APOBEC3A functions as a restriction factor of human papillomavirus

Journal of Virology

Volumn 89, Issue 1, 2015, Pages 688-702

  Warren, Cody J ^a   Xu, Tao ^a   Guo, Kejun ^a   Griffin, Laura M ^a   Westrich, Joseph A ^a   Lee, Denis ^b   Lambert, Paul F ^b   Santiago, Mario L ^a   Pyeon, Dohun ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B MRNA EDITING ENZYME CATALYTIC POLYPEPTIDE LIKE 3A; APOLIPOPROTEIN B MRNA EDITING ENZYME CATALYTIC POLYPEPTIDE LIKE 3B; CYTIDINE DEAMINASE; PROTEIN E7; UNCLASSIFIED DRUG; VIRUS DNA; APOBEC3A PROTEIN, HUMAN; PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVITY; FEMALE; GENE OVEREXPRESSION; HA3A GENE; HA3B GENE; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; IN VIVO STUDY; INNATE IMMUNITY; KERATINOCYTE; MOUSE; NONHUMAN; PAPILLOMAVIRUS INFECTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; UTERINE CERVIX CANCER; VIRION; VIRUS CARCINOGENESIS; VIRUS GENOME; VIRUS VIRULENCE; WART VIRUS; ANIMAL; C57BL MOUSE; GENE EXPRESSION PROFILING; IMMUNOLOGY; METABOLISM; PAPILLOMAVIRIDAE; PATHOLOGY; UTERINE CERVIX; VIROLOGY;

DNA VIRUSES; HUMAN PAPILLOMAVIRUS; PAPILLOMAVIRIDAE;

ANIMALS; CERVIX UTERI; CYTIDINE DEAMINASE; FEMALE; GENE EXPRESSION PROFILING; HUMANS; KERATINOCYTES; MICE, INBRED C57BL; PAPILLOMAVIRIDAE; PROTEINS;

EID: 84919459598     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02383-14     Document Type: Article

References (79)

1. Parkin DM, Bray F. 2006. Chapter 2: the burden of HPV-related cancers. Vaccine 24(Suppl 3):S11-S25. http://dx.doi.org/10.1016/j.vaccine.2006.05.111.
2. Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, Kim E, Jiang B, Goodman MT, Sibug-Saber M, Cozen W, Liu L, Lynch CF, Wentzensen N, Jordan RC, Altekruse S, Anderson WF, Rosenberg PS, Gillison ML. 2011. Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol 29:4294-4301. http://dx.doi.org/10.1200/JCO.2011.36.4596.
3. Jabbar SF, Abrams L, Glick A, Lambert PF. 2009. Persistence of highgrade cervical dysplasia and cervical cancer requires the continuous expression of the human papillomavirus type 16 E7 oncogene. Cancer Res 69:4407-4414. http://dx.doi.org/10.1158/0008-5472.CAN-09-0023.
4. Richardson H, Kelsall G, Tellier P, Voyer H, Abrahamowicz M, Ferenczy A, Coutlée F, Franco EL. 2003. The natural history of type-specific human papillomavirus infections in female university students. Cancer Epidemiol Biomarkers Prev 12:485-490.
5. Stanley M. 2008. Immunobiology of HPV and HPV vaccines. Gynecol Oncol 109:S15-S21. http://dx.doi.org/10.1016/j.ygyno.2008.02.003.
6. Bodily J, Laimins LA. 2011. Persistence of human papillomavirus infection: keys to malignant progression. Trends Microbiol 19:33-39. http://dx.doi.org/10.1016/j.tim.2010.10.002.
7. Stanley MA. 2012. Epithelial cell responses to infection with human papillomavirus. Clin Microbiol Rev 25:215-222. http://dx.doi.org/10.1128/CMR.05028-11.
8. Woo YL, van den Hende M, Sterling JC, Coleman N, Crawford RAF, Kwappenberg KMC, Stanley MA, van der Burg SH. 2010. A prospective study on the natural course of low-grade squamous intraepithelial lesions and the presence of HPV16 E2-, E6-and E7-specific T-cell responses. Int J Cancer 126:133-141. http://dx.doi.org/10.1002/ijc.24804.
9. Welters MJP, de Jong A, van den Eeden SJF, van der Hulst JM, Kwappenberg KMC, Hassane S, Franken KLMC, Drijfhout JW, Fleuren GJ, Kenter G, Melief CJM, Offringa R, van der Burg SH. 2003. Frequent display of human papillomavirus type 16 E6-specific memory T-helper cells in the healthy population as witness of previous viral encounter. Cancer Res 63:636-641.
10. de Jong A, van der Burg SH, Kwappenberg KMC, van der Hulst JM, Franken KLMC, Geluk A, van Meijgaarden KE, Drijfhout JW, Kenter G, Vermeij P, Melief CJM, Offringa R. 2002. Frequent detection of human papillomavirus 16 E2-specific T-helper immunity in healthy subjects. Cancer Res 62:472-479.
11. Stanley MA. 2009. Immune responses to human papilloma viruses. Indian J Med Res 130:266-276.
12. Sheehy AM, Gaddis NC, Choi JD, Malim MH. 2002. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418:646-650. http://dx.doi.org/10.1038/nature00939.
13. Zheng Y-H, Irwin D, Kurosu T, Tokunaga K, Sata T, Peterlin BM. 2004. Human APOBEC3F is another host factor that blocks human immunodeficiency virus type 1 replication. J Virol 78:6073-6076. http://dx.doi.org/10.1128/JVI.78.11.6073-6076.2004.
14. Hultquist JF, Lengyel JA, Refsland EW, LaRue RS, Lackey L, Brown WL, Harris RS. 2011. Human and rhesus APOBEC3D, APOBEC3F, APOBEC3G, and APOBEC3H demonstrate a conserved capacity to restrict Vif-deficient HIV-1. J Virol 85:11220-11234. http://dx.doi.org/10.1128/JVI.05238-11.
15. Jarmuz A, Chester A, Bayliss J, Gisbourne J, Dunham I, Scott J, Navaratnam N. 2002. An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22. Genomics 79:285-296. http://dx.doi.org/10.1006/geno.2002.6718.
16. LaRue RS, Andrésdóttir V, Blanchard Y, Conticello SG, Derse D, Emerman M, Greene WC, Jónsson SR, Landau NR, Löchelt M, Malik HS, Malim MH, Münk C, O'Brien SJ, Pathak VK, Strebel K, Wain-Hobson S, Yu X-F, Yuhki N, Harris RS. 2009. Guidelines for naming nonprimate APOBEC3 genes and proteins. J Virol 83:494-497. http://dx.doi.org/10.1128/JVI.01976-08.
17. Chelico L, Pham P, Calabrese P, Goodman MF. 2006. APOBEC3G DNA deaminase acts processively 3'→5' on single-stranded DNA. Nat Struct Mol Biol 13:392-399. http://dx.doi.org/10.1038/nsmb1086.
18. Yu Q, König R, Pillai S, Chiles K, Kearney M, Palmer S, Richman D, Coffin JM, Landau NR. 2004. Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat Struct Mol Biol 11:435-442. http://dx.doi.org/10.1038/nsmb758.
19. Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SAJR, Behjati S, Biankin AV, Bignell GR, Bolli N, Borg Å, Børresen-Dale A-L, 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, Imielinsk M, Jäger N, Jones DTW, Jones D, Knappskog S, Kool M, Lakhani SR, López-Otín C, Martin S, Munshi NC, Nakamura H, Northcott PA, Pajic M, Papaemmanuil E, Paradiso A, Pearson JV, Puente XS, Raine K, Ramakrishna M, Richardson AL, Richter J, Rosenstiel P, Schlesner M, Schumacher TN, Span PN, Teague JW, et al. 2013. Signatures of mutational processes in human cancer. Nature 500:415-421. http://dx.doi.org/10.1038/nature12477.
20. Chen H, Lilley CE, Yu Q, Lee DV, Chou J, Narvaiza I, Landau NR, Weitzman MD. 2006. APOBEC3A is a potent inhibitor of adenoassociated virus and retrotransposons. Curr Biol 16:480-485. http://dx.doi.org/10.1016/j.cub.2006.01.031.
21. Narvaiza I, Linfesty DC, Greener BN, Hakata Y, Pintel DJ, Logue E, Landau NR, Weitzman MD. 2009. Deaminase-independent inhibition of parvoviruses by the APOBEC3A cytidine deaminase. PLoS Pathog 5:e1000439. http://dx.doi.org/10.1371/journal.ppat.1000439.
22. Schmitt K, Guo K, Algaier M, Ruiz A, Cheng F, Qiu J, Wissing S, Santiago ML, Stephens EB. 2011. Differential virus restriction patterns of rhesus macaque and human APOBEC3A: implications for lentivirus evolution. Virology 419:24-42. http://dx.doi.org/10.1016/j.virol.2011.07.017.
23. Suspène R, Aynaud M-M, Koch S, Pasdeloup D, Labetoulle M, Gaertner B, Vartanian J-P, Meyerhans A, Wain-Hobson S. 2011. Genetic editing of herpes simplex virus 1 and Epstein-Barr herpesvirus genomes by human APOBEC3 cytidine deaminases in culture and in vivo. J Virol 85:7594-7602. http://dx.doi.org/10.1128/JVI.00290-11.
24. Vartanian J-P, Guétard D, Henry M, Wain-Hobson S. 2008. Evidence for editing of human papillomavirus DNA by APOBEC3 in benign and precancerous lesions. Science 320:230-233. http://dx.doi.org/10.1126/science.1153201.
25. 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. 2013. APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 494:366-370. http://dx.doi.org/10.1038/nature11881.
26. Burns MB, Temiz NA, Harris RS. 2013. Evidence for APOBEC3B mutagenesis in multiple human cancers. Nat Genet 45:977-983. http://dx.doi.org/10.1038/ng.2701.
27. 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, Stephens PJ, McLaren S, Butler AP, Teague JW, Jönsson G, Garber JE, Silver D, Miron P, Fatima A, Boyault S, Langerød A, Tutt A, Martens JWM, Aparicio SAJR, Borg Å, Salomon AV, Thomas G, Børresen-Dale A-L, Richardson AL, Neuberger MS, Futreal PA, Campbell PJ, Stratton MR, Breast Cancer Working Group of the International Cancer Genome Consortium. 2012. Mutational processes molding the genomes of 21 breast cancers. Cell 149:979-993. http://dx.doi.org/10.1016/j.cell.2012.04.024.
28. Kuong KJ, Loeb LA. 2013. APOBEC3B mutagenesis in cancer. Nat Genet 45:964-965. http://dx.doi.org/10.1038/ng.2736.
29. Taylor B, Nik-Zainal S, Wu YL, Stebbings LA. 2013. DNA deaminases induce break-associated mutation showers with implication of APOBEC3B and 3A in breast cancer kataegis. eLife 2:e00534. http://dx.doi.org/10.7554/eLife.00534.
30. Nowarski R, Kotler M. 2013. APOBEC3 cytidine deaminases in doublestrand DNA break repair and cancer promotion. Cancer Res 73:3494-3498. http://dx.doi.org/10.1158/0008-5472.CAN-13-0728.
31. 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, Lin P, Lichtenstein L, Heiman DI, Fennell T, Imielinski M, Hernandez B, Hodis E, Baca S, Dulak AM, Lohr J, Landau D-A, Wu CJ, Melendez-Zajgla J, Hidalgo-Miranda A, Koren A, McCarroll SA, Mora J, Lee RS, Crompton B, Onofrio R, et al. 2013. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 499: 214-218. http://dx.doi.org/10.1038/nature12213.
32. 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. 2013. An APOBEC cytidine deaminase mutagenesis pattern is widespread in human cancers. Nat Genet 45: 970-976. http://dx.doi.org/10.1038/ng.2702.
33. Pyeon D, Lambert PF, Ahlquist P. 2005. Production of infectious human papillomavirus independently of viral replication and epithelial cell differentiation. Proc Natl Acad Sci USA 102:9311-9316. http://dx.doi.org/10.1073/pnas.0504020102.
34. Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, Fusenig NE. 1988. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106:761-771. http://dx.doi.org/10.1083/jcb.106.3.761.
35. Allen-Hoffmann BL, Schlosser SJ, Ivarie CA, Sattler CA, Meisner LF, O'Connor SL. 2000. Normal growth and differentiation in a spontaneously immortalized near-diploid human keratinocyte cell line, NIKS. J Investig Dermatol 114:444-455. http://dx.doi.org/10.1046/j.1523-1747.2000.00869.x.
36. Flores ER, Allen-Hoffmann BL, Lee D, Lambert PF. 2000. The human papillomavirus type 16 E7 oncogene is required for the productive stage of the viral life cycle. J Virol 74:6622-6631. http://dx.doi.org/10.1128/JVI.74.14.6622-6631.2000.
37. Stanley MA, Browne HM, Appleby M, Minson AC. 1989. Properties of a non-tumorigenic human cervical keratinocyte cell line. Int J Cancer 43:672-676. http://dx.doi.org/10.1002/ijc.2910430422.
38. Jeon S, Allen-Hoffmann BL, Lambert PF. 1995. Integration of human papillomavirus type 16 into the human genome correlates with a selective growth advantage of cells. J Virol 69:2989-2997.
39. Kimple RJ, Smith MA, Blitzer GC, Torres AD, Martin JA, Yang RZ, Peet CR, Lorenz LD, Nickel KP, Klingelhutz AJ, Lambert PF, Harari PM. 2013. Enhanced radiation sensitivity in HPV-positive head and neck cancer. Cancer Res 73:4791-4800. http://dx.doi.org/10.1158/0008-5472.CAN-13-0587.
40. Buck CB, Day PM, Thompson CD, Lubkowski J, Lu W, Lowy DR, Schiller JT. 2006. Human alpha-defensins block papillomavirus infection. Proc Natl Acad Sci USA 103:1516-1521. http://dx.doi.org/10.1073/pnas.0508033103.
41. Genther SM, Sterling S, Duensing S, Münger K, Sattler C, Lambert PF. 2003. Quantitative role of the human papillomavirus type 16 E5 gene during the productive stage of the viral life cycle. J Virol 77:2832-2842. http://dx.doi.org/10.1128/JVI.77.5.2832-2842.2003.
42. Buck CB, Pastrana DV, Lowy DR, Schiller JT. 2004. Efficient intracellular assembly of papillomaviral vectors. J Virol 78:751-757. http://dx.doi.org/10.1128/JVI.78.2.751-757.2004.
43. Griffin LM, Cicchini L, Pyeon D. 2013. Human papillomavirus infection is inhibited by host autophagy in primary human keratinocytes. Virology 437:12-19. http://dx.doi.org/10.1016/j.virol.2012.12.004.
44. Chen C, Okayama H. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7:2745-2752.
45. Pyeon D, Pearce SM, Lank SM, Ahlquist P, Lambert PF. 2009. Establishment ofhumanpapillomavirus infection requires cell cycle progression. PLoS Pathog 5:e1000318. http://dx.doi.org/10.1371/journal.ppat.1000318.
46. Stopak K, de Noronha C, Yonemoto W, Greene WC. 2003. HIV-1 Vif blocks the antiviral activity of APOBEC3G by impairing both its translation and intracellular stability. Mol Cell 12:591-601. http://dx.doi.org/10.1016/S1097-2765(03)00353-8.
47. Halemano K, Guo K, Heilman KJ, Barrett BS, Smith DS, Hasenkrug KJ, Santiago ML. 2014. Immunoglobulin somatic hypermutation by APOBEC3/Rfv3 during retroviral infection. Proc Natl Acad Sci USA 111: 7759-7764. http://dx.doi.org/10.1073/pnas.1403361111.
48. Masella AP, Bartram AK, Truszkowski JM, Brown DG, Neufeld JD. 2012. PANDAseq: paired-end assembler for Illumina sequences. BMC Bioinformatics 13:31. http://dx.doi.org/10.1186/1471-2105-13-31.
49. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461. http://dx.doi.org/10.1093/bioinformatics/btq461.
50. Santiago ML, Smith DS, Barrett BS, Montano M, Benitez RL, Pelanda R, Hasenkrug KJ, Greene WC. 2011. Persistent Friend virus replication and disease in Apobec3-deficient mice expressing functional B-cellactivating factor receptor. J Virol 85:189-199. http://dx.doi.org/10.1128/JVI.01838-10.
51. Schiffman M, Castle PE. 2005. The promise of global cervical-cancer prevention. N Engl J Med 353:2101-2104. http://dx.doi.org/10.1056/NEJMp058171.
52. Wang SS, Zuna RE, Wentzensen N, Dunn ST, Sherman ME, Gold MA, Schiffman M, Wacholder S, Allen RA, Block I, Downing K, Jeronimo J, Carreon JD, Safaeian M, Brown D, Walker JL. 2009. Human papillomavirus cofactors by disease progression and human papillomavirus types in the study to understand cervical cancer early endpoints and determinants. Cancer Epidemiol Biomarkers Prev 18:113-120. http://dx.doi.org/10.1158/1055-9965.EPI-08-0591.
53. Warren CJ, Griffin LM, Little AS, Huang IC, Farzan M. 2014. The antiviral restriction factors IFITM1, 2 and 3 do not inhibit infection of human papillomavirus, cytomegalovirus and adenovirus. PLoS One 9:e96579. http://dx.doi.org/10.1371/journal.pone.0096579.
54. Wang Z, Wakae K, Kitamura K, Aoyama S, Liu G, Koura M, Monjurul AM, Kukimoto I, Muramatsu M. 2014. APOBEC3 deaminases induce hypermutation in human papillomavirus 16 DNA upon beta interferon stimulation. J Virol 88:1308-1317. http://dx.doi.org/10.1128/JVI.03091-13.
55. Stenglein MD, Burns MB, Li M, Lengyel J, Harris RS. 2010. APOBEC3 proteins mediate the clearance of foreign DNA from human cells. Nat Struct Mol Biol 17:222-229. http://dx.doi.org/10.1038/nsmb.1744.
56. Simonson SJS, Difilippantonio MJ, Lambert PF. 2005. Two distinct activities contribute to human papillomavirus 16 E6's oncogenic potential. Cancer Res 65:8266-8273. http://dx.doi.org/10.1158/0008-5472.CAN-05-1651.
57. Ingle A, Ghim S, Joh J, Chepkoech I, Jenson AB, Sundberg JP. 2011. Novel laboratory mouse papillomavirus (MusPV) infection. Vet Pathol 48:500-505. http://dx.doi.org/10.1177/0300985810377186.
58. Joh J, Jenson AB, King W, Proctor M, Ingle A, Sundberg JP, Ghim S-J. 2011. Genomic analysis of the first laboratory-mouse papillomavirus. J Gen Virol 92:692-698. http://dx.doi.org/10.1099/vir.0.026138-0.
59. Cladel NM, Budgeon LR, Cooper TK, Balogh KK, Hu J, Christensen ND. 2013. Secondary infections, expanded tissue tropism, and evidence for malignant potential in immunocompromised mice infected with Mus musculus papillomavirus 1 DNA and virus. J Virol 87:9391-9395. http://dx.doi.org/10.1128/JVI.00777-13.
60. Williams R, Lee DW, Elzey BD, Anderson ME, Hostager BS, Lee JH. 2009. Preclinical models of HPV+ and HPV-HNSCC in mice: an immune clearance of HPV+ HNSCC. Head Neck 31:911-918. http://dx.doi.org/10.1002/hed.21040.
61. Nyitray AG, Menezes L, Lu B, Lin H-Y, Smith D, Abrahamsen M, Papenfuss M, Gage C, Giuliano AR. 2012. Genital human papillomavirus (HPV) concordance in heterosexual couples. J Infect Dis 206:202-211. http://dx.doi.org/10.1093/infdis/jis327.
62. Repp KK, Nielson CM, Fu R, Schafer S, Lazcano-Ponce E, Salmerón J, Quiterio M, Villa LL, Giuliano AR, HIM Study. 2012. Male human papillomavirus prevalence and association with condom use in Brazil, Mexico, and the United States. J Infect Dis 205:1287-1293. http://dx.doi.org/10.1093/infdis/jis181.
63. Suspène R, Guétard D, Henry M, Sommer P, Wain-Hobson S, Vartanian J-P. 2005. Extensive editing of both hepatitis B virus DNA strands by APOBEC3 cytidine deaminases in vitro and in vivo. Proc Natl Acad Sci U S A 102:8321-8326. http://dx.doi.org/10.1073/pnas.0408223102.
64. Bogerd HP, Wiegand HL, Doehle BP, Lueders KK, Cullen BR. 2006. APOBEC3A and APOBEC3B are potent inhibitors of LTRretrotransposon function in human cells. Nucleic Acids Res 34:89-95. http://dx.doi.org/10.1093/nar/gkj416.
65. Bulliard Y, Narvaiza I, Bertero A, Peddi S, Röhrig UF, Ortiz M, Zoete V, Castro-Díaz N, Turelli P, Telenti A, Michielin O, Weitzman MD, Trono D. 2011. Structure-function analyses point to a polynucleotideaccommodating groove essential for APOBEC3A restriction activities. J Virol 85:1765-1776. http://dx.doi.org/10.1128/JVI.01651-10.
66. Minkah N, Chavez K, Shah P, MacCarthy T, Chen H, Landau N, Krug LT. 2014. Host restriction of murine gammaherpesvirus 68 replication by human APOBEC3 cytidine deaminases but not murine APOBEC3. Virology 454-455:215-226. http://dx.doi.org/10.1016/j.virol.2014.02.022.
67. Peng G, Greenwell-Wild T, Nares S, Jin W, Lei KJ, Rangel ZG, Munson PJ, Wahl SM. 2007. Myeloid differentiation and susceptibility to HIV-1 are linked to APOBEC3 expression. Blood 110:393-400. http://dx.doi.org/10.1182/blood-2006-10-051763.
68. Refsland EW, Stenglein MD, Shindo K, Albin JS, Brown WL, Harris RS. 2010. Quantitative profiling of the full APOBEC3 mRNA repertoire in lymphocytes and tissues: implications for HIV-1 restriction. Nucleic Acids Res 38:4274-4284. http://dx.doi.org/10.1093/nar/gkq174.
69. Beale RCL, Petersen-Mahrt SK, Watt IN, Harris RS, Rada C, Neuberger MS. 2004. Comparison of the differential context-dependence of DNA deamination byAPOBECenzymes: correlation with mutation spectra in vivo. J Mol Biol 337:585-596. http://dx.doi.org/10.1016/j.jmb.2004.01.046.
70. Love RP, Xu H, Chelico L. 2012. Biochemical analysis of hypermutation by the deoxycytidine deaminase APOBEC3A. J Biol Chem 287:30812-30822. http://dx.doi.org/10.1074/jbc.M112.393181.
71. Land AM, Law EK, Carpenter MA, Lackey L, Brown WL, Harris RS. 2013. Endogenous APOBEC3A DNA cytosine deaminase is cytoplasmic and nongenotoxic. J Biol Chem 288:17253-17260. http://dx.doi.org/10.1074/jbc.M113.458661.
72. Lackey L, Law EK, Brown WL, Harris RS. 2013. Subcellular localization of the APOBEC3proteins during mitosisandimplications for genomicDNAdeamination. Cell Cycle 12:762-772. http://dx.doi.org/10.4161/cc.23713.
73. Schmitt K, Guo K, Katuwal M, Wilson D, Prochnow C, Bransteitter R, Chen XS, Santiago ML, Stephens EB. 2013. Lentivirus restriction by diverse primate APOBEC3A proteins. Virology 442:82-96. http://dx.doi.org/10.1016/j.virol.2013.04.002.
74. Landry S, Narvaiza I, Linfesty DC, Weitzman MD. 2011. APOBEC3A can activate the DNA damage response and cause cell-cycle arrest. EMBO Rep 12:444-450. http://dx.doi.org/10.1038/embor.2011.46.
75. Roberts SA, Sterling J, Thompson C, Harris S, Mav D, Shah R, Klimczak LJ, Kryukov GV, Malc E, Mieczkowski PA, Resnick MA, Gordenin DA. 2012. Clustered mutations in yeast and in human cancers can arise from damaged long single-strand DNA regions. Mol Cell 46:424-435. http://dx.doi.org/10.1016/j.molcel.2012.03.030.
76. Xuan D, Li G, Cai Q, Deming-Halverson S, Shrubsole MJ, Shu X-O, Kelley MC, Zheng W, Long J. 2013. APOBEC3 deletion polymorphism is associated with breast cancer risk among women of European ancestry. Carcinogenesis 34:2240-2243. http://dx.doi.org/10.1093/carcin/bgt185.
77. Long J, Delahanty RJ, Li G, Gao Y-T, Lu W, Cai Q, Xiang Y-B, Li C, Ji B-T, Zheng Y, Ali S, Shu X-O, Zheng W. 2013. A common deletion in the APOBEC3 genes and breast cancer risk. J Natl Cancer Inst 105:573-579. http://dx.doi.org/10.1093/jnci/djt018.
78. 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. 2014. Association of a germline copy number polymorphism of APOBEC3A and APOBEC3B with burden of putative APOBECdependent mutations in breast cancer. Nat Genet 46:487-491. http://dx.doi.org/10.1038/ng.2955.
79. Pyeon D, Newton MA, Lambert PF, den Boon JA, Sengupta S, Marsit CJ, Woodworth CD, Connor JP, Haugen TH, Smith EM, Kelsey KT, Turek LP, Ahlquist P. 2007. Fundamental differences in cell cycle deregulation in human papillomavirus-positive and human papillomavirusnegative head/neck and cervical cancers. Cancer Res 67:4605-4619. http://dx.doi.org/10.1158/0008-5472.CAN-06-3619.