APOBEC3D and APOBEC3F Potently Promote HIV-1 Diversification and Evolution in Humanized Mouse Model

1. ConticelloSG (2008) The AID/APOBEC family of nucleic acid mutators. Genome Biol 9 : 229.

2. ConticelloSG, LangloisMA, YangZ, NeubergerMS (2007) DNA deamination in immunity: AID in the context of its APOBEC relatives. Adv Immunol 94 : 37–73.

3. TengB, BurantCF, DavidsonNO (1993) Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science 260 : 1816–1819.

4. HarrisRS, LiddamentMT (2004) Retroviral restriction by APOBEC proteins. Nat Rev Immunol 4 : 868–877.

5. ZhangJ (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18 : 292–298.

6. SawyerSL, EmermanM, MalikHS (2004) Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2: E275.

7. StengleinMD, BurnsMB, LiM, LengyelJ, HarrisRS (2010) APOBEC3 proteins mediate the clearance of foreign DNA from human cells. Nat Struct Mol Biol 17 : 222–229.

8. BurnsMB, TemizNA, HarrisRS (2013) Evidence for APOBEC3B mutagenesis in multiple human cancers. Nat Genet 45 : 977–983.

9. ShinoharaM, IoK, ShindoK, MatsuiM, SakamotoT, et al. (2012) APOBEC3B can impair genomic stability by inducing base substitutions in genomic DNA in human cells. Sci Rep 2 : 806.

10. BurnsMB, LackeyL, CarpenterMA, RathoreA, LandAM, et al. (2013) APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 494 : 366–370.

11. SheehyAM, GaddisNC, ChoiJD, MalimMH (2002) Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418 : 646–650.

12. IzumiT, ShirakawaK, Takaori-KondoA (2008) Cytidine deaminases as a weapon against retroviruses and a new target for antiviral therapy. Mini Rev Med Chem 8 : 231–238.

13. DangY, WangX, EsselmanWJ, ZhengYH (2006) Identification of APOBEC3DE as another antiretroviral factor from the human APOBEC family. J Virol 80 : 10522–10533.

14. LiddamentMT, BrownWL, SchumacherAJ, HarrisRS (2004) APOBEC3F properties and hypermutation preferences indicate activity against HIV-1 in vivo. Curr Biol 14 : 1385–1391.

15. RefslandEW, HultquistJF, HarrisRS (2012) Endogenous origins of HIV-1 G-to-A hypermutation and restriction in the nonpermissive T cell line CEM2n. PLoS Pathog 8: e1002800.

16. MiyagiE, BrownCR, OpiS, KhanM, Goila-GaurR, et al. (2010) Stably expressed APOBEC3F has negligible antiviral activity. J Virol 84 : 11067–11075.

17. ChaipanC, SmithJL, HuWS, PathakVK (2013) APOBEC3G restricts HIV-1 to a greater extent than APOBEC3F and APOBEC3DE in human primary CD4+ T cells and macrophages. J Virol 87 : 444–453.

18. PillaiSK, WongJK, BarbourJD (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.

19. CasartelliN, Guivel-BenhassineF, BouziatR, BrandlerS, SchwartzO, et al. (2010) The antiviral factor APOBEC3G improves CTL recognition of cultured HIV-infected T cells. J Exp Med 207 : 39–49.

20. JernP, RussellRA, PathakVK, CoffinJM (2009) Likely role of APOBEC3G-mediated G-to-A mutations in HIV-1 evolution and drug resistance. PLoS Pathog 5: e1000367.

21. WoodN, BhattacharyaT, KeeleBF, GiorgiE, LiuM, et al. (2009) HIV evolution in early infection: selection pressures, patterns of insertion and deletion, and the impact of APOBEC. PLoS Pathog 5: e1000414.

22. NieC, SatoK, MisawaN, KitayamaH, FujinoH, et al. (2009) Selective infection of CD4+ effector memory T lymphocytes leads to preferential depletion of memory T lymphocytes in R5 HIV-1-infected humanized NOD/SCID/IL-2Rγnull mice. Virology 394 : 64–72.

23. SatoK, IzumiT, MisawaN, KobayashiT, YamashitaY, et al. (2010) Remarkable lethal G-to-A mutations in vif-proficient HIV-1 provirus by individual APOBEC3 proteins in humanized mice. J Virol 84 : 9546–9556.

24. SatoK, KoyanagiY (2011) The mouse is out of the bag: insights and perspectives on HIV-1-infected humanized mouse models. Exp Biol Med 236 : 977–985.

25. SatoK, MisawaN, FukuharaM, IwamiS, AnDS, et al. (2012) Vpu augments the initial burst phase of HIV-1 propagation and downregulates BST2 and CD4 in humanized mice. J Virol 86 : 5000–5013.

26. SatoK, MisawaN, NieC, SatouY, IwakiriD, et al. (2011) A novel animal model of Epstein-Barr virus-associated hemophagocytic lymphohistiocytosis in humanized mice. Blood 117 : 5663–5673.

27. SatoK, NieC, MisawaN, TanakaY, ItoM, et al. (2010) Dynamics of memory and naive CD8+ T lymphocytes in humanized NOD/SCID/IL-2Rγnull mice infected with CCR5-tropic HIV-1. Vaccine 28 Suppl 2: B32–37.

28. SatoK, MisawaN, IwamiS, SatouY, MatsuokaM, et al. (2013) HIV-1 Vpr accelerates viral replication during acute infection by exploitation of proliferating CD4+ T cells in vivo. PLoS Pathog 9: e1003812.

29. FitzgibbonJE, MazarS, DubinDT (1993) A new type of G→A hypermutation affecting human immunodeficiency virus. AIDS Res Hum Retroviruses 9 : 833–838.

30. GandhiSK, SilicianoJD, BaileyJR, SilicianoRF, BlanksonJN (2008) Role of APOBEC3G/F-mediated hypermutation in the control of human immunodeficiency virus type 1 in elite suppressors. J Virol 82 : 3125–3130.

31. JaniniM, RogersM, BirxDR, McCutchanFE (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 : 7973–7986.

32. PaceC, KellerJ, NolanD, JamesI, GaudieriS, et al. (2006) Population level analysis of human immunodeficiency virus type 1 hypermutation and its relationship with APOBEC3G and vif genetic variation. J Virol 80 : 9259–9269.

33. PiantadosiA, HumesD, ChohanB, McClellandRS, OverbaughJ (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 : 7805–7814.

34. UlengaNK, SarrAD, HamelD, SankaleJL, MboupS, et al. (2008) 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 : 1285–1290.

35. VartanianJP, HenryM, Wain-HobsonS (2002) Sustained G→A hypermutation during reverse transcription of an entire human immunodeficiency virus type 1 strain Vau group O genome. J Gen Virol 83 : 801–805.

36. VartanianJP, MeyerhansA, AsjoB, Wain-HobsonS (1991) Selection, recombination, and G→A hypermutation of human immunodeficiency virus type 1 genomes. J Virol 65 : 1779–1788.

37. KijakGH, JaniniLM, TovanabutraS, Sanders-BuellE, ArroyoMA, et al. (2008) Variable contexts and levels of hypermutation in HIV-1 proviral genomes recovered from primary peripheral blood mononuclear cells. Virology 376 : 101–111.

38. RussellRA, PathakVK (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.

39. SmithJL, PathakVK (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 : 12599–12608.

40. SuzukiY, KoyanagiY, TanakaY, MurakamiT, MisawaN, et al. (1999) Determinant in human immunodeficiency virus type 1 for efficient replication under cytokine-induced CD4+ T-helper 1 (Th1) -⁠ and Th2-type conditions. J Virol 73 : 316–324.

41. KriskoJF, Martinez-TorresF, FosterJL, GarciaJV (2013) HIV restriction by APOBEC3 in humanized mice. PLoS Pathog 9: e1003242.

42. KoningFA, NewmanEN, KimEY, KunstmanKJ, WolinskySM, et al. (2009) Defining APOBEC3 expression patterns in human tissues and hematopoietic cell subsets. J Virol 83 : 9474–9485.

43. RefslandEW, StengleinMD, ShindoK, AlbinJS, BrownWL, et al. (2010) Quantitative profiling of the full APOBEC3 mRNA repertoire in lymphocytes and tissues: implications for HIV-1 restriction. Nucleic Acids Res 38 : 4274–4284.

44. LepelleyA, LouisS, SourisseauM, LawHK, PothlichetJ, et al. (2011) Innate sensing of HIV-infected cells. PLoS Pathog 7: e1001284.

45. von SydowM, SonnerborgA, GainesH, StrannegardO (1991) Interferon-α and tumor necrosis factor-α in serum of patients in various stages of HIV-1 infection. AIDS Res Hum Retroviruses 7 : 375–380.

46. PillaiSK, Abdel-MohsenM, GuatelliJ, SkaskoM, MontoA, et al. (2012) Role of retroviral restriction factors in the interferon-α-mediated suppression of HIV-1 in vivo. Proc Natl Acad Sci U S A 109 : 3035–3040.

47. StopakKS, ChiuYL, KroppJ, GrantRM, GreeneWC (2007) Distinct patterns of cytokine regulation of APOBEC3G expression and activity in primary lymphocytes, macrophages, and dendritic cells. J Biol Chem 282 : 3539–3546.

48. HultquistJF, LengyelJA, RefslandEW, LaRueRS, LackeyL, et al. (2011) Human and rhesus APOBEC3D, APOBEC3F, APOBEC3G, and APOBEC3H demonstrate a conserved capacity to restrict Vif-deficient HIV-1. J Virol 85 : 11220–11234.

49. SuspeneR, RusniokC, VartanianJP, Wain-HobsonS (2006) Twin gradients in APOBEC3 edited HIV-1 DNA reflect the dynamics of lentiviral replication. Nucleic Acids Res 34 : 4677–4684.

50. PalmerS, KearneyM, MaldarelliF, HalvasEK, BixbyCJ, et al. (2005) Multiple, linked human immunodeficiency virus type 1 drug resistance mutations in treatment-experienced patients are missed by standard genotype analysis. J Clin Microbiol 43 : 406–413.

51. YuQ, KonigR, PillaiS, ChilesK, KearneyM, et al. (2004) Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat Struct Mol Biol 11 : 435–442.

52. De JongJJ, De RondeA, KeulenW, TersmetteM, GoudsmitJ (1992) Minimal requirements for the human immunodeficiency virus type 1 V3 domain to support the syncytium-inducing phenotype: analysis by single amino acid substitution. J Virol 66 : 6777–6780.

53. ShiodaT, LevyJA, Cheng-MayerC (1992) Small amino acid changes in the V3 hypervariable region of gp120 can affect the T-cell-line and macrophage tropism of human immunodeficiency virus type 1. Proc Natl Acad Sci U S A 89 : 9434–9438.

54. LengauerT, SanderO, SierraS, ThielenA, KaiserR (2007) Bioinformatics prediction of HIV coreceptor usage. Nat Biotechnol 25 : 1407–1410.

55. EbrahimiD, AnwarF, DavenportMP (2012) APOBEC3G and APOBEC3F rarely co-mutate the same HIV genome. Retrovirology 9 : 113.

56. MulderLC, OomsM, MajdakS, SmedresmanJ, LinscheidC, et al. (2010) Moderate influence of human APOBEC3F on HIV-1 replication in primary lymphocytes. J Virol 84 : 9613–9617.

57. BishopKN, HolmesRK, MalimMH (2006) Antiviral potency of APOBEC proteins does not correlate with cytidine deamination. J Virol 80 : 8450–8458.

58. HolmesRK, KoningFA, BishopKN, MalimMH (2007) APOBEC3F can inhibit the accumulation of HIV-1 reverse transcription products in the absence of hypermutation. Comparisons with APOBEC3G. J Biol Chem 282 : 2587–2595.

59. BishopKN, VermaM, KimEY, WolinskySM, MalimMH (2008) APOBEC3G inhibits elongation of HIV-1 reverse transcripts. PLoS Pathog 4: e1000231.

60. GillickK, PollpeterD, PhaloraP, KimEY, WolinskySM, et al. (2013) Suppression of HIV-1 infection by APOBEC3 proteins in primary human CD4+ T cells is associated with inhibition of processive reverse transcription as well as excessive cytidine deamination. J Virol 87 : 1508–1517.

61. KobayashiT, KoizumiY, TakeuchiJS, MisawaN, KimuraY, et al. (2014) Quantification of deaminase activity-dependent and -independent restriction of HIV-1 replication mediated by APOBEC3F and APOBEC3G through experimental-mathematical investigation. J Virol 88 : 5881–5887.

62. AlbinJS, BrownWL, HarrisRS (2014) Catalytic activity of APOBEC3F is required for efficient restriction of Vif-deficient human immunodeficiency virus. Virology 450–451 : 49–54.

63. MbisaJL, BuW, PathakVK (2010) APOBEC3F and APOBEC3G inhibit HIV-1 DNA integration by different mechanisms. J Virol 84 : 5250–5259.

64. SimonV, ZennouV, MurrayD, HuangY, HoDD, et al. (2005) Natural variation in Vif: differential impact on APOBEC3G/3F and a potential role in HIV-1 diversification. PLoS Pathog 1: e6.

65. ItoM, HiramatsuH, KobayashiK, SuzueK, KawahataM, et al. (2002) NOD/SCID/γcnull mouse: an excellent recipient mouse model for engraftment of human cells. Blood 100 : 3175–3182.

66. AnDS, PoonB, Ho Tsong FangR, WeijerK, BlomB, et al. (2007) Use of a novel chimeric mouse model with a functionally active human immune system to study human immunodeficiency virus type 1 infection. Clin Vaccine Immunol 14 : 391–396.

67. WeiX, DeckerJM, LiuH, ZhangZ, AraniRB, et al. (2002) Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother 46 : 1896–1905.

68. Chiba-MizutaniT, MiuraH, MatsudaM, MatsudaZ, YokomakuY, et al. (2007) Use of new T-cell-based cell lines expressing two luciferase reporters for accurately evaluating susceptibility to anti-human immunodeficiency virus type 1 drugs. J Clin Microbiol 45 : 477–487.

69. RussellRA, SmithJ, BarrR, BhattacharyyaD, PathakVK (2009) Distinct domains within APOBEC3G and APOBEC3F interact with separate regions of human immunodeficiency virus type 1 Vif. J Virol 83 : 1992–2003.

70. IzumiT, IoK, MatsuiM, ShirakawaK, ShinoharaM, et al. (2010) HIV-1 viral infectivity factor interacts with TP53 to induce G2 cell cycle arrest and positively regulate viral replication. Proc Natl Acad Sci U S A 107 : 20798–20803.

71. SatoK, AokiJ, MisawaN, DaikokuE, SanoK, et al. (2008) Modulation of human immunodeficiency virus type 1 infectivity through incorporation of tetraspanin proteins. J Virol 82 : 1021–1033.

72. SabbahA, ChangTH, HarnackR, FrohlichV, TominagaK, et al. (2009) Activation of innate immune antiviral responses by Nod2. Nat Immunol 10 : 1073–1080.

73. ThompsonJD, HigginsDG, GibsonTJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 : 4673–4680.

74. TamuraK, PetersonD, PetersonN, StecherG, NeiM, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28 : 2731–2739.

75. DarribaD, TaboadaGL, DoalloR, PosadaD (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9 : 772.

76. TamuraK, NeiM (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10 : 512–526.

77. CriscuoloA (2011) morePhyML: improving the phylogenetic tree space exploration with PhyML 3. Mol Phylogenet Evol 61 : 944–948.

78. JohnsonVA, CalvezV, GunthardHF, ParedesR, PillayD, et al. (2011) 2011 update of the drug resistance mutations in HIV-1. Top Antivir Med 19 : 156–164.

79. GuoY, DongL, QiuX, WangY, ZhangB, et al. (2014) Structural basis for hijacking CBF-β and CUL5 E3 ligase complex by HIV-1 Vif. Nature 505 : 229–233.

80. PerelsonAS, EssungerP, CaoY, VesanenM, HurleyA, et al. (1997) Decay characteristics of HIV-1-infected compartments during combination therapy. Nature 387 : 188–191.

81. MarkowitzM, LouieM, HurleyA, SunE, Di MascioM, et al. (2003) A novel antiviral intervention results in more accurate assessment of human immunodeficiency virus type 1 replication dynamics and T-cell decay in vivo. J Virol 77 : 5037–5038.