The Role of the Antiviral APOBEC3 Gene Family in Protecting Chimpanzees against Lentiviruses from Monkeys

English version České info

Many human pathogens are of zoonotic origin, meaning they originated in animals. This includes HIV-1, the cause of the human AIDS pandemic, which is the result of cross-species transmissions of lentiviruses from chimpanzees and gorillas. However, little is known about the host factors that provide natural protection against viral emergence in a new species. Chimpanzees, which are humans’ closest relatives, harbor only a single lentiviral lineage, despite their frequent exposure to lentiviruses that infect monkeys on which they prey. Here, we investigate the capacity of the accessory protein Vif from different primate lentiviruses to antagonize the APOBEC3 antiviral gene family found in chimpanzees. We found that the Vif protein from most monkey lentiviruses was not able to antagonize chimpanzee APOBEC3G. Furthermore, other APOBEC3 proteins from chimpanzees were also resistant to Vif antagonism. Finally, we showed that, despite polymorphism in the APOBEC3 genes, common chimpanzee and bonobo populations are uniformly resistant to monkey lentiviral Vif antagonism. Our results are consistent with the hypothesis that the host APOBEC3 antiviral proteins protect chimpanzees against many HIV-related viruses commonly found in monkeys.

Vyšlo v časopise: The Role of the Antiviral APOBEC3 Gene Family in Protecting Chimpanzees against Lentiviruses from Monkeys. PLoS Pathog 11(9): e32767. doi:10.1371/journal.ppat.1005149
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1005149

Souhrn

Zdroje

1. Locatelli S, Peeters M (2012) Cross-species transmission of simian retroviruses: how and why they could lead to the emergence of new diseases in the human population. Aids 26: 659–673. doi: 10.1097/QAD.0b013e328350fb68 22441170

2. Sharp PM, Hahn BH (2011) Origins of HIV and the AIDS Pandemic. Cold Spring Harb Perspect Med 1: a006841. doi: 10.1101/cshperspect.a006841 22229120

3. Bailes E, Gao F, Bibollet-Ruche F, Courgnaud V, Peeters M, et al. (2003) Hybrid origin of SIV in chimpanzees. Science 300: 1713. 12805540

4. Etienne L, Hahn BH, Sharp PM, Matsen FA, Emerman M (2013) Gene loss and adaptation to hominids underlie the ancient origin of HIV-1. Cell Host Microbe 14: 85–92. doi: 10.1016/j.chom.2013.06.002 23870316

5. Li Y, Ndjango JB, Learn GH, Ramirez MA, Keele BF, et al. (2012) Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir. J Virol 86: 10776–10791. doi: 10.1128/JVI.01498-12 22837215

6. Gogarten JF, Akoua-Koffi C, Calvignac-Spencer S, Leendertz SA, Weiss S, et al. (2014) The ecology of primate retroviruses—an assessment of 12 years of retroviral studies in the Tai national park area, Cote dIvoire. Virology 460–461: 147–153. doi: 10.1016/j.virol.2014.05.012 25010280

7. Leendertz SA, Locatelli S, Boesch C, Kucherer C, Formenty P, et al. (2011) No evidence for transmission of SIVwrc from western red colobus monkeys (Piliocolobus badius badius) to wild West African chimpanzees (Pan troglodytes verus) despite high exposure through hunting. BMC Microbiol 11: 24. doi: 10.1186/1471-2180-11-24 21284842

8. Leendertz FH, Junglen S, Boesch C, Formenty P, Couacy-Hymann E, et al. (2004) High variety of different simian T-cell leukemia virus type 1 strains in chimpanzees (Pan troglodytes verus) of the Tai National Park, Cote d'Ivoire. J Virol 78: 4352–4356. 15047848

9. Leendertz FH, Zirkel F, Couacy-Hymann E, Ellerbrok H, Morozov VA, et al. (2008) Interspecies transmission of simian foamy virus in a natural predator-prey system. J Virol 82: 7741–7744. doi: 10.1128/JVI.00549-08 18508895

10. Calattini S, Nerrienet E, Mauclere P, Georges-Courbot MC, Saib A, et al. (2006) Detection and molecular characterization of foamy viruses in Central African chimpanzees of the Pan troglodytes troglodytes and Pan troglodytes vellerosus subspecies. J Med Primatol 35: 59–66. 16556292

11. D'Arc M, Ayouba A, Esteban A, Learn GH, Boue V, et al. (2015) Origin of the HIV-1 group O epidemic in western lowland gorillas. Proc Natl Acad Sci U S A 112: E1343–1352. doi: 10.1073/pnas.1502022112 25733890

12. Duggal NK, Emerman M (2012) Evolutionary conflicts between viruses and restriction factors shape immunity. Nat Rev Immunol 12: 687–695. doi: 10.1038/nri3295 22976433

13. Malim MH, Bieniasz PD (2012) HIV Restriction Factors and Mechanisms of Evasion. Cold Spring Harb Perspect Med 2: a006940. doi: 10.1101/cshperspect.a006940 22553496

14. Hatziioannou T, Princiotta M, Piatak M Jr., Yuan F, Zhang F, et al. (2006) Generation of simian-tropic HIV-1 by restriction factor evasion. Science 314: 95. 17023652

15. Kamada K, Igarashi T, Martin MA, Khamsri B, Hatcho K, et al. (2006) Generation of HIV-1 derivatives that productively infect macaque monkey lymphoid cells. Proc Natl Acad Sci U S A 103: 16959–16964. 17065315

16. Krupp A, McCarthy KR, Ooms M, Letko M, Morgan JS, et al. (2013) APOBEC3G polymorphism as a selective barrier to cross-species transmission and emergence of pathogenic SIV and AIDS in a primate host. PLoS Pathog 9: e1003641. doi: 10.1371/journal.ppat.1003641 24098115

17. Compton AA, Hirsch VM, Emerman M (2012) The host restriction factor APOBEC3G and retroviral Vif protein coevolve due to ongoing genetic conflict. Cell Host Microbe 11: 91–98. doi: 10.1016/j.chom.2011.11.010 22264516

18. Feng Y, Baig TT, Love RP, Chelico L (2014) Suppression of APOBEC3-mediated restriction of HIV-1 by Vif. Front Microbiol 5: 450. doi: 10.3389/fmicb.2014.00450 25206352

19. Desimmie BA, Delviks-Frankenberrry KA, Burdick RC, Qi D, Izumi T, et al. (2014) Multiple APOBEC3 restriction factors for HIV-1 and one Vif to rule them all. J Mol Biol 426: 1220–1245. doi: 10.1016/j.jmb.2013.10.033 24189052

20. Compton AA, Emerman M (2013) Convergence and Divergence in the Evolution of the APOBEC3G-Vif Interaction Reveal Ancient Origins of Simian Immunodeficiency Viruses. PLoS Pathog 9: e1003135. doi: 10.1371/journal.ppat.1003135 23359341

21. IUCN (2014) IUCN Red List of Threatened Species. Version 2014.2.

22. Li MM, Wu LI, Emerman M (2010) The range of human APOBEC3H sensitivity to lentiviral Vif proteins. J Virol 84: 88–95. doi: 10.1128/JVI.01344-09 19828612

23. Jin MJ, Rogers J, Phillips-Conroy JE, Allan JS, Desrosiers RC, et al. (1994) Infection of a yellow baboon with simian immunodeficiency virus from African green monkeys: evidence for cross-species transmission in the wild. J Virol 68: 8454–8460. 7966642

24. Bibollet-Ruche F, Galat-Luong A, Cuny G, Sarni-Manchado P, Galat G, et al. (1996) Simian immunodeficiency virus infection in a patas monkey (Erythrocebus patas): evidence for cross-species transmission from African green monkeys (Cercopithecus aethiops sabaeus) in the wild. J Gen Virol 77 (Pt 4): 773–781. 8627266

25. Duggal NK, Malik HS, Emerman M (2011) The breadth of antiviral activity of Apobec3DE in chimpanzees has been driven by positive selection. J Virol 85: 11361–11371. doi: 10.1128/JVI.05046-11 21835794

26. Decker JM, Zammit KP, Easlick JL, Santiago ML, Bonenberger D, et al. (2009) Effective activation alleviates the replication block of CCR5-tropic HIV-1 in chimpanzee CD4+ lymphocytes. Virology 394: 109–118. doi: 10.1016/j.virol.2009.08.027 19748647

27. Refsland EW, Stenglein MD, Shindo K, Albin JS, Brown WL, 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. doi: 10.1093/nar/gkq174 20308164

28. Hultquist JF, Lengyel JA, Refsland EW, LaRue RS, Lackey L, 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. doi: 10.1128/JVI.05238-11 21835787

29. Gillick K, Pollpeter D, Phalora P, Kim EY, Wolinsky SM, 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. doi: 10.1128/JVI.02587-12 23152537

30. Rose PP, Korber BT (2000) Detecting hypermutations in viral sequences with an emphasis on G—> A hypermutation. Bioinformatics 16: 400–401. 10869039

31. Matsen FAt, Small CT, Soliven K, Engel GA, Feeroz MM, et al. (2014) A novel bayesian method for detection of APOBEC3-mediated hypermutation and its application to zoonotic transmission of simian foamy viruses. PLoS Comput Biol 10: e1003493. doi: 10.1371/journal.pcbi.1003493 24586139

32. Refsland EW, Hultquist JF, Harris RS (2012) Endogenous origins of HIV-1 G-to-A hypermutation and restriction in the nonpermissive T cell line CEM2n. PLoS Pathog 8: e1002800. doi: 10.1371/journal.ppat.1002800 22807680

33. 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: 249–259. doi: 10.1016/j.chom.2008.07.005 18779051

34. Prado-Martinez J, Sudmant PH, Kidd JM, Li H, Kelley JL, et al. (2013) Great ape genetic diversity and population history. Nature 499: 471–475. doi: 10.1038/nature12228 23823723

35. Duggal NK, Fu W, Akey JM, Emerman M (2013) Identification and antiviral activity of common polymorphisms in the APOBEC3 locus in human populations. Virology 443: 329–337. doi: 10.1016/j.virol.2013.05.016 23755966

36. Aydin H, Taylor MW, Lee JE (2014) Structure-guided analysis of the human APOBEC3-HIV restrictome. Structure 22: 668–684. doi: 10.1016/j.str.2014.02.011 24657093

37. Mamede JI, Sitbon M, Battini JL, Courgnaud V (2013) Heterogeneous susceptibility of circulating SIV isolate capsids to HIV-interacting factors. Retrovirology 10: 77. doi: 10.1186/1742-4690-10-77 23883001

38. Sauter D, Specht A, Kirchhoff F (2010) Tetherin: holding on and letting go. Cell 141: 392–398. doi: 10.1016/j.cell.2010.04.022 20434978

39. Han K, Lou DI, Sawyer SL (2011) Identification of a genomic reservoir for new TRIM genes in primate genomes. PLoS Genet 7: e1002388. doi: 10.1371/journal.pgen.1002388 22144910

40. Diamond MS, Farzan M (2013) The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat Rev Immunol 13: 46–57. doi: 10.1038/nri3344 23237964

41. Sato K, Takeuchi JS, Misawa N, Izumi T, Kobayashi T, et al. (2014) APOBEC3D and APOBEC3F potently promote HIV-1 diversification and evolution in humanized mouse model. PLoS Pathog 10: e1004453. doi: 10.1371/journal.ppat.1004453 25330146

42. Smith JL, Izumi T, Borbet TC, Hagedorn AN, Pathak VK (2014) HIV-1 and HIV-2 Vif interact with human APOBEC3 proteins using completely different determinants. J Virol 88: 9893–9908. doi: 10.1128/JVI.01318-14 24942576

43. Russell RA, Pathak VK (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. 17522216

44. Santiago ML, Range F, Keele BF, Li Y, Bailes E, et al. (2005) Simian immunodeficiency virus infection in free-ranging sooty mangabeys (Cercocebus atys atys) from the Tai Forest, Cote d'Ivoire: implications for the origin of epidemic human immunodeficiency virus type 2. J Virol 79: 12515–12527. 16160179

45. Ayouba A, Akoua-Koffi C, Calvignac-Spencer S, Esteban A, Locatelli S, et al. (2013) Evidence for continuing cross-species transmission of SIVsmm to humans: characterization of a new HIV-2 lineage in rural Cote d'Ivoire. AIDS 27: 2488–2491. doi: 10.1097/01.aids.0000432443.22684.50 23939239

46. Gifford RJ (2012) Viral evolution in deep time: lentiviruses and mammals. Trends Genet 28: 89–100. doi: 10.1016/j.tig.2011.11.003 22197521

47. Compton AA, Malik HS, Emerman M (2013) Host gene evolution traces the evolutionary history of ancient primate lentiviruses. Philos Trans R Soc Lond B Biol Sci 368: 20120496. doi: 10.1098/rstb.2012.0496 23938749

48. Harari A, Ooms M, Mulder LC, Simon V (2009) Polymorphisms and splice variants influence the antiretroviral activity of human APOBEC3H. J Virol 83: 295–303. doi: 10.1128/JVI.01665-08 18945781

49. Neel C, Etienne L, Li Y, Takehisa J, Rudicell RS, et al. (2010) Molecular epidemiology of simian immunodeficiency virus infection in wild-living gorillas. J Virol 84: 1464–1476. doi: 10.1128/JVI.02129-09 19906908

50. OhAinle M, Kerns JA, Malik HS, Emerman M (2006) Adaptive evolution and antiviral activity of the conserved mammalian cytidine deaminase APOBEC3H. J Virol 80: 3853–3862. 16571802

51. Sawyer SL, Emerman M, Malik HS (2004) Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2: E275. 15269786

52. de Groot NG, Heijmans CM, Zoet YM, de Ru AH, Verreck FA, et al. (2010) AIDS-protective HLA-B*27/B*57 and chimpanzee MHC class I molecules target analogous conserved areas of HIV-1/SIVcpz. Proc Natl Acad Sci U S A 107: 15175–15180. doi: 10.1073/pnas.1009136107 20696916

53. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

54. Bradley RK, Roberts A, Smoot M, Juvekar S, Do J, et al. (2009) Fast statistical alignment. PLoS Comput Biol 5: e1000392. doi: 10.1371/journal.pcbi.1000392 19478997

55. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704. 14530136

56. Letko M, Silvestri G, Hahn BH, Bibollet-Ruche F, Gokcumen O, et al. (2013) Vif proteins from diverse primate lentiviral lineages use the same binding site in APOBEC3G. J Virol 87: 11861–11871. doi: 10.1128/JVI.01944-13 23986590