by the foreign DNA restriction enzyme APOBEC3A. J Biol Chem 2012, 287:34801-34808.
60. Mussil B, Suspene R, Aynaud MM, Gauvrit A, Vartanian JP, Wain-Hobson S: Human APOBEC3A isoforms translocate to the nucleus and induce DNA double strand breaks leading to cell stress and death. PLoS One 2013, 8:e73641.
61. Shee C, Cox BD, Gu F, Luengas EM, Joshi MC, Chiu LY, Magnan D, Halliday JA, Frisch RL, Gibson JL, Nehring RB, Do HG, Hernandez M, Li L, Herman C, Hastings P, Bates D, Harris RS, Miller KM, Rosenberg SM: Engineered proteins detect spontaneous DNA breakage in human and bacterial cells. Elife 2013, 2:e01222.
62. Stenglein MD, Burns MB, Li M, Lengyel J, Harris RS: APOBEC3 proteins mediate the clearance of foreign DNA from human cells. Nat Struct Mol Biol 2010, 17:222-229.
63. Land AM, Law EK, Carpenter MA, Lackey L, Brown WL, Harris RS: Endogenous APOBEC3A DNA cytosine deaminase is cytoplasmic and nongenotoxic. J Biol Chem 2013, 288:17253-17260.
64. Vieira VC, Leonard B, White EA, Starrett GJ, Temiz NA, Lorenz LD, Lee D, Soares MA, Lambert PF, Howley PM, Harris RS: HPV E6 triggers upregulation of the antiviral and cancer genomic DNA deaminase APOBEC3B. MBio 2014, in press.
65. Ohba K, Ichiyama K, Yajima M, Gemma N, Nikaido M, Wu Q, Chong P, Mori S, Yamamoto R, Wong JE, Yamamoto N: In vivo and in vitro studies suggest a possible involvement of HPV infection in the early stage of breast carcinogenesis via APOBEC3B induction. PLoS One 2014, 9:e97787.
66. Komatsu A, Nagasaki K, Fujimori M, Amano J, Miki Y: Identification of novel deletion polymorphisms in breast cancer. Int J Oncol 2008, 33:261-270.
67. Xuan D, Li G, Cai Q, Deming-Halverson S, Shrubsole MJ, Shu XO, Kelley MC, Zheng W, Long J: APOBEC3 deletion polymorphism is associated with breast cancer risk among women of European ancestry. Carcinogenesis 2013, 34:2240-2243.
68. Long J, Delahanty RJ, Li G, Gao YT, Lu W, Cai Q, Xiang YB, Li C, Ji BT, Zheng Y, Ali S, Shu XO, Zheng W: A common deletion in the APOBEC3 genes and breast cancer risk. J Natl Cancer Inst 2013, 105:573-579.
69. Solyom S, Ewing AD, Rahrmann EP, Doucet T, Nelson HH, Burns MB, Harris RS, Sigmon DF, Casella A, Erlanger B, Wheelan S, Upton KR, Shukla R, Faulkner GJ, Largaespada DA, Kazazian HH Jr: Extensive somatic L1 retrotransposition in colorectal tumors. Genome Res 2012, 22:2328-2338.
70. Sieuwerts AM, Willis S, Burns MB, Look MP, Gelder ME, Schlicker A, Heideman MR, Jacobs H, Wessels L, Leyland-Jones B, Gray KP, Foekens JA, Harris RS, Martens JW: Elevated APOBEC3B correlates with poor outcomes for estrogen receptor-positive breast cancers. Horm Cancer 2014, in press.
71. Li M, Shandilya SM, Carpenter MA, Rathore A, Brown WL, Perkins AL, Harki DA, Solberg J, Hook DJ, Pandey KK, Parniak MA, Johnson JR, Krogan NJ, Somasundaran M, Ali A, Schiffer CA, Harris RS: First-in-class small molecule inhibitors of the single-strand DNA cytosine deaminase APOBEC3G. ACS Chem Biol 2012, 7:506-517.
72. Olson ME, Li M, Harris RS, Harki DA: Small-molecule APOBEC3G DNA cytosine deaminase inhibitors based on a 4-amino-1,2,4-triazole-3-thiol scaffold. ChemMedChem 2013, 8:112-117.