Human APOBEC3 Induced Mutation of Human Immunodeficiency Virus Type-1 Contributes to Adaptation and Evolution in Natural Infection

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Cytidine deaminases of the human APOBEC3 gene family act as an intrinsic defense mechanism against infection with HIV-1 and other viruses. The APOBEC3 proteins introduce mutations into the viral genome by inducing enzymatic modification of nucleotide sequences and inhibiting synthesis of cDNA strands from the viral RNA. Viral Vif counters this impediment to the fidelity of HIV-1 replication by targeting the APOBEC3 proteins for degradation. Low-level APOBEC3 activity that outlasts blockade by viral Vif may foster infrequent mutations that provide a source of genetic variation upon which natural selection acts. Here, we defined the APOBEC3 nucleotide contexts of the edited sites by titration of the wild type and non-editing APOBEC3 mutant in cultured cells. We then followed the patterns of G-to-A mutations we identified in viral DNA in cells obtained from ten patients with acute infection. Our deep sequencing analyses demonstrate an association between sub-lethal APOBEC3 editing and HIV-1 diversification. Mutations at APOBEC3 editing contexts that occurred at particular positions within specific known or predicted epitopes could disrupt peptide binding critical for immune control. Our findings reveal a role for human APOBEC3 in HIV-1 sequence diversification that may influence fitness and evolution of beneficial variants and phenotypes in the population.

Vyšlo v časopise: Human APOBEC3 Induced Mutation of Human Immunodeficiency Virus Type-1 Contributes to Adaptation and Evolution in Natural Infection. PLoS Pathog 10(7): e32767. doi:10.1371/journal.ppat.1004281
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004281

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1. 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.

2. ManskyLM, TeminHM (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: 5087–5094.

3. PeetersM, SharpPM (2000) Genetic diversity of HIV-1: the moving target. AIDS 14 Suppl 3: S129–140.

4. SteinhauerDA, DomingoE, HollandJJ (1992) Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. Gene 122: 281–288.

5. HarrisRS, BishopKN, SheehyAM, CraigHM, Petersen-MahrtSK, et al. (2003) DNA deamination mediates innate immunity to retroviral infection. Cell 113: 803–809.

6. 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.

7. SuspeneR, SommerP, HenryM, FerrisS, GuetardD, et al. (2004) APOBEC3G is a single-stranded DNA cytidine deaminase and functions independently of HIV reverse transcriptase. Nucleic Acids Res 32: 2421–2429.

8. 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.

9. Goila-GaurR, StrebelK (2008) HIV-1 Vif, APOBEC, and intrinsic immunity. Retrovirology 5: 51.

10. DesimmieBA, Delviks-FrankenberrryKA, BurdickRC, QiD, IzumiT, et al. (2014) Multiple APOBEC3 restriction factors for HIV-1 and one Vif to rule them all. J Mol Biol 426: 1220–1245.

11. HolmesRK, MalimMH, BishopKN (2007) APOBEC-mediated viral restriction: not simply editing? Trends Biochem Sci 32: 118–128.

12. BishopKN, HolmesRK, SheehyAM, DavidsonNO, ChoSJ, et al. (2004) Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr Biol 14: 1392–1396.

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

14. AriasJF, KoyamaT, KinomotoM, TokunagaK (2012) Retroelements versus APOBEC3 family members: No great escape from the magnificent seven. Front Microbiol 3: 275.

15. ChiuYL, GreeneWC (2008) The APOBEC3 cytidine deaminases: an innate defensive network opposing exogenous retroviruses and endogenous retroelements. Annu Rev Immunol 26: 317–353.

16. JagerS, KimDY, HultquistJF, ShindoK, LaRueRS, et al. (2012) Vif hijacks CBF-beta to degrade APOBEC3G and promote HIV-1 infection. Nature 481: 371–375.

17. MalimMH (2009) APOBEC proteins and intrinsic resistance to HIV-1 infection. Philos Trans R Soc Lond B Biol Sci 364: 675–687.

18. SheehyAM, GaddisNC, MalimMH (2003) The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat Med 9: 1404–1407.

19. YuX, YuY, LiuB, LuoK, KongW, et al. (2003) Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302: 1056–1060.

20. 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.

21. KimEY, BhattacharyaT, KunstmanK, SwantekP, KoningFA, et al. (2010) Human APOBEC3G-mediated editing can promote HIV-1 sequence diversification and accelerate adaptation to selective pressure. J Virol 84: 10402–10405.

22. 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.

23. MulderLC, HarariA, SimonV (2008) Cytidine deamination induced HIV-1 drug resistance. Proc Natl Acad Sci U S A 105: 5501–5506.

24. KeeleBF, GiorgiEE, Salazar-GonzalezJF, DeckerJM, PhamKT, et al. (2008) Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 105: 7552–7557.

25. 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.

26. 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.

27. 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.

28. ArmitageAE, KatzourakisA, de OliveiraT, WelchJJ, BelshawR, et al. (2008) Conserved footprints of APOBEC3G on Hypermutated human immunodeficiency virus type 1 and human endogenous retrovirus HERV-K(HML2) sequences. J Virol 82: 8743–8761.

29. 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.

30. WiegandHL, DoehleBP, BogerdHP, CullenBR (2004) A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins. The EMBO Journal 23: 2451–2458.

31. FischerW, GanusovVV, GiorgiEE, HraberPT, KeeleBF, et al. (2010) Transmission of single HIV-1 genomes and dynamics of early immune escape revealed by ultra-deep sequencing. PLoS One 5: e12303.

32. AcevedoA, BrodskyL, AndinoR (2014) Mutational and fitness landscapes of an RNA virus revealed through population sequencing. Nature 505: 686–690.

33. ArmitageAE, DeforcheK, ChangCH, WeeE, KramerB, et al. (2012) APOBEC3G-induced hypermutation of human immunodeficiency virus type-1 is typically a discrete “all or nothing” phenomenon. PLoS Genet 8: e1002550.

34. LeT, WrightEJ, SmithDM, HeW, CatanoG, et al. (2013) Enhanced CD4+ T-cell recovery with earlier HIV-1 antiretroviral therapy. N Engl J Med 368: 218–230.

35. HarariA, OomsM, MulderLC, SimonV (2009) Polymorphisms and splice variants influence the antiretroviral activity of human APOBEC3H. J Virol 83: 295–303.

36. LiMM, EmermanM (2011) Polymorphism in human APOBEC3H affects a phenotype dominant for subcellular localization and antiviral activity. J Virol 85: 8197–8207.

37. OomsM, BraytonB, LetkoM, MaioSM, PilcherCD, et al. (2013) HIV-1 Vif Adaptation to Human APOBEC3H Haplotypes. Cell Host Microbe 14: 411–421.

38. WangX, AbuduA, SonS, DangY, VentaPJ, et al. (2011) Analysis of human APOBEC3H haplotypes and anti-human immunodeficiency virus type 1 activity. J Virol 85: 3142–3152.

39. ZhenA, DuJ, ZhouX, XiongY, YuXF (2012) Reduced APOBEC3H variant anti-viral activities are associated with altered RNA binding activities. PLoS One 7: e38771.

40. ErikssonN, PachterL, MitsuyaY, RheeSY, WangC, et al. (2008) Viral population estimation using pyrosequencing. PLoS Comput Biol 4: e1000074.

41. AnisimovaM, GascuelO (2006) Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 55: 539–552.

42. Korber B (2000) HIV Signature and Sequence Variation Analysis. Computational Analysis of HIV Molecular Sequences. Allen G. Rodrigo and Gerald HLearn, eds. ed. Dordrecht, Netherlands: Kluwer Academic Publishers. pp. 55–72.

43. KorberB, MuldoonM, TheilerJ, GaoF, GuptaR, et al. (2000) Timing the ancestor of the HIV-1 pandemic strains. Science 288: 1789–1796.

44. LeitnerT, AlbertJ (1999) The molecular clock of HIV-1 unveiled through analysis of a known transmission history. Proc Natl Acad Sci U S A 96: 10752–10757.

45. Maljkovic BerryI, AthreyaG, KothariM, DanielsM, BrunoWJ, et al. (2009) The evolutionary rate dynamically tracks changes in HIV-1 epidemics: application of a simple method for optimizing the evolutionary rate in phylogenetic trees with longitudinal data. Epidemics 1: 230–239.

46. GouldSJ (1970) Dollo on Dollo's law: irreversibility and the status of evolutionary laws. J Hist Biol 3: 189–212.

47. AllenTM, AltfeldM, GeerSC, KalifeET, MooreC, et al. (2005) Selective escape from CD8+ T-cell responses represents a major driving force of human immunodeficiency virus type 1 (HIV-1) sequence diversity and reveals constraints on HIV-1 evolution. J Virol 79: 13239–13249.

48. FerrariG, KorberB, GoonetillekeN, LiuMK, TurnbullEL, et al. (2011) Relationship between functional profile of HIV-1 specific CD8 T cells and epitope variability with the selection of escape mutants in acute HIV-1 infection. PLoS Pathog 7: e1001273.

49. McMichaelAJ, Rowland-JonesSL (2001) Cellular immune responses to HIV. Nature 410: 980–987.

50. PondSL, FrostSD (2005) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21: 2531–2533.

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

52. AraA, LoveRP, ChelicoL (2014) Different Mutagenic Potential of HIV-1 Restriction Factors APOBEC3G and APOBEC3F Is Determined by Distinct Single-Stranded DNA Scanning Mechanisms. PLoS Pathog 10: e1004024.

53. VartanianJP, HenryM, MarchioA, SuspeneR, AynaudMM, et al. (2010) Massive APOBEC3 editing of hepatitis B viral DNA in cirrhosis. PLoS Pathog 6: e1000928.

54. PollomE, DangKK, PotterEL, GorelickRJ, BurchCL, et al. (2013) Comparison of SIV and HIV-1 genomic RNA structures reveals impact of sequence evolution on conserved and non-conserved structural motifs. PLoS Pathog 9: e1003294.

55. MalimMH, EmermanM (2001) HIV-1 sequence variation: drift, shift, and attenuation. Cell 104: 469–472.

56. PhaloraPK, ShererNM, WolinskySM, SwansonCM, MalimMH (2012) HIV-1 Replication and APOBEC3 Antiviral Activity Are Not Regulated by P Bodies. J Virol 86: 11712–11724.

57. MoonsamyPV, WilliamsT, BonellaP, HolcombCL, HoglundBN, et al. (2013) High throughput HLA genotyping using 454 sequencing and the Fluidigm Access Array System for simplified amplicon library preparation. Tissue Antigens 81: 141–149.

58. Foley B LT, Apetrei C, Hahn B, Mizrachi I, Mullins J, Rambaut A, Wolinsky S, and Korber B, editor (2013) HIV Sequence Compendium. Los Alamos, New Mexico: Theoretical Biology and Biophysics Group.

59. ArcherJ, BaillieG, WatsonSJ, KellamP, RambautA, et al. (2012) Analysis of high-depth sequence data for studying viral diversity: a comparison of next generation sequencing platforms using Segminator II. BMC Bioinformatics 13: 47.

60. PearsonWR, LipmanDJ (1988) Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A 85: 2444–2448.

61. EdgarRC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.

62. GuindonS, GascuelO (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704.

63. Kosakovsky PondSL, FrostSD (2005) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22: 1208–1222.

64. DrummondAJ, SuchardMA, XieD, RambautA (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29: 1969–1973.

65. HolcombCL, HoglundB, AndersonMW, BlakeLA, BohmeI, et al. (2011) A multi-site study using high-resolution HLA genotyping by next generation sequencing. Tissue Antigens 77: 206–217.

66. Yusim K, Korber, B. T. M., Brander C, Haynes BF, Koup, R, Moore JP, Walker, BD and Watkins, DI, editor (2009) HIV Molecular Immunology. Los Alamos, New Mexico: Los Alamos National Laboratory, Theoretical Biology and Biophysics.

67. R Development Core Team (2013) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.

68. Dorai-Raj S (2014) binom: Binomial Confidence Intervals For Several Parameterizations. version 1.1-1 ed. http://CRAN.R-project.org/package=binom.