APOBECs and their role in proviral DNA synthesis

Human Immunodeficiency Virus Reverse Transcriptase: A Bench-to-Bedside Success

Volumn , Issue , 2013, Pages 253-280

  Albin, John S ^a   Harris, Reuben S ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84890832226     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-7291-9_12     Document Type: Chapter

References (212)

1. Aiken C, Trono D (1995) Nef stimulates human immunodeficiency virus type 1 proviral DNA synthesis. J Virol 69(8):5048-5056
2. Albin JS, Harris RS (2010) Interactions of host APOBEC3 restriction factors with HIV-1 in vivo: implications for therapeutics. Expert Rev Mol Med 12(e4):1-26
3. Albin JS, Haché G, Hultquist JF, Brown WL, Harris RS (2010a) Long-term restriction by APOBEC3F selects human immunodeficiency virus type 1 variants with restored Vif function. J Virol 84(19):10209-10219
4. Albin JS, LaRue RS, Weaver JA, Brown WL, Shindo K, Harjes E, Harris RS (2010b) A single amino acid in human APOBEC3F alters susceptibility to HIV-1 Vif. J Biol Chem 285(52): 40785-40792
5. Alce TM, Popik W (2004) APOBEC3G is incorporated into virus-like particles by a direct interaction with HIV-1 Gag nucleocapsid protein. J Biol Chem 279(33):34083-34086
6. Amoedo ND, Afonso AO, Cunha SM, Oliveira RH, Machado ES, Soares MA (2011) Expression of APOBEC3G/3F and G-to-A hypermutation levels in HIV-1-Infected children with different profiles of disease progression. PLoS One 6(8):e24118
7. An P, Bleiber G, Duggal P, Nelson G, May M, Mangeat B et al (2004) APOBEC3G genetic variants and their influence on the progression to AIDS. J Virol 78(20):11070-11076
8. An P, Johnson R, Phair J, Kirk GD, Yu XF, Donfield S, Winkler CA (2009) APOBEC3B deletion and risk of HIV-1 acquisition. J Infect Dis 200(7):1054-1058
9. Autore F, Bergeron JR, Malim MH, Fraternali F, Huthoff H (2010) Rationalisation of the differences between APOBEC3G structures from crystallography and NMR studies by molecular dynamics simulations. PLoS One 5(7):e11515
10. Beale RC, Petersen-Mahrt SK, Watt IN, Harris RS, Rada C, Neuberger MS (2004) Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: correlation with mutation spectra in vivo. J Mol Biol 337(3):585-596
11. Berger A, Munk C, Schweizer M, Cichutek K, Schule S, Flory E (2010) Interaction of Vpx and apolipoprotein B mRNA-editing catalytic polypeptide 3 family member A (APOBEC3A) correlates with efficient lentivirus infection of monocytes. J Biol Chem 285(16): 12248-12254
12. Berger A, Sommer AF, Zwarg J, Hamdorf M, Welzel K, Esly N et al (2011a) SAMHD1-Deficient CD14+ Cells from individuals with Aicardi-Goutières syndrome are highly susceptible to HIV-1 infection. PLoS Pathog 7(12):e1002425
13. Berger G, Durand S, Fargier G, Nguyen XN, Cordeil S, Bouaziz S et al (2011b) APOBEC3A is a specific inhibitor of the early phases of HIV-1 infection in myeloid cells. PLoS Pathog 7(9):e1002221
14. Berkhout B, de Ronde A (2004) APOBEC3G versus reverse transcriptase in the generation of HIV-1 drug-resistance mutations. AIDS 18(13):1861-1863
15. Bewick S, Wu J, Lenaghan SC, Yang R, Zhang M, Hamel W (2011) The R5 to X4 coreceptor switch: a dead-end path, or a strategic maneuver? Lessons from a game theoretic analysis. Bull Math Biol 73(10):2339-2356
16. Biasin M, Piacentini L, Lo Caputo S, Kanari Y, Magri G, Trabattoni D et al (2007) Apolipoprotein B mRNA-editing enzyme, catalytic polypeptide-like 3G: a possible role in the resistance to HIV of HIV-exposed seronegative individuals. J Infect Dis 195(7):960-964
17. Bishop KN, Holmes RK, Sheehy AM, Davidson NO, Cho SJ, Malim MH (2004) Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr Biol 14(15):1392-1396
18. Bishop KN, Holmes RK, Malim MH (2006) Antiviral potency of APOBEC proteins does not correlate with cytidine deamination. J Virol 80(17):8450-8458
19. Bishop KN, Verma M, Kim EY, Wolinsky SM, Malim MH (2008) APOBEC3G inhibits elongation of HIV-1 reverse transcripts. PLoS Pathog 4(12):e1000231
20. Bogerd HP, Cullen BR (2008) Single-stranded RNA facilitates nucleocapsid: APOBEC3G complex formation. RNA 14(6):1228-1236
21. Bogerd HP, Doehle BP, Wiegand HL, Cullen BR (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 USA 101(11):3770-3774
22. Bogerd HP, Wiegand HL, Hulme AE, Garcia-Perez JL, O'Shea KS, Moran JV, Cullen BR (2006) Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc Natl Acad Sci USA 103(23):8780-8785
23. Borman AM, Quillent C, Charneau P, Dauguet C, Clavel F (1995) Human immunodeficiency virus type 1 Vif-mutant particles from restrictive cells: role of Vif in correct particle assembly and infectivity. J Virol 69(4):2058-2067
24. Breaker RR (2004) Natural and engineered nucleic acids as tools to explore biology. Nature 432(7019):838-845
25. Britan-Rosich E, Nowarski R, Kotler M (2011) Multifaceted counter-APOBEC3G mechanisms employed by HIV-1 Vif. J Mol Biol 410(5):1065-1076
26. Browne EP, Allers C, Landau NR (2009) Restriction of HIV-1 by APOBEC3G is cytidine deaminase-dependent. Virology 387(2):313-321
27. Cai H, Bloom LB, Eritja R, Goodman MF (1993) Kinetics of deoxyribonucleotide insertion and extension at abasic template lesions in different sequence contexts using HIV-1 reverse transcriptase. J Biol Chem 268(31):23567-23572
28. Cancio R, Spadari S, Maga G (2004) Vif is an auxiliary factor of the HIV-1 reverse transcriptase and facilitates abasic site bypass. Biochem J 383(Pt. 3):475-482
29. Carpenter MA, Rajagurubandara E, Wijesinghe P, Bhagwat AS (2010) Determinants of sequencespecificity within human AID and APOBEC3G. DNA Repair 9(5):579-587
30. Carr JM, Davis AJ, Coolen C, Cheney K, Burrell CJ, Li P (2006) Vif-deficient HIV reverse transcription complexes (RTCs) are subject to structural changes and mutation of RTC-associated reverse transcription products. Virology 351(1):80-91
31. Carr JM, Coolen C, Davis AJ, Burrell CJ, Li P (2008) Human immunodeficiency virus 1 (HIV-1) virion infectivity factor (Vif) is part of reverse transcription complexes and acts as an accessory factor for reverse transcription. Virology 372(1):147-156
32. Cen S, Guo F, Niu M, Saadatmand J, Deflassieux J, Kleiman L (2004) The interaction between HIV-1 Gag and APOBEC3G. J Biol Chem 279(32):33177-33184
33. 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(5):392-399
34. Chelico L, Sacho EJ, Erie DA, Goodman MF (2008) A model for oligomeric regulation of APOBEC3G cytosine deaminase-dependent restriction of HIV. J Biol Chem 283(20): 13780-13791
35. Chelico L, Prochnow C, Erie DA, Chen XS, Goodman MF (2010) Structural model for deoxycytidine deamination mechanisms of the HIV-1 inactivation enzyme APOBEC3G. J Biol Chem 285(21):16195-16205
36. Chen R, Le Rouzic E, Kearney JA, Mansky LM, Benichou S (2004) Vpr-mediated incorporation of UNG2 into HIV-1 particles is required to modulate the virus mutation rate and for replication in macrophages. J Biol Chem 279(27):28419-28425
37. Chen KM, Harjes E, Gross PJ, Fahmy A, Lu Y, Shindo K et al (2008) Structure of the DNA deaminase domain of the HIV-1 restriction factor APOBEC3G. Nature 452(7183):116-119
38. Cho SJ, Drechsler H, Burke RC, Arens MQ, Powderly W, Davidson NO (2006) APOBEC3F and APOBEC3G mRNA levels do not correlate with human immunodeficiency virus type 1 plasma viremia or CD4+ T-cell count. J Virol 80(4):2069-2072
39. Conticello SG (2008) The AID/APOBEC family of nucleic acid mutators. Genome Biol 9(6):229
40. Conticello SG, Harris RS, Neuberger MS (2003) The Vif protein of HIV triggers degradation of the human antiretroviral DNA deaminase APOBEC3G. Curr Biol 13(22):2009-2013
41. Courcoul M, Patience C, Rey F, Blanc D, Harmache A, Sire J et al (1995) Peripheral blood mononuclear cells produce normal amounts of defective Vif-human immunodeficiency virus type 1 particles which are restricted for the preretrotranscription steps. J Virol 69(4):2068-2074
42. Dang Y, Wang X, Esselman WJ, Zheng YH (2006) Identification of APOBEC3DE as another antiretroviral factor from the human APOBEC family. J Virol 80(21):10522-10533
43. Derse D, Hill SA, Princler G, Lloyd P, Heidecker G (2007) Resistance of human T cell leukemia virus type 1 to APOBEC3G restriction is mediated by elements in nucleocapsid. Proc Natl Acad Sci USA 104(8):2915-2920
44. Diamond TL, Roshal M, Jamburuthugoda VK, Reynolds HM, Merriam AR, Lee KY et al (2004) Macrophage tropism of HIV-1 depends on efficient cellular dNTP utilization by reverse transcriptase. J Biol Chem 279(49):51545-51553
45. Do H, Vasilescu A, Diop G, Hirtzig T, Heath SC, Coulonges C et al (2005) Exhaustive genotyping of the CEM15 (APOBEC3G) gene and absence of association with AIDS progression in a French cohort. J Infect Dis 191(2):159-163
46. Duggal NK, Malik HS, Emerman M (2011) Positive selection of Apobec3DE in chimpanzees has driven breadth in anti-viral activity. J Virol 85(21):11361-11371
47. Esnault C, Heidmann O, Delebecque F, Dewannieux M, Ribet D, Hance AJ et al (2005) APOBEC3G cytidine deaminase inhibits retrotransposition of endogenous retroviruses. Nature 433(7024):430-433
48. Esnault C, Millet J, Schwartz O, Heidmann T (2006) Dual inhibitory effects of APOBEC family proteins on retrotransposition of mammalian endogenous retroviruses. Nucleic Acids Res 34(5):1522-1531
49. Feng Y, Chelico L (2011) Intensity of deoxycytidine deamination of HIV-1 proviral DNA by the retroviral restriction factor APOBEC3G is mediated by the noncatalytic domain. J Biol Chem 286(13):11415-11426
50. Fletcher TM 3rd, Brichacek B, Sharova N, Newman MA, Stivahtis G, Sharp PM et al (1996) Nuclear import and cell cycle arrest functions of the HIV-1 Vpr protein are encoded by two separate genes in HIV-2/SIV(SM). EMBO J 15(22):6155-6165
51. Fourati S, Malet I, Binka M, Boukobza S, Wirden M, Sayon S et al (2010) Partially active HIV-1 Vif alleles facilitate viral escape from specific antiretrovirals. AIDS 24(15):2313-2321
52. Friew YN, Boyko V, Hu WS, Pathak VK (2009) Intracellular interactions between APOBEC3G, RNA, and HIV-1 Gag: APOBEC3G multimerization is dependent on its association with RNA. Retrovirology 6:56
53. Furukawa A, Nagata T, Matsugami A, Habu Y, Sugiyama R, Hayashi F et al (2009) Structure, interaction and real-time monitoring of the enzymatic reaction of wild-type APOBEC3G. EMBO J 28(4):440-451
54. Gabuzda DH, Lawrence K, Langhoff E, Terwilliger E, Dorfman T, Haseltine WA, Sodroski J (1992) Role of Vif in replication of human immunodeficiency virus type 1 in CD4+ T lymphocytes. J Virol 66(11):6489-6495
55. Gabuzda DH, Li H, Lawrence K, Vasir BS, Crawford K, Langhoff E (1994) Essential role of vif in establishing productive HIV-1 infection in peripheral blood T lymphocytes and monocyte/macrophages. J Acquir Immune Defic Syndr 7(9):908-915
56. Gandhi SK, Siliciano JD, Bailey JR, Siliciano RF, Blankson JN (2008) Role of APOBEC3G/F-mediated hypermutation in the control of human immunodeficiency virus type 1 in elite suppressors. J Virol 82(6):3125-3130
57. Goldstone DC, Ennis-Adeniran V, Hedden JJ, Groom HC, Rice GI, Christodoulou E et al (2011) HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase. Nature 480(7377):379-382
58. Goncalves J, Korin Y, Zack J, Gabuzda D (1996) Role of Vif in human immunodeficiency virus type 1 reverse transcription. J Virol 70(12):8701-8709
59. Gooch BD, Cullen BR (2008) Functional domain organization of human APOBEC3G. Virology 379(1):118-124
60. Goujon C, Riviere L, Jarrosson-Wuilleme L, Bernaud J, Rigal D, Darlix JL, Cimarelli A (2007) SIVSM/HIV-2 Vpx proteins promote retroviral escape from a proteasome-dependent restriction pathway present in human dendritic cells. Retrovirology 4:2
61. Gramberg T, Sunseri N, Landau NR (2010) Evidence for an activation domain at the amino terminus of simian immunodeficiency virus Vpx. J Virol 84(3):1387-1396
62. Guo F, Cen S, Niu M, Saadatmand J, Kleiman L (2006) Inhibition of formula-primed reverse transcription by human APOBEC3G during human immunodeficiency virus type 1 replication. J Virol 80(23):11710-11722
63. Guo F, Cen S, Niu M, Yang Y, Gorelick RJ, Kleiman L (2007) The interaction of APOBEC3G with human immunodeficiency virus type 1 nucleocapsid inhibits tRNA3Lys annealing to viral RNA. J Virol 81(20):11322-11331
64. Haché G, Liddament MT, Harris RS (2005) The retroviral hypermutation specificity of APOBEC3F and APOBEC3G is governed by the C-terminal DNA cytosine deaminase domain. J Biol Chem 280(12):10920-10924
65. Haché G, Mansky LM, Harris RS (2006) Human APOBEC3 proteins, retrovirus restriction, and HIV drug resistance. AIDS Rev 8(3):148-157
66. Haché G, Shindo K, Albin JS, Harris RS (2008) Evolution of HIV-1 isolates that use a novel Vifindependent mechanism to resist restriction by human APOBEC3G. Curr Biol 18(11):819-824
67. Harjes E, Gross PJ, Chen KM, Lu Y, Shindo K, Nowarski R et al (2009) An extended structure of the APOBEC3G catalytic domain suggests a unique holoenzyme model. J Mol Biol 389(5):819-832
68. Harris RS (2008) Enhancing immunity to HIV through APOBEC. Nat Biotechnol 26(10): 1089-1090
69. Harris RS, Petersen-Mahrt SK, Neuberger MS (2002) RNA editing enzyme APOBEC1 and some of its homologs can act as DNA mutators. Mol Cell 10(5):1247-1253
70. Harris RS, Bishop KN, Sheehy AM, Craig HM, Petersen-Mahrt SK, Watt IN et al (2003a) DNA deamination mediates innate immunity to retroviral infection. Cell 113(6):803-809
71. Harris RS, Sheehy AM, Craig HM, Malim MH, Neuberger MS (2003b) DNA deamination: not just a trigger for antibody diversification but also a mechanism for defense against retroviruses. Nat Immunol 4(7):641-643
72. Holden LG, Prochnow C, Chang YP, Bransteitter R, Chelico L, Sen U et al (2008) Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications. Nature 456(7218):121-124
73. Holmes RK, Koning FA, Bishop KN, Malim MH (2007) APOBEC3F can inhibit the accumulation of HIV-1 reverse transcription products in the absence of hypermutation. Comparisons with APOBEC3G. J Biol Chem 282(4):2587-2595
74. Hrecka K, Hao C, Gierszewska M, Swanson SK, Kesik-Brodacka M, Srivastava S et al (2011) Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474(7353):658-661
75. 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(21):11220-11234
76. Hultquist JF, Binka M, LaRue RS, Simon V, Harris RS (2012) Vif proteins of human and simian immunodeficiency viruses require cellular CBFβ to degrade APOBEC3 restriction factors. J Virol 68(5):2874-2877
77. Huthoff H, Malim MH (2007) Identification of amino acid residues in APOBEC3G required for regulation by human immunodeficiency virus type 1 Vif and Virion encapsidation. J Virol 81(8):3807-3815
78. Huthoff H, Autore F, Gallois-Montbrun S, Fraternali F, Malim MH (2009) RNA-dependent oligomerization of APOBEC3G is required for restriction of HIV-1. PLoS Pathog 5(3):e1000330
79. Itaya S, Nakajima T, Kaur G, Terunuma H, Ohtani H, Mehra N, Kimura A (2010) No evidence of an association between the APOBEC3B deletion polymorphism and susceptibility to HIV infection and AIDS in Japanese and Indian populations. J Infect Dis 202(5):815-816, author reply 816-817
80. Iwatani Y, Takeuchi H, Strebel K, Levin JG (2006) Biochemical activities of highly purified, catalytically active human APOBEC3G: correlation with antiviral effect. J Virol 80(12):5992-6002
81. Iwatani Y, Chan DS, Wang F, Maynard KS, Sugiura W, Gronenborn AM et al (2007) Deaminaseindependent inhibition of HIV-1 reverse transcription by APOBEC3G. Nucleic Acids Res 35(21):7096-7108
82. Jäger S, Kim DY, Hultquist JF, Shindo K, Larue RS, Kwon E et al (2011) Vif hijacks CBFβ to degrade APOBEC3G and promote HIV-1 infection. Nature 481(7381):371-375
83. Janini M, Rogers M, Birx DR, McCutchan FE (2001) 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(17):7973-7986
84. Jern P, Russell RA, Pathak VK, Coffin JM (2009) Likely role of APOBEC3G-mediated G-to-A mutations in HIV-1 evolution and drug resistance. PLoS Pathog 5(4):e1000367
85. Jin X, Brooks A, Chen H, Bennett R, Reichman R, Smith H (2005) APOBEC3G/CEM15 (hA3G) mRNA levels associate inversely with human immunodeficiency virus viremia. J Virol 79(17):11513-11516
86. Kaiser SM, Emerman M (2006) Uracil DNA glycosylase is dispensable for human immunodeficiency virus type 1 replication and does not contribute to the antiviral effects of the cytidine deaminase APOBEC3G. J Virol 80(2):875-882
87. Kao S, Khan MA, Miyagi E, Plishka R, Buckler-White A, Strebel K (2003) The human immunodeficiency virus type 1 Vif protein reduces intracellular expression and inhibits packaging of APOBEC3G (CEM15), a cellular inhibitor of virus infectivity. J Virol 77(21):11398-11407
88. Kaushik R, Zhu X, Stranska R, Wu Y, Stevenson M (2009) A cellular restriction dictates the permissivity of nondividing monocytes/macrophages to lentivirus and gammaretrovirus infection. Cell Host Microbe 6(1):68-80
89. Kewalramani VN, Emerman M (1996) Vpx association with mature core structures of HIV-2. Virology 218(1):159-168
90. Kim EY, Bhattacharya T, Kunstman K, Swantek P, Koning FA, Malim MH (2010) Human APOBEC3G-mediated editing can promote HIV-1 sequence diversification and accelerate adaptation to selective pressure. J Virol 84(19):10402-10405
91. Klarmann GJ, Chen X, North TW, Preston BD (2003) Incorporation of uracil into minus strand DNA affects the specificity of plus strand synthesis initiation during lentiviral reverse transcription. J Biol Chem 278(10):7902-7909
92. Kohli RM, Abrams SR, Gajula KS, Maul RW, Gearhart PJ, Stivers JT (2009) A portable hot spot recognition loop transfers sequence preferences from APOBEC family members to activationinduced cytidine deaminase. J Biol Chem 284(34):22898-22904
93. Kohli RM, Maul RW, Guminski AF, McClure RL, Gajula KS, Saribasak H et al (2010) Local sequence targeting in the AID/APOBEC family differentially impacts retroviral restriction and antibody diversification. J Biol Chem 285(52):40956-40964
94. Koning FA, Newman EN, Kim EY, Kunstman KJ, Wolinsky SM, Malim MH (2009) Defining APOBEC3 expression patterns in human tissues and hematopoietic cell subsets. J Virol 83:9474-9485
95. Koning FA, Goujon C, Bauby H, Malim MH (2011) Target cell-mediated editing of HIV-1 cDNA by APOBEC3 proteins in human macrophages. J Virol 85(24):13448-13452
96. Krokan HE, Drablos F, Slupphaug G (2002) Uracil in DNA-occurrence, consequences and repair. Oncogene 21(58):8935-8948
97. Laguette N, Sobhian B, Casartelli N, Ringeard M, Chable-Bessia C, Segeral E et al (2011) SAMHD1 is the dendritic-and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474(7353):654-657
98. Land AM, Ball TB, Luo M, Pilon R, Sandstrom P, Embree JE et al (2008) Human immunodeficiency virus (HIV) type 1 proviral hypermutation correlates with CD4 count in HIV-infected women from Kenya. J Virol 82(16):8172-8182
99. Langlois MA, Neuberger MS (2008) Human APOBEC3G can restrict retroviral infection in avian cells and acts independently of both UNG and SMUG1. J Virol 82(9):4660-4664
100. Langlois MA, Beale RC, Conticello SG, Neuberger MS (2005) Mutational comparison of the single-domained APOBEC3C and double-domained APOBEC3F/G anti-retroviral cytidine deaminases provides insight into their DNA target site specificities. Nucleic Acids Res 33(6):1913-1923
101. LaRue RS, Jónsson SR, Silverstein KAT, Lajoie M, Bertrand D, El-Mabrouk N et al (2008) The artiodactyl APOBEC3 innate immune repertoire shows evidence for a multi-functional domain organization that existed in the ancestor of placental mammals. BMC Mol Biol 9(1):104, 120 pages
102. LaRue RS, Andrésdóttir V, Blanchard Y, Conticello SG, Derse D, Emerman M et al (2009) Guidelines for naming nonprimate APOBEC3 genes and proteins. J Virol 83(2):494-497
103. Lecossier D, Bouchonnet F, Clavel F, Hance AJ (2003) Hypermutation of HIV-1 DNA in the absence of the Vif protein. Science 300(5622):1112
104. Li J, Potash MJ, Volsky DJ (2004) Functional domains of APOBEC3G required for antiviral activity. J Cell Biochem 92(3):560-572
105. Li XY, Guo F, Zhang L, Kleiman L, Cen S (2007) APOBEC3G inhibits DNA strand transfer during HIV-1 reverse transcription. J Biol Chem 282(44):32065-32074
106. Li X, Ma J, Zhang Q, Zhou J, Yin X, Zhai C et al (2011) Functional analysis of the two cytidine deaminase domains in APOBEC3G. Virology 414(2):130-136
107. Li M, Shandilya SM, Carpenter MA, Rathore A, Brown WL, Perkins AL et al (2012) First-in-class small molecule inhibitors of the single-strand DNA cytosine deaminase APOBEC3G. ACS Chem Biol 7(3):506-517
108. Liddament MT, Brown WL, Schumacher AJ, Harris RS (2004) APOBEC3F properties and hypermutation preferences indicate activity against HIV-1 in vivo. Curr Biol 14(15):1385-1391
109. Löchelt M, Romen F, Bastone P, Muckenfuss H, Kirchner N, Kim YB et al (2005) The antiretroviral activity of APOBEC3 is inhibited by the foamy virus accessory Bet protein. Proc Natl Acad Sci USA 102(22):7982-7987
110. Loeb LA, Essigmann JM, Kazazi F, Zhang J, Rose KD, Mullins JI (1999) Lethal mutagenesis of HIV with mutagenic nucleoside analogs. Proc Natl Acad Sci USA 96(4):1492-1497
111. Luo K, Liu B, Xiao Z, Yu Y, Yu X, Gorelick R, Yu XF (2004) Amino-terminal region of the human immunodeficiency virus type 1 nucleocapsid is required for human APOBEC3G packaging. J Virol 78(21):11841-11852
112. Luo K, Wang T, Liu B, Tian C, Xiao Z, Kappes J, Yu XF (2007) Cytidine deaminases APOBEC3G and APOBEC3F interact with human immunodeficiency virus type 1 integrase and inhibit proviral DNA formation. J Virol 81(13):7238-7248
113. Madani N, Kabat D (1998) An endogenous inhibitor of human immunodeficiency virus in human lymphocytes is overcome by the viral Vif protein. J Virol 72(12):10251-10255
114. 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(6944):99-103
115. Mangeat B, Turelli P, Liao S, Trono D (2004) A single amino acid determinant governs the speciesspecific sensitivity of APOBEC3G to Vif action. J Biol Chem 279(15):14481-14483
116. Mansky LM, Temin HM (1995) Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J Virol 69(8): 5087-5094
117. Mansky LM, Preveral S, Selig L, Benarous R, Benichou S (2000) The interaction of Vpr with uracil DNA glycosylase modulates the human immunodeficiency virus type 1 In vivo mutation rate. J Virol 74(15):7039-7047
118. Marin M, Rose KM, Kozak SL, Kabat D (2003) HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat Med 9(11):1398-1403
119. Mbisa JL, Barr R, Thomas JA, Vandegraaff N, Dorweiler IJ, Svarovskaia ES et al (2007) Human immunodeficiency virus type 1 cDNAs produced in the presence of APOBEC3G exhibit defects in plus-strand DNA transfer and integration. J Virol 81(13):7099-7110
120. Mbisa JL, Bu W, Pathak VK (2010) APOBEC3F and APOBEC3G inhibit HIV-1 DNA integration by different mechanisms. J Virol 84(10):5250-5259
121. Mehle A, Strack B, Ancuta P, Zhang C, McPike M, Gabuzda D (2004) Vif overcomes the innate antiviral activity of APOBEC3G by promoting its degradation in the ubiquitin-proteasome pathway. J Biol Chem 279(9):7792-7798
122. 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(24):13346-13353
123. Miyagi E, Brown CR, Opi S, Khan M, Goila-Gaur R, Kao S et al (2010) Stably expressed APOBEC3F has negligible antiviral activity. J Virol 84(21):11067-11075
124. Muckenfuss H, Hamdorf M, Held U, Perkovic M, Lower J, Cichutek K et al (2006) APOBEC3 proteins inhibit human LINE-1 retrotransposition. J Biol Chem 281(31):22161-22172
125. Mulder LC, Harari A, Simon V (2008) Cytidine deamination induced HIV-1 drug resistance. Proc Natl Acad Sci USA 105(14):5501-5506
126. Navarro F, Bollman B, Chen H, Konig R, Yu Q, Chiles K, Landau NR (2005) Complementary function of the two catalytic domains of APOBEC3G. Virology 333(2):374-386
127. Neil S, Martin F, Ikeda Y, Collins M (2001) Postentry restriction to human immunodeficiency virus-based vector transduction in human monocytes. J Virol 75(12):5448-5456
128. Newman EN, Holmes RK, Craig HM, Klein KC, Lingappa JR, Malim MH, Sheehy AM (2005) Antiviral function of APOBEC3G can be dissociated from cytidine deaminase activity. Curr Biol 15(2):166-170
129. Nowarski R, Britan-Rosich E, Shiloach T, Kotler M (2008) Hypermutation by intersegmental transfer of APOBEC3G cytidine deaminase. Nat Struct Mol Biol 15(10):1059-1066
130. OhAinle M, Kerns JA, Malik HS, Emerman M (2006) Adaptive evolution and antiviral activity of the conserved mammalian cytidine deaminase APOBEC3H. J Virol 80(8):3853-3862
131. OhAinle M, Kerns JA, Li MM, Malik HS, Emerman M (2008) Antiretroelement activity of APOBEC3H was lost twice in recent human evolution. Cell Host Microbe 4(3): 249-259
132. Okeoma CM, Lovsin N, Peterlin BM, Ross SR (2007) APOBEC3 inhibits mouse mammary tumour virus replication in vivo. Nature 445(7130):927-930
133. Opi S, Takeuchi H, Kao S, Khan MA, Miyagi E, Goila-Gaur R et al (2006) Monomeric APOBEC3G is catalytically active and has antiviral activity. J Virol 80(10):4673-4682
134. Pace C, Keller J, Nolan D, James I, Gaudieri S, Moore C, Mallal S (2006) Population level analysis of human immunodeficiency virus type 1 hypermutation and its relationship with APOBEC3G and vif genetic variation. J Virol 80(18):9259-9269
135. Pathak VK, Temin HM (1990) Broad spectrum of in vivo forward mutations, hypermutations, and mutational hotspots in a retroviral shuttle vector after a single replication cycle: substitutions, frameshifts, and hypermutations. Proc Natl Acad Sci USA 87(16):6019-6023
136. Peng G, Greenwell-Wild T, Nares S, Jin W, Lei KJ, Rangel ZG et al (2007) Myeloid differentiation and susceptibility to HIV-1 are linked to APOBEC3 expression. Blood 110(1):393-400
137. Pertel T, Hausmann S, Morger D, Zuger S, Guerra J, Lascano J et al (2011) TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 472(7343):361-365
138. Piantadosi A, Humes D, Chohan B, McClelland RS, Overbaugh J (2009) Analysis of the percentage of human immunodeficiency virus type 1 sequences that are hypermutated and markers of disease progression in a longitudinal cohort, including one individual with a partially defective Vif. J Virol 83(16):7805-7814
139. Pillai SK, Wong JK, Barbour JD (2008) Turning up the volume on mutational pressure: is more of a good thing always better? (A case study of HIV-1 Vif and APOBEC3). Retrovirology 5:26
140. Pillai SK, Abdel-Mohsen M, Guatelli J, Skasko M, Monto A, Fujimoto K et al (2012) Role of retroviral restriction factors in the interferon-alpha-mediated suppression of HIV-1 in vivo. Proc Natl Acad Sci USA 109(8):3035-3040
141. Powell RD, Holland PJ, Hollis T, Perrino FW (2011) Aicardi-Goutières syndrome gene and HIV-1 restriction factor SAMHD1 Is a dGTP-regulated deoxynucleotide triphosphohydrolase. J Biol Chem 286(51):43596-43600
142. Priet S, Gros N, Navarro JM, Boretto J, Canard B, Querat G, Sire J (2005) HIV-1-associated uracil DNA glycosylase activity controls dUTP misincorporation in viral DNA and is essential to the HIV-1 life cycle. Mol Cell 17(4):479-490
143. Rai K, Huggins IJ, James SR, Karpf AR, Jones DA, Cairns BR (2008) DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell 135(7): 1201-1212
144. Rausch JW, Chelico L, Goodman MF, Le Grice SF (2009) Dissecting APOBEC3G substrate specificity by nucleoside analog interference. J Biol Chem 284(11):7047-7058
145. Reddy K, Winkler CA, Werner L, Mlisana K, Abdool Karim SS, Ndung'u T (2010) APOBEC3G expression is dysregulated in primary HIV-1 infection and polymorphic variants influence CD4+ T-cell counts and plasma viral load. AIDS 24(2):195-204
146. 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(13):4274-4284
147. Refsland EW, Hultquist JF, Harris RS (2012) Endogenous origins of HIV-1 G-to-A hypermutation. PLoS Pathog 8(7):e1002800
148. Rice GI, Bond J, Asipu A, Brunette RL, Manfield IW, Carr IM et al (2009) Mutations involved in Aicardi-Goutières syndrome implicate SAMHD1 as regulator of the innate immune response. Nat Genet 41(7):829-832
149. Russell RA, Wiegand HL, Moore MD, Schafer A, McClure MO, Cullen BR (2005) Foamy virus Bet proteins function as novel inhibitors of the APOBEC3 family of innate antiretroviral defense factors. J Virol 79(14):8724-8731
150. Russell RA, Moore MD, Hu WS, Pathak VK (2009) APOBEC3G induces a hypermutation gradient: purifying selection at multiple steps during HIV-1 replication results in levels of G-to-A mutations that are high in DNA, intermediate in cellular viral RNA, and low in virion RNA. Retrovirology 6:16
151. Sadler HA, Stenglein MD, Harris RS, Mansky LM (2010) APOBEC3G contributes to HIV-1 variation through sublethal mutagenesis. J Virol 84(14):7396-7404
152. Santa-Marta M, da Silva FA, Fonseca AM, Goncalves J (2005) HIV-1 Vif can directly inhibit apolipoprotein B mRNA-editing enzyme catalytic polypeptide-like 3G-mediated cytidine deamination by using a single amino acid interaction and without protein degradation. J Biol Chem 280(10):8765-8775
153. Sawyer SL, Emerman M, Malik HS (2004) Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2(9):E275
154. Sayah DM, Sokolskaja E, Berthoux L, Luban J (2004) Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430(6999):569-573
155. Schafer A, Bogerd HP, Cullen BR (2004) Specific packaging of APOBEC3G into HIV-1 virions is mediated by the nucleocapsid domain of the gag polyprotein precursor. Virology 328(2): 163-168
156. Schröfelbauer B, Chen D, Landau NR (2004) A single amino acid of APOBEC3G controls its species-specific interaction with virion infectivity factor (Vif). Proc Natl Acad Sci USA 101(11):3927-3932
157. Schröfelbauer B, Yu Q, Zeitlin SG, Landau NR (2005) Human immunodeficiency virus type 1 Vpr induces the degradation of the UNG and SMUG uracil-DNA glycosylases. J Virol 79(17):10978-10987
158. Schumacher AJ, Haché G, MacDuff DA, Brown WL, Harris RS (2008) The DNA deaminase activity of human APOBEC3G is required for Ty1, MusD, and human immunodeficiency virus type 1 restriction. J Virol 82(6):2652-2660
159. Schwartz O, Marechal V, Danos O, Heard JM (1995) Human immunodeficiency virus type 1 Nef increases the efficiency of reverse transcription in the infected cell. J Virol 69(7):4053-4059
160. Shandilya SM, Nalam MN, Nalivaika EA, Gross PJ, Valesano JC, Shindo K et al (2010) Crystal structure of the APOBEC3G catalytic domain reveals potential oligomerization interfaces. Structure 18(1):28-38
161. 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(6898):646-650
162. Sheehy AM, Gaddis NC, Malim MH (2003) The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat Med 9(11):1404-1407
163. Shindo K, Takaori-Kondo A, Kobayashi M, Abudu A, Fukunaga K, Uchiyama T (2003) The enzymatic activity of CEM15/Apobec-3G is essential for the regulation of the infectivity of HIV-1 virion but not a sole determinant of its antiviral activity. J Biol Chem 278(45):44412-44416
164. Shlyakhtenko LS, Lushnikov AY, Li M, Lackey L, Harris RS, Lyubchenko YL (2011) Atomic force microscopy studies provide direct evidence for dimerization of the HIV restriction factor APOBEC3G. J Biol Chem 286(5):3387-3395
165. Simon JH, Malim MH (1996) The human immunodeficiency virus type 1 Vif protein modulates the postpenetration stability of viral nucleoprotein complexes. J Virol 70(8):5297-5305
166. Simon JH, Gaddis NC, Fouchier RA, Malim MH (1998) Evidence for a newly discovered cellular anti-HIV-1 phenotype. Nat Med 4(12):1397-1400
167. Simon V, Zennou V, Murray D, Huang Y, Ho DD, Bieniasz PD (2005) Natural variation in Vif: differential impact on APOBEC3G/3F and a potential role in HIV-1 diversification. PLoS Pathog 1(1):e6
168. Smith JL, Pathak VK (2010) Identification of specific determinants of human APOBEC3F, APOBEC3C, and APOBEC3DE and African green monkey APOBEC3F that interact with HIV-1 Vif. J Virol 84(24):12599-12608
169. Soros VB, Yonemoto W, Greene WC (2007) Newly synthesized APOBEC3G is incorporated into HIV virions, inhibited by HIV RNA, and subsequently activated by RNase H. PLoS Pathog 3(2):e15
170. Sova P, Volsky DJ (1993) Efficiency of viral DNA synthesis during infection of permissive and nonpermissive cells with vif-negative human immunodeficiency virus type 1. J Virol 67(10):6322-6326
171. Stenglein MD, Harris RS (2006) APOBEC3B and APOBEC3F inhibit L1 retrotransposition by a DNA deamination-independent mechanism. J Biol Chem 281(25):16837-16841
172. 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(2):222-229
173. Stetson DB, Ko JS, Heidmann T, Medzhitov R (2008) Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 134(4):587-598
174. Stevenson M, Stanwick TL, Dempsey MP, Lamonica CA (1990) HIV-1 replication is controlled at the level of T cell activation and proviral integration. EMBO J 9(5):1551-1560
175. 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(3):591-601
176. Strebel K, Daugherty D, Clouse K, Cohen D, Folks T, Martin MA (1987) The HIV 'A' (sor) gene product is essential for virus infectivity. Nature 328(6132):728-730
177. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J (2004) The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427(6977):848-853
178. Sunseri N, O'Brien M, Bhardwaj N, Landau NR (2011) Human immunodeficiency virus type 1 modified to package Simian immunodeficiency virus Vpx efficiently infects macrophages and dendritic cells. J Virol 85(13):6263-6274
179. Suspène R, Sommer P, Henry M, Ferris S, Guetard D, Pochet S et al (2004) APOBEC3G is a single-stranded DNA cytidine deaminase and functions independently of HIV reverse transcriptase. Nucleic Acids Res 32(8):2421-2429
180. Suspène R, Rusniok C, Vartanian JP, Wain-Hobson S (2006) Twin gradients in APOBEC3 edited HIV-1 DNA reflect the dynamics of lentiviral replication. Nucleic Acids Res 34(17):4677-4684
181. Svarovskaia ES, Xu H, Mbisa JL, Barr R, Gorelick RJ, Ono A et al (2004) Human apolipoprotein B mRNA-editing enzyme-catalytic polypeptide-like 3G (APOBEC3G) is incorporated into HIV-1 virions through interactions with viral and nonviral RNAs. J Biol Chem 279(34):35822-35828
182. Tan L, Sarkis PT, Wang T, Tian C, Yu XF (2009) Sole copy of Z2-type human cytidine deaminase APOBEC3H has inhibitory activity against retrotransposons and HIV-1. FASEB J 23(1): 279-287
183. Thielen BK, McNevin JP, McElrath MJ, Hunt BV, Klein KC, Lingappa JR (2010) Innate immune signaling induces high levels of TC-specific deaminase activity in primary monocyte-derived cells through expression of APOBEC3A isoforms. J Biol Chem 285(36):27753-27766
184. Tian C, Wang T, Zhang W, Yu XF (2007) Virion packaging determinants and reverse transcription of SRP RNA in HIV-1 particles. Nucleic Acids Res 35(21):7288-7302
185. Towers GJ, Hatziioannou T, Cowan S, Goff SP, Luban J, Bieniasz PD (2003) Cyclophilin A modulates the sensitivity of HIV-1 to host restriction factors. Nat Med 9(9):1138-1143
186. Turelli P, Mangeat B, Jost S, Vianin S, Trono D (2004) Inhibition of hepatitis B virus replication by APOBEC3G. Science 303(5665):1829
187. Ulenga NK, Sarr AD, Hamel D, Sankale JL, Mboup S, Kanki PJ (2008a) The level of APOBEC3G (hA3G)-related G-to-A mutations does not correlate with viral load in HIV type 1-infected individuals. AIDS Res Hum Retroviruses 24(10):1285-1290
188. Ulenga NK, Sarr AD, Thakore-Meloni S, Sankale JL, Eisen G, Kanki PJ (2008b) Relationship between human immunodeficiency type 1 infection and expression of human APOBEC3G and APOBEC3F. J Infect Dis 198(4):486-492
189. Vartanian JP, Meyerhans A, Asjo B, Wain-Hobson S (1991) Selection, recombination, and G → A hypermutation of human immunodeficiency virus type 1 genomes. J Virol 65(4):1779-1788
190. Vartanian JP, Meyerhans A, Sala M, Wain-Hobson S (1994) G → A hypermutation of the human immunodeficiency virus type 1 genome: evidence for dCTP pool imbalance during reverse transcription. Proc Natl Acad Sci USA 91(8):3092-3096
191. Vazquez-Perez JA, Ormsby CE, Hernandez-Juan R, Torres KJ, Reyes-Teran G (2009) APOBEC3G mRNA expression in exposed seronegative and early stage HIV infected individuals decreases with removal of exposure and with disease progression. Retrovirology 6:23
192. von Schwedler U, Song J, Aiken C, Trono D (1993) Vif is crucial for human immunodeficiency virus type 1 proviral DNA synthesis in infected cells. J Virol 67(8):4945-4955
193. Wang T, Tian C, Zhang W, Luo K, Sarkis PT, Yu L (2007) 7SL RNA mediates virion packaging of the antiviral cytidine deaminase APOBEC3G. J Virol 81(23):13112-13124
194. Wang T, Tian C, Zhang W, Sarkis PT, Yu XF (2008) Interaction with 7SL RNA but not with HIV-1 genomic RNA or P bodies is required for APOBEC3F virion packaging. J Mol Biol 375(4):1098-1112
195. 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(7):3777-3786
196. Watts JM, Dang KK, Gorelick RJ, Leonard CW, Bess JW Jr, Swanstrom R et al (2009) Architecture and secondary structure of an entire HIV-1 RNA genome. Nature 460(7256):711-716
197. Wedekind JE, Gillilan R, Janda A, Krucinska J, Salter JD, Bennett RP et al (2006) Nanostructures of APOBEC3G support a hierarchical assembly model of high molecular mass ribonucleoprotein particles from dimeric subunits. J Biol Chem 281(50):38122-38126
198. Wiegand HL, Doehle BP, Bogerd HP, Cullen BR (2004) A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins. EMBO J 23(12):2451-2458
199. Wood N, Bhattacharya T, Keele BF, Giorgi E, Liu M, Gaschen B et al (2009) HIV evolution in early infection: selection pressures, patterns of insertion and deletion, and the impact of APOBEC. PLoS Pathog 5(5):e1000414
200. Xu H, Svarovskaia ES, Barr R, Zhang Y, Khan MA, Strebel K, Pathak VK (2004) A single amino acid substitution in human APOBEC3G antiretroviral enzyme confers resistance to HIV-1 virion infectivity factor-induced depletion. Proc Natl Acad Sci USA 101(15):5652-5657
201. Xu H, Chertova E, Chen J, Ott DE, Roser JD, Hu WS, Pathak VK (2007) Stoichiometry of the antiviral protein APOBEC3G in HIV-1 virions. Virology 360(2):247-256
202. Yan N, O'Day E, Wheeler LA, Engelman A, Lieberman J (2011) HIV DNA is heavily uracilated, which protects it from autointegration. Proc Natl Acad Sci USA 108(22):9244-9249
203. Yang B, Chen K, Zhang C, Huang S, Zhang H (2007a) Virion-associated uracil DNA glycosylase-2 and apurinic/apyrimidinic endonuclease are involved in the degradation of APOBEC3Gedited nascent HIV-1 DNA. J Biol Chem 282(16):11667-11675
204. Yang Y, Guo F, Cen S, Kleiman L (2007b) Inhibition of initiation of reverse transcription in HIV-1 by human APOBEC3F. Virology 365(1):92-100
205. Yu X, Yu Y, Liu B, Luo K, Kong W, Mao P, Yu XF (2003) Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302(5647):1056-1060
206. Yu Q, Konig R, Pillai S, Chiles K, Kearney M, Palmer S et al (2004) Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat Struct Mol Biol 11(5):435-442
207. Zack JA, Arrigo SJ, Weitsman SR, Go AS, Haislip A, Chen IS (1990) HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 61(2): 213-222
208. Zennou V, Perez-Caballero D, Gottlinger H, Bieniasz PD (2004) APOBEC3G incorporation into human immunodeficiency virus type 1 particles. J Virol 78(21):12058-12061
209. Zhang H, Yang B, Pomerantz RJ, Zhang C, Arunachalam SC, Gao L (2003) The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424(6944):94-98
210. Zhang W, Du J, Evans SL, Yu Y, Yu XF (2011) T-cell differentiation factor CBFβ regulates HIV-1 Vif-mediated evasion of host restriction. Nature 481(7381):376-379
211. Zhen A, Wang T, Zhao K, Xiong Y, Yu XF (2010) A single amino acid difference in human APOBEC3H variants determines HIV-1 Vif sensitivity. J Virol 84(4):1902-1911
212. Zheng YH, 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(11):6073-6076