1887

Abstract

The apolipoprotein mRNA editing enzyme catalytic polypeptide-like 3 (APOBEC3; A3) proteins are a family of seven cytidine deaminases (A3A, A3B, A3C, A3D, A3F, A3G and A3H) that restrict certain viral infections. These innate defence factors are best known for their ability to restrict the replication of human immunodeficiency virus type 1 (HIV-1) lacking a functional Vif protein (HIV-1Δ) through the deamination of cytidine residues to uridines during reverse transcription, ultimately leading to lethal G → A changes in the viral genome. The best studied of the A3 proteins has been APOBEC3G because of its potent activity against HIV-1Δ. However, one member of this family, A3A, has biological properties that make it unique among the A3 proteins. In this review, we will focus on the structural and phylogenetic features of the human and non-human primate A3A proteins, their role in the restriction of retroviruses and other viruses, and current findings on other biological properties affected by this protein.

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2016-01-01
2019-10-17
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References

  1. Abe H. , Ochi H. , Maekawa T. , Hatakeyama T. , Tsuge M. , Kitamura S. , Kimura T. , Miki D. , Mitsui F. , other authors . ( 2009;). Effects of structural variations of APOBEC3A and APOBEC3B genes in chronic hepatitis B virus infection. Hepatol Res 39: 1159–1168 [CrossRef] [PubMed].
    [Google Scholar]
  2. Adolph M. B. , Webb J. , Chelico L. . ( 2013;). Retroviral restriction factor APOBEC3G delays the initiation of DNA synthesis by HIV-1 reverse transcriptase. PLoS One 8: e64196 [CrossRef] [PubMed].
    [Google Scholar]
  3. Aguiar R. S. , Lovsin N. , Tanuri A. , Peterlin B. M. . ( 2008;). Vpr.A3A chimera inhibits HIV replication. J Biol Chem 283: 2518–2525 [CrossRef] [PubMed].
    [Google Scholar]
  4. Ahasan M. M. , Wakae K. , Wang Z. , Kitamura K. , Liu G. , Koura M. , Imayasu M. , Sakamoto N. , Hanaoka K. , other authors . ( 2015;). APOBEC3A and 3C decrease human papillomavirus 16 pseudovirion infectivity. Biochem Biophys Res Commun 457: 295–299 [CrossRef] [PubMed].
    [Google Scholar]
  5. Alke A. , Schwantes A. , Kido K. , Flötenmeyer M. , Flügel R. M. , Löchelt M. . ( 2001;). The bet gene of feline foamy virus is required for virus replication. Virology 287: 310–320 [CrossRef] [PubMed].
    [Google Scholar]
  6. Aynaud M. M. , Suspène R. , Vidalain P. O. , Mussil B. , Guétard D. , Tangy F. , Wain-Hobson S. , Vartanian J. P. . ( 2012;). Human Tribbles 3 protects nuclear DNA from cytidine deamination by APOBEC3A. J Biol Chem 287: 39182–39192 [CrossRef] [PubMed].
    [Google Scholar]
  7. Bannert N. , Kurth R. . ( 2006;). The evolutionary dynamics of human endogenous retroviral families. Annu Rev Genomics Hum Genet 7: 149–173 [CrossRef] [PubMed].
    [Google Scholar]
  8. Barbulescu M. , Turner G. , Seaman M. I. , Deinard A. S. , Kidd K. K. , Lenz J. . ( 1999;). Many human endogenous retrovirus K (HERV-K) proviruses are unique to humans. Curr Biol 9: 861–868 [CrossRef] [PubMed].
    [Google Scholar]
  9. Bélanger K. , Savoie M. , Rosales Gerpe M. C. , Couture J. F. , Langlois M. A. . ( 2013;). Binding of RNA by APOBEC3G controls deamination-independent restriction of retroviruses. Nucleic Acids Res 41: 7438–7452 [CrossRef] [PubMed].
    [Google Scholar]
  10. Bennett R. P. , Presnyak V. , Wedekind J. E. , Smith H. C. . ( 2008;). Nuclear exclusion of the HIV-1 host defense factor APOBEC3G requires a novel cytoplasmic retention signal and is not dependent on RNA binding. J Biol Chem 283: 7320–7327 [CrossRef] [PubMed].
    [Google Scholar]
  11. Berger G. , Durand S. , Fargier G. , Nguyen X. N. , Cordeil S. , Bouaziz S. , Muriaux D. , Darlix J. L. , Cimarelli A. . ( 2011;). APOBEC3A is a specific inhibitor of the early phases of HIV-1 infection in myeloid cells. PLoS Pathog 7: e1002221 [CrossRef] [PubMed].
    [Google Scholar]
  12. Bininda-Emonds O. R. , Cardillo M. , Jones K. E. , MacPhee R. D. , Beck R. M. , Grenyer R. , Price S. A. , Vos R. A. , Gittleman J. L. , Purvis A. . ( 2007;). The delayed rise of present-day mammals. Nature 446: 507–512 [CrossRef] [PubMed].
    [Google Scholar]
  13. Bishop K. N. , Holmes R. K. , Sheehy A. M. , Davidson N. O. , Cho S. J. , Malim M. H. . ( 2004;). Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr Biol 14: 1392–1396 [CrossRef] [PubMed].
    [Google Scholar]
  14. Bishop K. N. , Holmes R. K. , Malim M. H. . ( 2006;). Antiviral potency of APOBEC proteins does not correlate with cytidine deamination. J Virol 80: 8450–8458 [CrossRef] [PubMed].
    [Google Scholar]
  15. Bock M. , Stoye J. P. . ( 2000;). Endogenous retroviruses and the human germline. Curr Opin Genet Dev 10: 651–655 [CrossRef] [PubMed].
    [Google Scholar]
  16. Bogerd H. P. , Doehle B. P. , Wiegand H. L. , Cullen B. R. . ( 2004;). A single amino acid difference in the host APOBEC3G protein controls the primate species specificity of HIV type 1 virion infectivity factor. Proc Natl Acad Sci U S A 101: 3770–3774 [CrossRef] [PubMed].
    [Google Scholar]
  17. Bogerd H. P. , Wiegand H. L. , Doehle B. P. , Lueders K. K. , Cullen B. R. . ( 2006a;). APOBEC3A and APOBEC3B are potent inhibitors of LTR-retrotransposon function in human cells. Nucleic Acids Res 34: 89–95 [CrossRef] [PubMed].
    [Google Scholar]
  18. Bogerd H. P. , Wiegand H. L. , Hulme A. E. , Garcia-Perez J. L. , O'Shea K. S. , Moran J. V. , Cullen B. R. . ( 2006b;). Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc Natl Acad Sci U S A 103: 8780–8785 [CrossRef] [PubMed].
    [Google Scholar]
  19. Bohn M. F. , Shandilya S. M. , Silvas T. V. , Nalivaika E. A. , Kouno T. , Kelch B. A. , Ryder S. P. , Kurt-Yilmaz N. , Somasundaran M. , Schiffer C. A. . ( 2015;). The ssDNA mutator APOBEC3A is regulated by cooperative dimerization. Structure 23: 903–911 [CrossRef] [PubMed].
    [Google Scholar]
  20. Browne E. P. , Allers C. , Landau N. R. . ( 2009;). Restriction of HIV-1 by APOBEC3G is cytidine deaminase-dependent. Virology 387: 313–321 [CrossRef] [PubMed].
    [Google Scholar]
  21. Bulliard Y. , Narvaiza I. , Bertero A. , Peddi S. , Röhrig U. F. , Ortiz M. , Zoete V. , Castro-Díaz N. , Turelli P. , other authors . ( 2011;). Structure-function analyses point to a polynucleotide-accommodating groove essential for APOBEC3A restriction activities. J Virol 85: 1765–1776 [CrossRef] [PubMed].
    [Google Scholar]
  22. Burma S. , Chen B. P. , Murphy M. , Kurimasa A. , Chen D. J. . ( 2001;). ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem 276: 42462–42467 [CrossRef] [PubMed].
    [Google Scholar]
  23. Burns M. B. , Lackey L. , Carpenter M. A. , Rathore A. , Land A. M. , Leonard B. , Refsland E. W. , Kotandeniya D. , Tretyakova N. , other authors . ( 2013;). APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 494: 366–370 [CrossRef] [PubMed].
    [Google Scholar]
  24. Byeon I. J. , Ahn J. , Mitra M. , Byeon C. H. , Hercík K. , Hritz J. , Charlton L. M. , Levin J. G. , Gronenborn A. M. . ( 2013;). NMR structure of human restriction factor APOBEC3A reveals substrate binding and enzyme specificity. Nat Commun 4: 1890 [CrossRef] [PubMed].
    [Google Scholar]
  25. Cagliani R. , Riva S. , Fumagalli M. , Biasin M. , Caputo S. L. , Mazzotta F. , Piacentini L. , Pozzoli U. , Bresolin N. , other authors . ( 2011;). A positively selected APOBEC3H haplotype is associated with natural resistance to HIV-1 infection. Evolution 65: 3311–3322 [CrossRef] [PubMed].
    [Google Scholar]
  26. Carpenter M. A. , Li M. , Rathore A. , Lackey L. , Law E. K. , Land A. M. , Leonard B. , Shandilya S. M. , Bohn M. F. , other authors . ( 2012;). Methylcytosine and normal cytosine deamination by the foreign DNA restriction enzyme APOBEC3A. J Biol Chem 287: 34801–34808 [CrossRef] [PubMed].
    [Google Scholar]
  27. Caval V. , Suspène R. , Vartanian J.-P. , Wain-Hobson S. . ( 2014a;). Orthologous mammalian APOBEC3A cytidine deaminases hypermutate nuclear DNA. Mol Biol Evol 31: 330–340 [CrossRef] [PubMed].
    [Google Scholar]
  28. Caval V. , Suspène R. , Shapira M. , Vartanian J. P. , Wain-Hobson S. . ( 2014b;). A prevalent cancer susceptibility APOBEC3A hybrid allele bearing APOBEC3B 3′UTR enhances chromosomal DNA damage. Nat Commun 5: 5129 [CrossRef] [PubMed].
    [Google Scholar]
  29. Chareza S. , Slavkovic Lukic D. , Liu Y. , Räthe A. M. , Münk C. , Zabogli E. , Pistello M. , Löchelt M. . ( 2012;). Molecular and functional interactions of cat APOBEC3 and feline foamy and immunodeficiency virus proteins: different ways to counteract host-encoded restriction. Virology 424: 138–146 [CrossRef] [PubMed].
    [Google Scholar]
  30. Chelico L. , Pham P. , Calabrese P. , Goodman M. F. . ( 2006;). APOBEC3G DNA deaminase acts processively 3′ → 5′ on single-stranded DNA. Nat Struct Mol Biol 13: 392–399 [CrossRef] [PubMed].
    [Google Scholar]
  31. Chen H. , Lilley C. E. , Yu Q. , Lee D. V. , Chou J. , Narvaiza I. , Landau N. R. , Weitzman M. D. . ( 2006;). APOBEC3A is a potent inhibitor of adeno-associated virus and retrotransposons. Curr Biol 16: 480–485 [CrossRef] [PubMed].
    [Google Scholar]
  32. Chen G. , He Z. , Wang T. , Xu R. , Yu X. F. . ( 2009;). A patch of positively charged amino acids surrounding the human immunodeficiency virus type 1 Vif SLVx4Yx9Y motif influences its interaction with APOBEC3G. J Virol 83: 8674–8682 [CrossRef] [PubMed].
    [Google Scholar]
  33. Conticello S. G. , Harris R. S. , Neuberger M. S. . ( 2003;). The Vif protein of HIV triggers degradation of the human antiretroviral DNA deaminase APOBEC3G. Curr Biol 13: 2009–2013 [CrossRef] [PubMed].
    [Google Scholar]
  34. Dang Y. , Wang X. , York I. A. , Zheng Y. H. . ( 2010;). Identification of a critical T(Q/D/E)x5ADx2(I/L) motif from primate lentivirus Vif proteins that regulate APOBEC3G and APOBEC3F neutralizing activity. J Virol 84: 8561–8570 [CrossRef] [PubMed].
    [Google Scholar]
  35. Duggal N. K. , Malik H. S. , Emerman M. . ( 2011;). The breadth of antiviral activity of Apobec3DE in chimpanzees has been driven by positive selection. J Virol 85: 11361–11371 [CrossRef] [PubMed].
    [Google Scholar]
  36. Dussart S. , Courcoul M. , Bessou G. , Douaisi M. , Duverger Y. , Vigne R. , Decroly E. . ( 2004;). The Vif protein of human immunodeficiency virus type 1 is posttranslationally modified by ubiquitin. Biochem Biophys Res Commun 315: 66–72 [CrossRef] [PubMed].
    [Google Scholar]
  37. Espert L. , Varbanov M. , Robert-Hebmann V. , Sagnier S. , Robbins I. , Sanchez F. , Lafont V. , Biard-Piechaczyk M. . ( 2009;). Differential role of autophagy in CD4 T cells and macrophages during X4 and R5 HIV-1 infection. PLoS One 4: e5787 [CrossRef] [PubMed].
    [Google Scholar]
  38. Ezzikouri S. , Kitab B. , Rebbani K. , Marchio A. , Wain-Hobson S. , Dejean A. , Vartanian J. P. , Pineau P. , Benjelloun S. . ( 2013;). Polymorphic APOBEC3 modulates chronic hepatitis B in Moroccan population. J Viral Hepat 20: 678–686 [CrossRef] [PubMed].
    [Google Scholar]
  39. Goila-Gaur R. , Khan M. A. , Miyagi E. , Kao S. , Strebel K. . ( 2007;). Targeting APOBEC3A to the viral nucleoprotein complex confers antiviral activity. Retrovirology 4: 61 [CrossRef] [PubMed].
    [Google Scholar]
  40. Golka K. , Selinski S. , Lehmann M. L. , Blaszkewicz M. , Marchan R. , Ickstadt K. , Schwender H. , Bolt H. M. , Hengstler J. G. . ( 2011;). Genetic variants in urinary bladder cancer: collective power of the wimp SNPs. Arch Toxicol 85: 539–554 [CrossRef] [PubMed].
    [Google Scholar]
  41. Guan P. , Howell-Jones R. , Li N. , Bruni L. , de Sanjosé S. , Franceschi S. , Clifford G. M. . ( 2012;). Human papillomavirus types in 115,789 HPV-positive women: a meta-analysis from cervical infection to cancer. Int J Cancer 131: 2349–2359 [CrossRef] [PubMed].
    [Google Scholar]
  42. Hahn B. H. , Shaw G. M. , De Cock K. M. , Sharp P. M. . ( 2000;). AIDS as a zoonosis: scientific and public health implications. Science 287: 607–614 [CrossRef] [PubMed].
    [Google Scholar]
  43. Heneine W. , Schweizer M. , Sandstrom P. , Folks T. . ( 2003;). Human infection with foamy viruses. Curr Top Microbiol Immunol 277: 181–196 [PubMed].
    [Google Scholar]
  44. Henry M. , Guétard D. , Suspène R. , Rusniok C. , Wain-Hobson S. , Vartanian J. P. . ( 2009;). Genetic editing of HBV DNA by monodomain human APOBEC3 cytidine deaminases and the recombinant nature of APOBEC3G. PLoS One 4: e4277 [CrossRef] [PubMed].
    [Google Scholar]
  45. Henry M. , Terzian C. , Peeters M. , Wain-Hobson S. , Vartanian J. P. . ( 2012;). Evolution of the primate APOBEC3A cytidine deaminase gene and identification of related coding regions. PLoS One 7: e30036 [CrossRef] [PubMed].
    [Google Scholar]
  46. Holden L. G. , Prochnow C. , Chang Y. P. , Bransteitter R. , Chelico L. , Sen U. , Stevens R. C. , Goodman M. F. , Chen X. S. . ( 2008;). Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications. Nature 456: 121–124 [CrossRef] [PubMed].
    [Google Scholar]
  47. Hultquist J. F. , Lengyel J. A. , Refsland E. W. , LaRue R. S. , Lackey L. , Brown W. L. , Harris R. S. . ( 2011;). Human and rhesus APOBEC3D, APOBEC3F, APOBEC3G, and APOBEC3H demonstrate a conserved capacity to restrict Vif-deficient HIV-1. J Virol 85: 11220–11234 [CrossRef] [PubMed].
    [Google Scholar]
  48. Hussain A. I. , Shanmugam V. , Bhullar V. B. , Beer B. E. , Vallet D. , Gautier-Hion A. , Wolfe N. D. , Karesh W. B. , Kilbourn A. M. , other authors . ( 2003;). Screening for simian foamy virus infection by using a combined antigen Western blot assay: evidence for a wide distribution among Old World primates and identification of four new divergent viruses. Virology 309: 248–257 [CrossRef] [PubMed].
    [Google Scholar]
  49. Iwatani Y. , Chan D. S. , Wang F. , Maynard K. S. , Sugiura W. , Gronenborn A. M. , Rouzina I. , Williams M. C. , Musier-Forsyth K. , Levin J. G. . ( 2007;). Deaminase-independent inhibition of HIV-1 reverse transcription by APOBEC3G. Nucleic Acids Res 35: 7096–7108 [CrossRef] [PubMed].
    [Google Scholar]
  50. Jäger S. , Kim D. Y. , Hultquist J. F. , Shindo K. , LaRue R. S. , Kwon E. , Li M. , Anderson B. D. , Yen L. , other authors . ( 2012;). Vif hijacks CBF-β to degrade APOBEC3G and promote HIV-1 infection. Nature 481: 371–375 [PubMed].
    [Google Scholar]
  51. 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 [CrossRef] [PubMed].
    [Google Scholar]
  52. Jern P. , Coffin J. M. . ( 2008;). Effects of retroviruses on host genome function. Annu Rev Genet 42: 709–732 [CrossRef] [PubMed].
    [Google Scholar]
  53. Katuwal M. , Wang Y. , Schmitt K. , Guo K. , Halemano K. , Santiago M. L. , Stephens E. B. . ( 2014;). Cellular HIV-1 inhibition by truncated Old World primate APOBEC3A proteins lacking a complete deaminase domain. Virology 468-470: 532–544 [CrossRef] [PubMed].
    [Google Scholar]
  54. Keele B. F. , Van Heuverswyn F. , Li Y. , Bailes E. , Takehisa J. , Santiago M. L. , Bibollet-Ruche F. , Chen Y. , Wain L. V. , other authors . ( 2006;). Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313: 523–526 [CrossRef] [PubMed].
    [Google Scholar]
  55. Khan A. S. . ( 2009;). Simian foamy virus infection in humans: prevalence and management. Expert Rev Anti Infect Ther 7: 569–580 [CrossRef] [PubMed].
    [Google Scholar]
  56. Kidd J. M. , Newman T. L. , Tuzun E. , Kaul R. , Eichler E. E. . ( 2007;). Population stratification of a common APOBEC gene deletion polymorphism. PLoS Genet 3: e63 [CrossRef] [PubMed].
    [Google Scholar]
  57. Kinomoto M. , Kanno T. , Shimura M. , Ishizaka Y. , Kojima A. , Kurata T. , Sata T. , Tokunaga K. . ( 2007;). All APOBEC3 family proteins differentially inhibit LINE-1 retrotransposition. Nucleic Acids Res 35: 2955–2964 [CrossRef] [PubMed].
    [Google Scholar]
  58. Kitamura S. , Ode H. , Nakashima M. , Imahashi M. , Naganawa Y. , Kurosawa T. , Yokomaku Y. , Yamane T. , Watanabe N. , other authors . ( 2012;). The APOBEC3C crystal structure and the interface for HIV-1 Vif binding. Nat Struct Mol Biol 19: 1005–1010 [CrossRef] [PubMed].
    [Google Scholar]
  59. Kobayashi M. , Takaori-Kondo A. , Miyauchi Y. , Iwai K. , Uchiyama T. . ( 2005;). Ubiquitination of APOBEC3G by an HIV-1 Vif-Cullin5-Elongin B-Elongin C complex is essential for Vif function. J Biol Chem 280: 18573–18578 [CrossRef] [PubMed].
    [Google Scholar]
  60. Koito A. , Ikeda T. . ( 2011;). Intrinsic restriction activity by AID/APOBEC family of enzymes against the mobility of retroelements. Mob Genet Elements 1: 197–202 [CrossRef] [PubMed].
    [Google Scholar]
  61. Koning F. A. , Newman E. N. , Kim E. Y. , Kunstman K. J. , Wolinsky S. M. , Malim M. H. . ( 2009;). Defining APOBEC3 expression patterns in human tissues and hematopoietic cell subsets. J Virol 83: 9474–9485 [CrossRef] [PubMed].
    [Google Scholar]
  62. Koning F. A. , Goujon C. , Bauby H. , Malim M. H. . ( 2011;). Target cell-mediated editing of HIV-1 cDNA by APOBEC3 proteins in human macrophages. J Virol 85: 13448–13452 [CrossRef] [PubMed].
    [Google Scholar]
  63. Kyei G. B. , Dinkins C. , Davis A. S. , Roberts E. , Singh S. B. , Dong C. , Wu L. , Kominami E. , Ueno T. , other authors . ( 2009;). Autophagy pathway intersects with HIV-1 biosynthesis and regulates viral yields in macrophages. J Cell Biol 186: 255–268 [CrossRef] [PubMed].
    [Google Scholar]
  64. Lackey L. , Law E. K. , Brown W. L. , Harris R. S. . ( 2013;). Subcellular localization of the APOBEC3 proteins during mitosis and implications for genomic DNA deamination. Cell Cycle 12: 762–772 [CrossRef] [PubMed].
    [Google Scholar]
  65. Land A. M. , Law E. K. , Carpenter M. A. , Lackey L. , Brown W. L. , Harris R. S. . ( 2013;). Endogenous APOBEC3A is cytoplasmic and non-genotoxic. J Biol Chem 288: 17253–17260 [CrossRef] [PubMed].
    [Google Scholar]
  66. Lander E. S. , Linton L. M. , Birren B. , Nusbaum C. , Zody M. C. , Baldwin J. , Devon K. , Dewar K. , Doyle M. , other authors . ( 2001;). Initial sequencing and analysis of the human genome. Nature 409: 860–921 [CrossRef] [PubMed].
    [Google Scholar]
  67. Landry S. , Narvaiza I. , Linfesty D. C. , Weitzman M. D. . ( 2011;). APOBEC3A can activate the DNA damage response and cause cell-cycle arrest. EMBO Rep 12: 444–450 [CrossRef] [PubMed].
    [Google Scholar]
  68. LaRue R. S. , Andrésdóttir V. , Blanchard Y. , Conticello S. G. , Derse D. , Emerman M. , Greene W. C. , Jónsson S. R. , Landau N. R. , other authors . ( 2009;). Guidelines for naming nonprimate APOBEC3 genes and proteins. J Virol 83: 494–497 [CrossRef] [PubMed].
    [Google Scholar]
  69. Lecossier D. , Bouchonnet F. , Clavel F. , Hance A. J. . ( 2003;). Hypermutation of HIV-1 DNA in the absence of the Vif protein. Science 300: 1112 [CrossRef] [PubMed].
    [Google Scholar]
  70. Lee Y. N. , Bieniasz P. D. . ( 2007;). Reconstitution of an infectious human endogenous retrovirus. PLoS Pathog 3: e10 [CrossRef] [PubMed].
    [Google Scholar]
  71. Lee Y. N. , Malim M. H. , Bieniasz P. D. . ( 2008;). Hypermutation of an ancient human retrovirus by APOBEC3G. J Virol 82: 8762–8770 [CrossRef] [PubMed].
    [Google Scholar]
  72. Leendertz F. H. , Zirkel F. , Couacy-Hymann E. , Ellerbrok H. , Morozov V. A. , Pauli G. , Hedemann C. , Formenty P. , Jensen S. A. , other authors . ( 2008;). Interspecies transmission of simian foamy virus in a natural predator-prey system. J Virol 82: 7741–7744 [CrossRef] [PubMed].
    [Google Scholar]
  73. Letvin N. L. , Daniel M. D. , Sehgal P. K. , Desrosiers R. C. , Hunt R. D. , Waldron L. M. , MacKey J. J. , Schmidt D. K. , Chalifoux L. V. , King N. W. . ( 1985;). Induction of AIDS-like disease in macaque monkeys with T-cell tropic retrovirus STLV-III. Science 230: 71–73.[CrossRef]
    [Google Scholar]
  74. Li X. Y. , Guo F. , Zhang L. , Kleiman L. , Cen S. . ( 2007;). APOBEC3G inhibits DNA strand transfer during HIV-1 reverse transcription. J Biol Chem 282: 32065–32074 [CrossRef] [PubMed].
    [Google Scholar]
  75. Li J. , Chen Y. , Li M. , Carpenter M. A. , McDougle R. M. , Luengas E. M. , Macdonald P. J. , Harris R. S. , Mueller J. D. . ( 2014;). APOBEC3 multimerization correlates with HIV-1 packaging and restriction activity in living cells. J Mol Biol 426: 1296–1307 [CrossRef] [PubMed].
    [Google Scholar]
  76. Liang J. W. , Shi Z. Z. , Shen T. Y. , Che X. , Wang Z. , Shi S. S. , Xu X. , Cai Y. , Zhao P. , other authors . ( 2014;). Identification of genomic alterations in pancreatic cancer using array-based comparative genomic hybridization. PLoS One 9: e114616 [CrossRef] [PubMed].
    [Google Scholar]
  77. Liu B. , Yu X. , Luo K. , Yu Y. , Yu X. F. . ( 2004;). Influence of primate lentiviral Vif and proteasome inhibitors on human immunodeficiency virus type 1 virion packaging of APOBEC3G. J Virol 78: 2072–2081 [CrossRef] [PubMed].
    [Google Scholar]
  78. Löchelt M. , Romen F. , Bastone P. , Muckenfuss H. , Kirchner N. , Kim Y. B. , Truyen U. , Rösler U. , Battenberg M. , other authors . ( 2005;). The antiretroviral activity of APOBEC3 is inhibited by the foamy virus accessory Bet protein. Proc Natl Acad Sci U S A 102: 7982–7987 [CrossRef] [PubMed].
    [Google Scholar]
  79. Logue E. C. , Bloch N. , Dhuey E. , Zhang R. , Cao P. , Herate C. , Chauveau L. , Hubbard S. R. , Landau N. R. . ( 2014;). A DNA sequence recognition loop on APOBEC3A controls substrate specificity. PLoS One 9: e97062 [CrossRef] [PubMed].
    [Google Scholar]
  80. Long J. , Delahanty R. J. , Li G. , Gao Y. T. , Lu W. , Cai Q. , Xiang Y. B. , Li C. , Ji B. T. , other authors . ( 2013;). A common deletion in the APOBEC3 genes and breast cancer risk. J Natl Cancer Inst 105: 573–579 [CrossRef] [PubMed].
    [Google Scholar]
  81. Love R. P. , Xu H. , Chelico L. . ( 2012;). Biochemical analysis of hypermutation by the deoxycytidine deaminase APOBEC3A. J Biol Chem 287: 30812–30822 [CrossRef] [PubMed].
    [Google Scholar]
  82. Luo K. , Xiao Z. , Ehrlich E. , Yu Y. , Liu B. , Zheng S. , Yu X. F. . ( 2005;). Primate lentiviral virion infectivity factors are substrate receptors that assemble with cullin 5-E3 ligase through a HCCH motif to suppress APOBEC3G. Proc Natl Acad Sci U S A 102: 11444–11449 [CrossRef] [PubMed].
    [Google Scholar]
  83. Luo K. , Wang T. , Liu B. , Tian C. , Xiao Z. , Kappes J. , Yu X. F. . ( 2007;). Cytidine deaminases APOBEC3G and APOBEC3F interact with human immunodeficiency virus type 1 integrase and inhibit proviral DNA formation. J Virol 81: 7238–7248 [CrossRef] [PubMed].
    [Google Scholar]
  84. Magiorkinis G. , Belshaw R. , Katzourakis A. . ( 2013;). ‘There and back again’: revisiting the pathophysiological roles of human endogenous retroviruses in the post-genomic era. Philos Trans R Soc Lond B Biol Sci 368: 20120504 [CrossRef] [PubMed].
    [Google Scholar]
  85. Mangeat B. , Turelli P. , Caron G. , Friedli M. , Perrin L. , Trono D. . ( 2003;). Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424: 99–103 [CrossRef] [PubMed].
    [Google Scholar]
  86. Marin M. , Rose K. M. , Kozak S. L. , Kabat D. . ( 2003;). HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat Med 9: 1398–1403 [CrossRef] [PubMed].
    [Google Scholar]
  87. Mehle A. , Goncalves J. , Santa-Marta M. , McPike M. , Gabuzda D. . ( 2004a;). Phosphorylation of a novel SOCS-box regulates assembly of the HIV-1 Vif-Cul5 complex that promotes APOBEC3G degradation. Genes Dev 18: 2861–2866 [CrossRef] [PubMed].
    [Google Scholar]
  88. Mehle A. , Strack B. , Ancuta P. , Zhang C. , McPike M. , Gabuzda D. . ( 2004b;). Vif overcomes the innate antiviral activity of APOBEC3G by promoting its degradation in the ubiquitin-proteasome pathway. J Biol Chem 279: 7792–7798 [CrossRef] [PubMed].
    [Google Scholar]
  89. Mehle A. , Thomas E. R. , Rajendran K. S. , Gabuzda D. . ( 2006;). A zinc-binding region in Vif binds Cul5 and determines cullin selection. J Biol Chem 281: 17259–17265 [CrossRef] [PubMed].
    [Google Scholar]
  90. Mehle A. , Wilson H. , Zhang C. , Brazier A. J. , McPike M. , Pery E. , Gabuzda D. . ( 2007;). Identification of an APOBEC3G binding site in human immunodeficiency virus type 1 Vif and inhibitors of Vif-APOBEC3G binding. J Virol 81: 13235–13241 [CrossRef] [PubMed].
    [Google Scholar]
  91. Meiering C. D. , Linial M. L. . ( 2001;). Historical perspective of foamy virus epidemiology and infection. Clin Microbiol Rev 14: 165–176 [CrossRef] [PubMed].
    [Google Scholar]
  92. Miyagi E. , Opi S. , Takeuchi H. , Khan M. , Goila-Gaur R. , Kao S. , Strebel K. . ( 2007;). Enzymatically active APOBEC3G is required for efficient inhibition of human immunodeficiency virus type 1. J Virol 81: 13346–13353 [CrossRef] [PubMed].
    [Google Scholar]
  93. Muckenfuss H. , Hamdorf M. , Held U. , Perkovic M. , Löwer J. , Cichutek K. , Flory E. , Schumann G. G. , Münk C. . ( 2006;). APOBEC3 proteins inhibit human LINE-1 retrotransposition. J Biol Chem 281: 22161–22172 [CrossRef] [PubMed].
    [Google Scholar]
  94. Münk C. , Willemsen A. , Bravo I. G. . ( 2012;). An ancient history of gene duplications, fusions and losses in the evolution of APOBEC3 mutators in mammals. BMC Evol Biol 12: 71 [CrossRef] [PubMed].
    [Google Scholar]
  95. Mussil B. , Suspène R. , Aynaud M. M. , Gauvrit A. , Vartanian J. P. , Wain-Hobson S. . ( 2013;). Human APOBEC3A isoforms translocate to the nucleus and induce DNA double strand breaks leading to cell stress and death. PLoS One 8: e73641 [CrossRef] [PubMed].
    [Google Scholar]
  96. Narvaiza I. , Linfesty D. C. , Greener B. N. , Hakata Y. , Pintel D. J. , Logue E. , Landau N. R. , Weitzman M. D. . ( 2009;). Deaminase-independent inhibition of parvoviruses by the APOBEC3A cytidine deaminase. PLoS Pathog 5: e1000439 [CrossRef] [PubMed].
    [Google Scholar]
  97. Navarro F. , Bollman B. , Chen H. , König R. , Yu Q. , Chiles K. , Landau N. R. . ( 2005;). Complementary function of the two catalytic domains of APOBEC3G. Virology 333: 374–386 [CrossRef] [PubMed].
    [Google Scholar]
  98. Neil S. J. , Zang T. , Bieniasz P. D. . ( 2008;). Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451: 425–430 [CrossRef] [PubMed].
    [Google Scholar]
  99. Newman E. N. , Holmes R. K. , Craig H. M. , Klein K. C. , Lingappa J. R. , Malim M. H. , Sheehy A. M. . ( 2005;). Antiviral function of APOBEC3G can be dissociated from cytidine deaminase activity. Curr Biol 15: 166–170 [CrossRef] [PubMed].
    [Google Scholar]
  100. Niavarani A. , Currie E. , Reyal Y. , Anjos-Afonso F. , Horswell S. , Griessinger E. , Luis Sardina J. , Bonnet D. . ( 2015;). APOBEC3A is implicated in a novel class of G-to-A mRNA editing in WT1 transcripts. PLoS One 10: e0120089 [CrossRef] [PubMed].
    [Google Scholar]
  101. Niewiadomska A. M. , Tian C. , Tan L. , Wang T. , Sarkis P. T. , Yu X. F. . ( 2007;). Differential inhibition of long interspersed element 1 by APOBEC3 does not correlate with high-molecular-mass-complex formation or P-body association. J Virol 81: 9577–9583 [CrossRef] [PubMed].
    [Google Scholar]
  102. Nik-Zainal S. , Wedge D. C. , Alexandrov L. B. , Petljak M. , Butler A. P. , Bolli N. , Davies H. R. , Knappskog S. , Martin S. , other authors . ( 2014;). Association of a germline copy number polymorphism of APOBEC3A and APOBEC3B with burden of putative APOBEC-dependent mutations in breast cancer. Nat Genet 46: 487–491 [CrossRef] [PubMed].
    [Google Scholar]
  103. OhAinle M. , Kerns J. A. , Malik H. S. , Emerman M. . ( 2006;). Adaptive evolution and antiviral activity of the conserved mammalian cytidine deaminase APOBEC3H. J Virol 80: 3853–3862 [CrossRef] [PubMed].
    [Google Scholar]
  104. Ooms M. , Krikoni A. , Kress A. K. , Simon V. , Münk C. . ( 2012;). APOBEC3A, APOBEC3B, and APOBEC3H haplotype 2 restrict human T-lymphotropic virus type 1. J Virol 86: 6097–6108 [CrossRef] [PubMed].
    [Google Scholar]
  105. Ortiz M. , Guex N. , Patin E. , Martin O. , Xenarios I. , Ciuffi A. , Quintana-Murci L. , Telenti A. . ( 2009;). Evolutionary trajectories of primate genes involved in HIV pathogenesis. Mol Biol Evol 26: 2865–2875 [CrossRef] [PubMed].
    [Google Scholar]
  106. Peng G. , Greenwell-Wild T. , Nares S. , Jin W. , Lei K. J. , Rangel Z. G. , Munson P. J. , Wahl S. M. . ( 2007;). Myeloid differentiation and susceptibility to HIV-1 are linked to APOBEC3 expression. Blood 110: 393–400 [CrossRef] [PubMed].
    [Google Scholar]
  107. Pery E. , Rajendran K. S. , Brazier A. J. , Gabuzda D. . ( 2009;). Regulation of APOBEC3 proteins by a novel YXXL motif in human immunodeficiency virus type 1 Vif and simian immunodeficiency virus SIVagm Vif. J Virol 83: 2374–2381 [CrossRef] [PubMed].
    [Google Scholar]
  108. Pham P. , Landolph A. , Mendez C. , Li N. , Goodman M. F. . ( 2013;). A biochemical analysis linking APOBEC3A to disparate HIV-1 restriction and skin cancer. J Biol Chem 288: 29294–29304 [CrossRef] [PubMed].
    [Google Scholar]
  109. Refsland E. W. , Stenglein M. D. , Shindo K. , Albin J. S. , Brown W. L. , Harris R. S. . ( 2010;). Quantitative profiling of the full APOBEC3 mRNA repertoire in lymphocytes and tissues: implications for HIV-1 restriction. Nucleic Acids Res 38: 4274–4284 [CrossRef] [PubMed].
    [Google Scholar]
  110. Rethwilm A. . ( 2010;). Molecular biology of foamy viruses. Med Microbiol Immunol (Berl) 199: 197–207 [CrossRef] [PubMed].
    [Google Scholar]
  111. Rogakou E. P. , Pilch D. R. , Orr A. H. , Ivanova V. S. , Bonner W. M. . ( 1998;). DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858–5868 [CrossRef] [PubMed].
    [Google Scholar]
  112. Rogakou E. P. , Boon C. , Redon C. , Bonner W. M. . ( 1999;). Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146: 905–916 [CrossRef] [PubMed].
    [Google Scholar]
  113. Rogozin I. B. , Basu M. K. , Jordan I. K. , Pavlov Y. I. , Koonin E. V. . ( 2005;). APOBEC4, a new member of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases predicted by computational analysis. Cell Cycle 4: 1281–1285 [CrossRef] [PubMed].
    [Google Scholar]
  114. Rothman N. , Garcia-Closas M. , Chatterjee N. , Malats N. , Wu X. , Figueroa J. D. , Real F. X. , Van Den Berg D. , Matullo G. , other authors . ( 2010;). A multi-stage genome-wide association study of bladder cancer identifies multiple susceptibility loci. Nat Genet 42: 978–984 [CrossRef] [PubMed].
    [Google Scholar]
  115. Russell R. A. , Pathak V. K. . ( 2007;). Identification of two distinct human immunodeficiency virus type 1 Vif determinants critical for interactions with human APOBEC3G and APOBEC3F. J Virol 81: 8201–8210 [CrossRef] [PubMed].
    [Google Scholar]
  116. Russell R. A. , Wiegand H. L. , Moore M. D. , Schäfer A. , McClure M. O. , Cullen B. R. . ( 2005;). Foamy virus Bet proteins function as novel inhibitors of the APOBEC3 family of innate antiretroviral defense factors. J Virol 79: 8724–8731 [CrossRef] [PubMed].
    [Google Scholar]
  117. Saïb A. , Koken M. H. , van der Spek P. , Périès J. , de Thé H. . ( 1995;). Involvement of a spliced and defective human foamy virus in the establishment of chronic infection. J Virol 69: 5261–5268 [PubMed].
    [Google Scholar]
  118. Santiago M. L. , Range F. , Keele B. F. , Li Y. , Bailes E. , Bibollet-Ruche F. , Fruteau C. , Noë R. , Peeters M. , other authors . ( 2005;). Simian immunodeficiency virus infection in free-ranging sooty mangabeys (Cercocebus atys atys) from the Taï Forest, Côte d'Ivoire: implications for the origin of epidemic human immunodeficiency virus type 2. J Virol 79: 12515–12527 [CrossRef] [PubMed].
    [Google Scholar]
  119. Sawyer S. L. , Emerman M. , Malik H. S. . ( 2004;). Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2: e275 [CrossRef] [PubMed].
    [Google Scholar]
  120. Schmitt K. , Guo K. , Algaier M. , Ruiz A. , Cheng F. , Qiu J. , Wissing S. , Santiago M. L. , Stephens E. B. . ( 2011;). Differential virus restriction patterns of rhesus macaque and human APOBEC3A: implications for lentivirus evolution. Virology 419: 24–42 [CrossRef] [PubMed].
    [Google Scholar]
  121. Schmitt K. , Guo K. , Katuwal M. , Wilson D. , Prochnow C. , Bransteitter R. , Chen X. S. , Santiago M. L. , Stephens E. B. . ( 2013;). Lentivirus restriction by diverse primate APOBEC3A proteins. Virology 442: 82–96 [CrossRef] [PubMed].
    [Google Scholar]
  122. Schrago C. G. . ( 2007;). On the time scale of New World primate diversification. Am J Phys Anthropol 132: 344–354 [CrossRef] [PubMed].
    [Google Scholar]
  123. Schrago C. G. , Russo C. A. . ( 2003;). Timing the origin of New World monkeys. Mol Biol Evol 20: 1620–1625 [CrossRef] [PubMed].
    [Google Scholar]
  124. Schröfelbauer B. , Chen D. , Landau N. R. . ( 2004;). A single amino acid of APOBEC3G controls its species-specific interaction with virion infectivity factor (Vif). Proc Natl Acad Sci U S A 101: 3927–3932 [CrossRef] [PubMed].
    [Google Scholar]
  125. Schumacher A. J. , Haché G. , Macduff D. A. , Brown W. L. , Harris R. S. . ( 2008;). The DNA deaminase activity of human APOBEC3G is required for Ty1, MusD, and human immunodeficiency virus type 1 restriction. J Virol 82: 2652–2660 [CrossRef] [PubMed].
    [Google Scholar]
  126. Schwantes A. , Truyen U. , Weikel J. , Weiss C. , Löchelt M. . ( 2003;). Application of chimeric feline foamy virus-based retroviral vectors for the induction of antiviral immunity in cats. J Virol 77: 7830–7842 [CrossRef] [PubMed].
    [Google Scholar]
  127. Sharma S. , Patnaik S. K. , Taggart R. T. , Kannisto E. D. , Enriquez S. M. , Gollnick P. , Baysal B. E. . ( 2015;). APOBEC3A cytidine deaminase induces RNA editing in monocytes and macrophages. Nat Commun 6: 6881 [CrossRef] [PubMed].
    [Google Scholar]
  128. Sheehy A. M. , Gaddis N. C. , Choi J. D. , Malim M. H. . ( 2002;). Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418: 646–650 [CrossRef] [PubMed].
    [Google Scholar]
  129. Sheehy A. M. , Gaddis N. C. , Malim M. H. . ( 2003;). The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat Med 9: 1404–1407 [CrossRef] [PubMed].
    [Google Scholar]
  130. Stavrou S. , Crawford D. , Blouch K. , Browne E. P. , Kohli R. M. , Ross S. R. . ( 2014;). Different modes of retrovirus restriction by human APOBEC3A and APOBEC3G in vivo. PLoS Pathog 10: e1004145 [CrossRef] [PubMed].
    [Google Scholar]
  131. Stenglein M. D. , Matsuo H. , Harris R. S. . ( 2008;). Two regions within the amino-terminal half of APOBEC3G cooperate to determine cytoplasmic localization. J Virol 82: 9591–9599 [CrossRef] [PubMed].
    [Google Scholar]
  132. Stenglein M. D. , Burns M. B. , Li M. , Lengyel J. , Harris R. S. . ( 2010;). APOBEC3 proteins mediate the clearance of foreign DNA from human cells. Nat Struct Mol Biol 17: 222–229 [CrossRef] [PubMed].
    [Google Scholar]
  133. Stopak K. , de Noronha C. , Yonemoto W. , Greene W. C. . ( 2003;). HIV-1 Vif blocks the antiviral activity of APOBEC3G by impairing both its translation and intracellular stability. Mol Cell 12: 591–601 [CrossRef] [PubMed].
    [Google Scholar]
  134. Stremlau M. , Owens C. M. , Perron M. J. , Kiessling M. , Autissier P. , Sodroski J. . ( 2004;). The cytoplasmic body component TRIM5α restricts HIV-1 infection in Old World monkeys. Nature 427: 848–853 [CrossRef] [PubMed].
    [Google Scholar]
  135. Suspène R. , Aynaud M. M. , Guétard D. , Henry M. , Eckhoff G. , Marchio A. , Pineau P. , Dejean A. , Vartanian J. P. , Wain-Hobson S. . ( 2011a;). Somatic hypermutation of human mitochondrial and nuclear DNA by APOBEC3 cytidine deaminases, a pathway for DNA catabolism. Proc Natl Acad Sci U S A 108: 4858–4863 [CrossRef] [PubMed].
    [Google Scholar]
  136. Suspène R. , Aynaud M. M. , Koch S. , Pasdeloup D. , Labetoulle M. , Gaertner B. , Vartanian J. P. , Meyerhans A. , Wain-Hobson S. . ( 2011b;). 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 [CrossRef] [PubMed].
    [Google Scholar]
  137. Switzer W. M. , Salemi M. , Shanmugam V. , Gao F. , Cong M. E. , Kuiken C. , Bhullar V. , Beer B. E. , Vallet D. , other authors . ( 2005;). Ancient co-speciation of simian foamy viruses and primates. Nature 434: 376–380 [CrossRef] [PubMed].
    [Google Scholar]
  138. Trobridge G. D. . ( 2009;). Foamy virus vectors for gene transfer. Expert Opin Biol Ther 9: 1427–1436 [CrossRef] [PubMed].
    [Google Scholar]
  139. Van Damme N. , Goff D. , Katsura C. , Jorgenson R. L. , Mitchell R. , Johnson M. C. , Stephens E. B. , Guatelli J. . ( 2008;). The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 3: 245–252 [CrossRef] [PubMed].
    [Google Scholar]
  140. 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 [CrossRef] [PubMed].
    [Google Scholar]
  141. Virgen C. A. , Hatziioannou T. . ( 2007;). Antiretroviral activity and Vif sensitivity of rhesus macaque APOBEC3 proteins. J Virol 81: 13932–13937 [CrossRef] [PubMed].
    [Google Scholar]
  142. Wang X. , Ao Z. , Chen L. , Kobinger G. , Peng J. , Yao X. . ( 2012;). The cellular antiviral protein APOBEC3G interacts with HIV-1 reverse transcriptase and inhibits its function during viral replication. J Virol 86: 3777–3786 [CrossRef] [PubMed].
    [Google Scholar]
  143. Warren C. J. , Griffin L. M. , Little A. S. , Huang I. C. , Farzan M. , Pyeon D. . ( 2014;). The antiviral restriction factors IFITM1, 2 and 3 do not inhibit infection of human papillomavirus, cytomegalovirus and adenovirus. PLoS One 9: e96579 [CrossRef] [PubMed].
    [Google Scholar]
  144. Warren C. J. , Xu T. , Guo K. , Griffin L. M. , Westrich J. A. , Lee D. , Lambert P. F. , Santiago M. L. , Pyeon D. . ( 2015;). APOBEC3A functions as a restriction factor of human papillomavirus. J Virol 89: 688–702 [CrossRef] [PubMed].
    [Google Scholar]
  145. Wichroski M. J. , Ichiyama K. , Rana T. M. . ( 2005;). Analysis of HIV-1 viral infectivity factor-mediated proteasome-dependent depletion of APOBEC3G: correlating function and subcellular localization. J Biol Chem 280: 8387–8396 [CrossRef] [PubMed].
    [Google Scholar]
  146. Wiegand H. L. , Cullen B. R. . ( 2007;). Inhibition of alpharetrovirus replication by a range of human APOBEC3 proteins. J Virol 81: 13694–13699 [CrossRef] [PubMed].
    [Google Scholar]
  147. Xuan D. , Li G. , Cai Q. , Deming-Halverson S. , Shrubsole M. J. , Shu X. O. , Kelley M. C. , Zheng W. , Long J. . ( 2013;). APOBEC3 deletion polymorphism is associated with breast cancer risk among women of European ancestry. Carcinogenesis 34: 2240–2243 [CrossRef] [PubMed].
    [Google Scholar]
  148. Yu X. , Yu Y. , Liu B. , Luo K. , Kong W. , Mao P. , Yu X. F. . ( 2003;). Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif–Cul5–SCF complex. Science 302: 1056–1060 [CrossRef] [PubMed].
    [Google Scholar]
  149. Yu Q. , König R. , Pillai S. , Chiles K. , Kearney M. , Palmer S. , Richman D. , Coffin J. M. , Landau N. R. . ( 2004;). Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat Struct Mol Biol 11: 435–442 [CrossRef] [PubMed].
    [Google Scholar]
  150. Yuan J. , Adamski R. , Chen J. . ( 2010;). Focus on histone variant H2AX: to be or not to be. FEBS Lett 584: 3717–3724 [CrossRef] [PubMed].
    [Google Scholar]
  151. Zhang J. , Webb D. M. . ( 2004;). Rapid evolution of primate antiviral enzyme APOBEC3G. Hum Mol Genet 13: 1785–1791 [CrossRef] [PubMed].
    [Google Scholar]
  152. Zhang H. , Yang B. , Pomerantz R. J. , Zhang C. , Arunachalam S. C. , Gao L. . ( 2003;). The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424: 94–98 [CrossRef] [PubMed].
    [Google Scholar]
  153. Zhang W. , Du J. , Evans S. L. , Yu Y. , Yu X. F. . ( 2012;). T-cell differentiation factor CBF-β regulates HIV-1 Vif-mediated evasion of host restriction. Nature 481: 376–379 [PubMed].
    [Google Scholar]
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