#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

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


Mutation can produce three outcomes in viruses:
detrimental, neutral, or beneficial. The first one leads to abrogation of virus replication because of error catastrophe, while the last one lets the virus escape from anti-viral immune system or adapt to the host. Human APOBEC3D, APOBEC3F, and APOBEC3G are cellular cytidine deaminases which cause G-to-A mutations in HIV-1 genome. Here we use a humanized mouse model and demonstrate that endogenous APOBEC3F and APOBEC3G induce G-to-A hypermutation in viral genomes and exert strong anti-HIV-1 activity in vivo. We also reveal that endogenous APOBEC3D and/or APOBEC3F induce viral diversification, which can lead to the emergence of a mutated virus that converts its coreceptor usage. Our results suggest that APOBEC3D and APOBEC3F are capable of promoting viral diversification and functional evolution in vivo.


Vyšlo v časopise: APOBEC3D and APOBEC3F Potently Promote HIV-1 Diversification and Evolution in Humanized Mouse Model. PLoS Pathog 10(10): e32767. doi:10.1371/journal.ppat.1004453
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004453

Souhrn

Mutation can produce three outcomes in viruses:
detrimental, neutral, or beneficial. The first one leads to abrogation of virus replication because of error catastrophe, while the last one lets the virus escape from anti-viral immune system or adapt to the host. Human APOBEC3D, APOBEC3F, and APOBEC3G are cellular cytidine deaminases which cause G-to-A mutations in HIV-1 genome. Here we use a humanized mouse model and demonstrate that endogenous APOBEC3F and APOBEC3G induce G-to-A hypermutation in viral genomes and exert strong anti-HIV-1 activity in vivo. We also reveal that endogenous APOBEC3D and/or APOBEC3F induce viral diversification, which can lead to the emergence of a mutated virus that converts its coreceptor usage. Our results suggest that APOBEC3D and APOBEC3F are capable of promoting viral diversification and functional evolution in vivo.


Zdroje

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.

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2014 Číslo 10
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#