Key Viral Adaptations Preceding the AIDS Pandemic

Cell Host and Microbe

Volumn 25, Issue 1, 2019, Pages 27-38

  Sauter, Daniel ^a   Kirchhoff, Frank ^a  

^a UNIVERSITY HOSPITAL ULM   (Germany)

Author keywords

adaptation; AIDS; arms race; evolution; HIV; primate lentiviruses; restriction factors; viral zoonoses

Indexed keywords

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ADAPTATION; CHIMPANZEE; CROSS SPECIES TRANSMISSION; GORILLA; HAPLORHINI; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 2; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NONHUMAN; PANDEMIC; PRIORITY JOURNAL; REVIEW; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS TRANSMISSION; ZOONOSIS; ANIMAL; GENETIC RECOMBINATION; GENETICS; GORILLA GORILLA; HOST RANGE; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; INNATE IMMUNITY; PAN TROGLODYTES; PATHOGENICITY; PRIMATE DISEASE; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SPECIES DIFFERENCE; TRANSMISSION; VETERINARY MEDICINE; VIROLOGY; VIRUS REPLICATION; WILD ANIMAL;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANIMALS, WILD; GORILLA GORILLA; HAPLORHINI; HIV-1; HIV-2; HOST SPECIFICITY; HUMANS; IMMUNITY, INNATE; PAN TROGLODYTES; PANDEMICS; PRIMATE DISEASES; RECOMBINATION, GENETIC; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; SPECIES SPECIFICITY; VIRUS REPLICATION; ZOONOSES;

EID: 85058976226     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2018.12.002     Document Type: Review

References (105)

1. Aghokeng, A.F., Liu, W., Bibollet-Ruche, F., Loul, S., Mpoudi-Ngole, E., Laurent, C., Mwenda, J.M., Langat, D.K., Chege, G.K., McClure, H.M., et al. Widely varying SIV prevalence rates in naturally infected primate species from Cameroon. Virology 345 (2006), 174–189.
2. Aghokeng, A.F., Ayouba, A., Mpoudi-Ngole, E., Loul, S., Liegeois, F., Delaporte, E., Peeters, M., Extensive survey on the prevalence and genetic diversity of SIVs in primate bushmeat provides insights into risks for potential new cross-species transmissions. Infect. Genet. Evol. 10 (2010), 386–396.
3. Apetrei, C., Kaur, A., Lerche, N.W., Metzger, M., Pandrea, I., Hardcastle, J., Falkenstein, S., Bohm, R., Koehler, J., Traina-Dorge, V., et al. Molecular epidemiology of simian immunodeficiency virus SIVsm in U.S. Primate Centers unravels the origin of SIVmac and SIVstm. J. Virol. 79 (2005), 8991–9005.
4. Ayouba, A., Akoua-Koffi, C., Calvignac-Spencer, S., Esteban, A., Locatelli, S., Li, H., Li, Y., Hahn, B.H., Delaporte, E., Leendertz, F.H., et al. Evidence for continuing cross-species transmission of SIVsmm to humans: characterization of a new HIV-2 lineage in rural Côte d'Ivoire. AIDS 27 (2013), 2488–2491.
5. Ayouba, A., Njouom, R., Chia, J.E., Ahuka-Mundeke, S., Kfutwah, A., Ngole, E.M., Nerrienet, E., Delaporte, E., Peeters, M., Molecular characterization of a new mosaic simian immunodeficiency virus in a naturally infected tantalus monkey (Chlorocebus tantalus) from Cameroon: a challenge to the virus–host co-evolution of SIVagm in African green monkeys. Infect. Genet. Evol. 30 (2015), 65–73.
6. Bailes, E., Gao, F., Bibollet-Ruche, F., Courgnaud, V., Peeters, M., Marx, P.A., Hahn, B.H., Sharp, P.M., Hybrid origin of SIV in chimpanzees. Science, 300, 2003, 1713.
7. Barre-Sinoussi, F., Chermann, J.C., Rey, F., Nugeyre, M.T., Chamaret, S., Gruest, J., Dauguet, C., Axler-Blin, C., Vezinet-Brun, F., Rouzioux, C., et al. Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science 220 (1983), 868–871.
8. Beaumier, C.M., Harris, L.D., Goldstein, S., Klatt, N.R., Whitted, S., McGinty, J., Apetrei, C., Pandrea, I., Hirsch, V.M., Brenchley, J.M., CD4 downregulation by memory CD4+ T cells in vivo renders African green monkeys resistant to progressive SIVagm infection. Nat. Med. 15 (2009), 879–885.
9. Beer, B.E., Bailes, E., Dapolito, G., Campbell, B.J., Goeken, R.M., Axthelm, M.K., Markham, P.D., Bernard, J., Zagury, D., Franchini, G., et al. Patterns of genomic sequence diversity among their simian immunodeficiency viruses suggest that L'Hoest monkeys (Cercopithecus lhoesti) are a natural lentivirus reservoir. J. Virol. 74 (2000), 3892–3898.
10. Bell, S.M., Bedford, T., Modern-day SIV viral diversity generated by extensive recombination and cross-species transmission. PLoS Pathog., 13, 2017, e1006466.
11. Bertine, M., Charpentier, C., Visseaux, B., Storto, A., Collin, G., Larrouy, L., Damond, F., Matheron, S., Brun-Vézinet, F., Descamps, D., et al. High level of APOBEC3F/3G editing in HIV-2 DNA vif and pol sequences from antiretroviral-naive patients. AIDS 29 (2015), 779–784.
12. Bibollet-Ruche, F., Heigele, A., Keele, B.F., Easlick, J.L., Decker, J.M., Takehisa, J., Learn, G., Sharp, P.M., Hahn, B.H., Kirchhoff, F., Efficient SIVcpz replication in human lymphoid tissue requires viral matrix protein adaptation. J. Clin. Invest. 122 (2012), 1644–1652.
13. Chahroudi, A., Bosinger, S.E., Vanderford, T.H., Paiardini, M., Silvestri, G., Natural SIV hosts: showing AIDS the door. Science 335 (2012), 1188–1193.
14. Chougui, G., Munir-Matloob, S., Matkovic, R., Martin, M.M., Morel, M., Lahouassa, H., Leduc, M., Ramirez, B.C., Etienne, L., Margottin-Goguet, F., HIV-2/SIV viral protein x counteracts HUSH repressor complex. Nat. Microbiol. 3 (2018), 891–897.
15. Clavel, F., Guétard, D., Brun-Vézinet, F., Chamaret, S., Rey, M.A., Santos-Ferreira, M.O., Laurent, A.G., Dauguet, C., Katlama, C., Rouzioux, C., et al. Isolation of a new human retrovirus from West African patients with AIDS. Science 233 (1986), 343–346.
16. Compton, A.A., Emerman, M., Convergence and divergence in the evolution of the APOBEC3G-Vif interaction reveal ancient origins of simian immunodeficiency viruses. PLoS Pathog., 9, 2013, e1003135.
17. Compton, A.A., Hirsch, V.M., Emerman, M., The host restriction factor APOBEC3G and retroviral Vif protein coevolve due to ongoing genetic conflict. Cell Host Microbe 11 (2012), 91–98.
18. Compton, A.A., Malik, H.S., Emerman, M., Host gene evolution traces the evolutionary history of ancient primate lentiviruses. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 368, 2013, 20120496.
19. Daniel, M.D., Letvin, N.L., King, N.W., Kannagi, M., Sehgal, P.K., Hunt, R.D., Kanki, P.J., Essex, M., Desrosiers, R.C., Isolation of T-cell tropic HTLV-III-like retrovirus from macaques. Science 228 (1985), 1201–1204.
20. D'arc, M., Ayouba, A., Esteban, A., Learn, G.H., Boué V., Liegeois, F., Etienne, L., Tagg, N., Leendertz, F.H., Boesch, C., et al. Origin of the HIV-1 group O epidemic in western lowland gorillas. Proc. Natl. Acad. Sci. USA, 112, 2015, E1343.
21. Desimmie, B.A., Delviks-Frankenberrry, K.A., Burdick, R.C., Qi, D., Izumi, T., Pathak, V.K., Multiple APOBEC3 restriction factors for HIV-1 and one Vif to rule them all. J. Mol. Biol. 426 (2014), 1220–1245.
22. Duggal, N.K., Malik, H.S., Emerman, M., The breadth of antiviral activity of Apobec3DE in chimpanzees has been driven by positive selection. J. Virol. 85 (2011), 11361–11371.
23. Etienne, L., Hahn, B.H., Sharp, P.M., Matsen, F.A., Emerman, M., Gene loss and adaptation to hominids underlie the ancient origin of HIV-1. Cell Host Microbe 14 (2013), 85–92.
24. Etienne, L., Bibollet-Ruche, F., Sudmant, P.H., Wu, L.I., Hahn, B.H., Emerman, M., The role of the antiviral APOBEC3 gene family in protecting chimpanzees against lentiviruses from monkeys. PLoS Pathog., 11, 2015, e1005149.
25. Faria, N.R., Rambaut, A., Suchard, M.A., Baele, G., Bedford, T., Ward, M.J., Tatem, A.J., Sousa, J.D., Arinaminpathy, N., Pépin, J., et al. HIV epidemiology. The early spread and epidemic ignition of HIV-1 in human populations. Science 346 (2014), 56–61.
26. Fregoso, O.I., Ahn, J., Wang, C., Mehrens, J., Skowronski, J., Emerman, M., Evolutionary toggling of Vpx/Vpr specificity results in divergent recognition of the restriction factor SAMHD1. PLoS Pathog., 9, 2013, e1003496.
27. Gao, F., Yue, L., White, A.T., Pappas, P.G., Barchue, J., Hanson, A.P., Greene, B.M., Sharp, P.M., Shaw, G.M., Hahn, B.H., Human infection by genetically diverse SIVSM-related HIV-2 in west Africa. Nature 358 (1992), 495–499.
28. Gao, F., Bailes, E., Robertson, D.L., Chen, Y., Rodenburg, C.M., Michael, S.F., Cummins, L.B., Arthur, L.O., Peeters, M., Shaw, G.M., et al. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397 (1999), 436–441.
29. Gautam, R., Carter, A.C., Katz, N., Butler, I.F., Barnes, M., Hasegawa, A., Ratterree, M., Silvestri, G., Marx, P.A., Hirsch, V.M., et al. In vitro characterization of primary SIVsmm isolates belonging to different lineages. In vitro growth on rhesus macaque cells is not predictive for in vivo replication in rhesus macaques. Virology 362 (2007), 257–270.
30. Gifford, R.J., Viral evolution in deep time: lentiviruses and mammals. Trends Genet. 28 (2012), 89–100.
31. Gifford, R.J., Katzourakis, A., Tristem, M., Pybus, O.G., Winters, M., Shafer, R.W., A transitional endogenous lentivirus from the genome of a basal primate and implications for lentivirus evolution. Proc. Natl. Acad. Sci. USA 105 (2008), 20362–20367.
32. Gilbert, C., Maxfield, D.G., Goodman, S.M., Feschotte, C., Parallel germline infiltration of a lentivirus in two Malagasy lemurs. PLoS Genet., 5, 2009, e1000425.
33. de Groot, N.G., Bontrop, R.E., The HIV-1 pandemic: does the selective sweep in chimpanzees mirror humankind's future?. Retrovirology, 10, 2013, 53.
34. Heigele, A., Kmiec, D., Regensburger, K., Langer, S., Peiffer, L., Stürzel, C.M., Sauter, D., Peeters, M., Pizzato, M., Learn, G.H., et al. The potency of nef-mediated SERINC5 antagonism correlates with the prevalence of primate lentiviruses in the wild. Cell Host Microbe 20 (2016), 381–391.
35. Heusinger, E., Deppe, K., Sette, P., Krapp, C., Kmiec, D., Kluge, S.F., Marx, P.A., Apetrei, C., Kirchhoff, F., Sauter, D., Preadaptation of simian immunodeficiency virus SIVsmm facilitated env-mediated counteraction of human tetherin by human immunodeficiency virus Type 2. J. Virol., 92, 2018 e00276-18.
36. Hey, J., The divergence of chimpanzee species and subspecies as revealed in multipopulation isolation-with-migration analyses. Mol. Biol. Evol. 27 (2010), 921–933.
37. Hirsch, V.M., Olmsted, R.A., Murphey-Corb, M., Purcell, R.H., Johnson, P.R., An African primate lentivirus (SIVsm) closely related to HIV-2. Nature 339 (1989), 389–392.
38. Holmes, E.C., On the origin and evolution of the human immunodeficiency virus (HIV). Biol. Rev. Camb. Philos. Soc. 76 (2001), 239–254.
39. Hotter, D., Krabbe, T., Reith, E., Gawanbacht, A., Rahm, N., Ayouba, A., Van Driessche, B., Van Lint, C., Peeters, M., Kirchhoff, F., et al. Primate lentiviruses use at least three alternative strategies to suppress NF-κB-mediated immune activation. PLoS Pathog., 13, 2017, e1006598.
40. Hrecka, K., Hao, C., Gierszewska, M., Swanson, S.K., Kesik-Brodacka, M., Srivastava, S., Florens, L., Washburn, M.P., Skowronski, J., Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474 (2011), 658–661.
41. Iyer, S.S., Bibollet-Ruche, F., Sherrill-Mix, S., Learn, G.H., Plenderleith, L., Smith, A.G., Barbian, H.J., Russell, R.M., Gondim, M.V.P., Bahari, C.Y., et al. Resistance to type 1 interferons is a major determinant of HIV-1 transmission fitness. Proc. Natl. Acad. Sci. USA 114 (2017), E590–E599.
42. Jia, B., Serra-Moreno, R., Neidermyer, W., Rahmberg, A., Mackey, J., Fofana, I.B., Johnson, W.E., Westmoreland, S., Evans, D.T., Species-specific activity of SIV nef and HIV-1 Vpu in overcoming restriction by Tetherin/BST2. PLoS Pathog., 5, 2009, e1000429.
43. Joas, S., Parrish, E.H., Gnanadurai, C.W., Lump, E., Stürzel, C.M., Parrish, N.F., Learn, G.H., Sauermann, U., Neumann, B., Rensing, K.M., et al. Species-specific host factors rather than virus-intrinsic virulence determine primate lentiviral pathogenicity. Nat. Commun., 9, 2018, 1371.
44. Keele, B.F., Van Heuverswyn, F., Li, Y., Bailes, E., Takehisa, J., Santiago, M.L., Bibollet-Ruche, F., Chen, Y., Wain, L.V., Liegeois, F., et al. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313 (2006), 523–526.
45. Keele, B.F., Jones, J.H., Terio, K.A., Estes, J.D., Rudicell, R.S., Wilson, M.L., Li, Y., Learn, G.H., Beasley, T.M., Schumacher-Stankey, J., et al. Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature 460 (2009), 515–519.
46. Kluge, S.F., Sauter, D., Vogl, M., Peeters, M., Li, Y., Bibollet-Ruche, F., Hahn, B.H., Kirchhoff, F., The transmembrane domain of HIV-1 Vpu is sufficient to confer anti-tetherin activity to SIVcpz and SIVgor Vpu proteins: cytoplasmic determinants of Vpu function. Retrovirology, 10, 2013, 32.
47. Kluge, S.F., Mack, K., Iyer, S.S., Pujol, F.M., Heigele, A., Learn, G.H., Usmani, S.M., Sauter, D., Joas, S., Hotter, D., et al. Nef proteins of epidemic HIV-1 group O strains antagonize human tetherin. Cell Host Microbe 16 (2014), 639–650.
48. Kluge, S.F., Sauter, D., Kirchhoff, F., SnapShot: antiviral restriction factors. Cell 163 (2015), 774–774.e1.
49. Kmiec, D., Iyer, S.S., Stürzel, C.M., Sauter, D., Hahn, B.H., Kirchhoff, F., Vpu-mediated counteraction of tetherin is a major determinant of HIV-1 interferon resistance. MBio., 7, 2016 e00934-16.
50. Kobayashi, T., Takeuchi, J.S., Ren, F., Matsuda, K., Sato, K., Kimura, Y., Misawa, N., Yoshikawa, R., Nakano, Y., Yamada, E., et al. Characterization of red-capped mangabey tetherin: implication for the co-evolution of primates and their lentiviruses. Sci. Rep., 4, 2014, 5529.
51. König, R., Zhou, Y., Elleder, D., Diamond, T.L., Bonamy, G.M.C., Irelan, J.T., Chiang, C.-Y., Tu, B.P., De Jesus, P.D., Lilley, C.E., et al. Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell 135 (2008), 49–60.
52. Kratovac, Z., Virgen, C.A., Bibollet-Ruche, F., Hahn, B.H., Bieniasz, P.D., Hatziioannou, T., Primate lentivirus capsid sensitivity to TRIM5 proteins. J. Virol. 82 (2008), 6772–6777.
53. Laguette, N., Sobhian, B., Casartelli, N., Ringeard, M., Chable-Bessia, C., Ségéral, E., Yatim, A., Emiliani, S., Schwartz, O., Benkirane, M., SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474 (2011), 654–657.
54. Laguette, N., Rahm, N., Sobhian, B., Chable-Bessia, C., Münch, J., Snoeck, J., Sauter, D., Switzer, W.M., Heneine, W., Kirchhoff, F., et al. Evolutionary and functional analyses of the interaction between the myeloid restriction factor SAMHD1 and the lentiviral Vpx protein. Cell Host Microbe 11 (2012), 205–217.
55. Le Tortorec, A., Neil, S.J.D., Antagonism to and intracellular sequestration of human tetherin by the human immunodeficiency virus type 2 envelope glycoprotein. J. Virol. 83 (2009), 11966–11978.
56. Leendertz, S.A.J., Locatelli, S., Boesch, C., Kücherer, C., Formenty, P., Liegeois, F., Ayouba, A., Peeters, M., Leendertz, F.H., 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, 2011, 24.
57. Letko, M., Silvestri, G., Hahn, B.H., Bibollet-Ruche, F., Gokcumen, O., Simon, V., Ooms, M., Vif proteins from diverse primate lentiviral lineages use the same binding site in APOBEC3G. J. Virol. 87 (2013), 11861–11871.
58. Lim, E.S., Malik, H.S., Emerman, M., Ancient adaptive evolution of tetherin shaped the functions of Vpu and Nef in human immunodeficiency virus and primate lentiviruses. J. Virol. 84 (2010), 7124–7134.
59. McCarthy, K.R., Kirmaier, A., Autissier, P., Johnson, W.E., Evolutionary and functional analysis of Old World primate TRIM5 reveals the ancient emergence of primate lentiviruses and convergent evolution targeting a conserved capsid interface. PLoS Pathog., 11, 2015, e1005085.
60. Meyerson, N.R., Warren, C.J., Vieira, D.A.S.A., Diaz-Griferro, F., Sawyer, S.L., Species-specific vulnerability of RanBP2 shaped the evolution of SIV as it transmitted in African apes. PLoS Pathog., 14, 2018, e1006906.
61. Mitani, J.C., Watts, D.P., Demographic influences on the hunting behavior of chimpanzees. Am. J. Phys. Anthropol. 109 (1999), 439–454.
62. Nakano, Y., Yamamoto, K., Soper, A., Kumata, R., Aso, H., Misawa, N., Konno, Y., Kimura, I., Nagaoka, S., Juarez-Fernandez, G., et al. Gorilla APOBEC3 restricts SIVcpz and influences lentiviral evolution in great ape cross-species transmissions. BioRxiv, 2018, 362079.
63. Nyamweya, S., Hegedus, A., Jaye, A., Rowland-Jones, S., Flanagan, K.L., Macallan, D.C., Comparing HIV-1 and HIV-2 infection: lessons for viral immunopathogenesis. Rev. Med. Virol. 23 (2013), 221–240.
64. Ocwieja, K.E., Brady, T.L., Ronen, K., Huegel, A., Roth, S.L., Schaller, T., James, L.C., Towers, G.J., Young, J.A.T., Chanda, S.K., et al. HIV integration targeting: a pathway involving Transportin-3 and the nuclear pore protein RanBP2. PLoS Pathog., 7, 2011, e1001313.
65. Olesen, J.S., Jespersen, S., da Silva, Z.J., Rodrigues, A., Erikstrup, C., Aaby, P., Wejse, C., Hønge, B.L., HIV-2 continues to decrease, whereas HIV-1 is stabilizing in Guinea-Bissau. AIDS 32 (2018), 1193–1198.
66. 4+ T cells are associated with limited CCR5 expression. Nat. Med. 17 (2011), 830–836.
67. Palesch, D., Bosinger, S.E., Tharp, G.K., Vanderford, T.H., Paiardini, M., Chahroudi, A., Johnson, Z.P., Kirchhoff, F., Hahn, B.H., Norgren, R.B., et al. Sooty mangabey genome sequence provides insight into AIDS resistance in a natural SIV host. Nature 553 (2018), 77–81.
68. Peeters, M., Courgnaud, V., Abela, B., Auzel, P., Pourrut, X., Bibollet-Ruche, F., Loul, S., Liegeois, F., Butel, C., Koulagna, D., et al. Risk to human health from a plethora of simian immunodeficiency viruses in primate bushmeat. Emerg. Infect. Dis. 8 (2002), 451–457.
69. Pyndiah, N., Telenti, A., Rausell, A., Evolutionary genomics and HIV restriction factors. Curr. Opin. HIV AIDS 10 (2015), 79–83.
70. Sandberg, J.K., Andersson, S.K., Bächle, S.M., Nixon, D.F., Moll, M., HIV-1 Vpu interference with innate cell-mediated immune mechanisms. Curr. HIV Res. 10 (2012), 327–333.
71. Santiago, M.L., Rodenburg, C.M., Kamenya, S., Bibollet-Ruche, F., Gao, F., Bailes, E., Meleth, S., Soong, S.-J., Kilby, J.M., Moldoveanu, Z., et al. SIVcpz in wild chimpanzees. Science, 295, 2002, 465.
72. Santiago, M.L., Range, F., Keele, B.F., Li, Y., Bailes, E., Bibollet-Ruche, F., Fruteau, C., Noë R., Peeters, M., Brookfield, J.F.Y., et al. Simian immunodeficiency virus infection in free-ranging sooty mangabeys (Cercocebus atys atys) from the Taï Forest, Côte d'Ivoire: implications for the origin of epidemic human immunodeficiency virus type 2. J. Virol. 79 (2005), 12515–12527.
73. Sauter, D., Kirchhoff, F., Multilayered and versatile inhibition of cellular antiviral factors by HIV and SIV accessory proteins. Cytokine Growth Factor Rev. 40 (2018), 3–12.
74. Sauter, D., Schindler, M., Specht, A., Landford, W.N., Münch, J., Kim, K.-A., Votteler, J., Schubert, U., Bibollet-Ruche, F., Keele, B.F., et al. Tetherin-driven adaptation of Vpu and Nef function and the evolution of pandemic and nonpandemic HIV-1 strains. Cell Host Microbe 6 (2009), 409–421.
75. Sauter, D., Hué S., Petit, S.J., Plantier, J.-C., Towers, G.J., Kirchhoff, F., Gupta, R.K., HIV-1 Group P is unable to antagonize human tetherin by Vpu, Env or Nef. Retrovirology, 8, 2011, 103.
76. Sauter, D., Unterweger, D., Vogl, M., Usmani, S.M., Heigele, A., Kluge, S.F., Hermkes, E., Moll, M., Barker, E., Peeters, M., et al. Human tetherin exerts strong selection pressure on the HIV-1 group N Vpu protein. PLoS Pathog., 8, 2012, e1003093.
77. Sauter, D., Hotter, D., Van Driessche, B., Stürzel, C.M., Kluge, S.F., Wildum, S., Yu, H., Baumann, B., Wirth, T., Plantier, J.-C., et al. Differential regulation of NF-κB-mediated proviral and antiviral host gene expression by primate lentiviral Nef and Vpu proteins. Cell Rep. 10 (2015), 586–599.
78. Schindler, M., Münch, J., Kutsch, O., Li, H., Santiago, M.L., Bibollet-Ruche, F., Müller-Trutwin, M.C., Novembre, F.J., Peeters, M., Courgnaud, V., et al. Nef-mediated suppression of T cell activation was lost in a lentiviral lineage that gave rise to HIV-1. Cell 125 (2006), 1055–1067.
79. Schmidt, F., Liegeois, F., Greenwood, E.J.D., LeBreton, M., Lester, J., Deleplancque, L., Peeters, M., Aghokeng, A., Tamoufe, U., Diffo, J.L.D., et al. Phyloepidemiological analysis reveals that viral divergence led to the paucity of simian immunodeficiency virus SIVmus/gsn/mon infections in wild populations. J. Virol., 91, 2017 e01884-16.
80. Schmitt, K., Mohan Kumar, D., Curlin, J., Remling-Mulder, L., Stenglein, M., O'Connor, S., Marx, P., Akkina, R., Modeling the evolution of SIV sooty mangabey progenitor virus towards HIV-2 using humanized mice. Virology 510 (2017), 175–184.
81. Sharp, P.M., Hahn, B.H., Origins of HIV and the AIDS pandemic. Cold Spring Harb. Perspect. Med., 1, 2011, a006841.
82. Sharp, P.M., Bailes, E., Stevenson, M., Emerman, M., Hahn, B.H., Gene acquisition in HIV and SIV. Nature 383 (1996), 586–587.
83. Sharp, P.M., Bailes, E., Gao, F., Beer, B.E., Hirsch, V.M., Hahn, B.H., Origins and evolution of AIDS viruses: estimating the time-scale. Biochem. Soc. Trans. 28 (2000), 275–282.
84. Sheehy, A.M., Gaddis, N.C., Choi, J.D., Malim, M.H., Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418 (2002), 646–650.
85. Simon, V., Bloch, N., Landau, N.R., Intrinsic host restrictions to HIV-1 and mechanisms of viral escape. Nat. Immunol. 16 (2015), 546–553.
86. Stremlau, M., Owens, C.M., Perron, M.J., Kiessling, M., Autissier, P., Sodroski, J., The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427 (2004), 848–853.
87. Takehisa, J., Kraus, M.H., Decker, J.M., Li, Y., Keele, B.F., Bibollet-Ruche, F., Zammit, K.P., Weng, Z., Santiago, M.L., Kamenya, S., et al. Generation of infectious molecular clones of simian immunodeficiency virus from fecal consensus sequences of wild chimpanzees. J. Virol. 81 (2007), 7463–7475.
88. Takehisa, J., Kraus, M.H., Ayouba, A., Bailes, E., Van Heuverswyn, F., Decker, J.M., Li, Y., Rudicell, R.S., Learn, G.H., Neel, C., et al. Origin and biology of simian immunodeficiency virus in wild-living western gorillas. J. Virol. 83 (2009), 1635–1648.
89. Takeuchi, J.S., Perche, B., Migraine, J., Mercier-Delarue, S., Ponscarme, D., Simon, F., Clavel, F., Labrosse, B., High level of susceptibility to human TRIM5α conferred by HIV-2 capsid sequences. Retrovirology, 10, 2013, 50.
90. Takeuchi, J.S., Ren, F., Yoshikawa, R., Yamada, E., Nakano, Y., Kobayashi, T., Matsuda, K., Izumi, T., Misawa, N., Shintaku, Y., et al. Coevolutionary dynamics between tribe Cercopithecini tetherins and their lentiviruses. Sci. Rep., 5, 2015, 16021.
91. Taylor, B.S., Sobieszczyk, M.E., McCutchan, F.E., Hammer, S.M., The challenge of HIV-1 subtype diversity. N. Engl. J. Med. 358 (2008), 1590–1602.
92. Venner, C.M., Nankya, I., Kyeyune, F., Demers, K., Kwok, C., Chen, P.-L., Rwambuya, S., Munjoma, M., Chipato, T., Byamugisha, J., et al. Infecting HIV-1 subtype predicts disease progression in women of sub-Saharan Africa. EBioMedicine 13 (2016), 305–314.
93. Vigan, R., Neil, S.J.D., Determinants of tetherin antagonism in the transmembrane domain of the human immunodeficiency virus type 1 Vpu protein. J. Virol. 84 (2010), 12958–12970.
94. Visseaux, B., Damond, F., Matheron, S., Descamps, D., Charpentier, C., Hiv-2 molecular epidemiology. Infect. Genet. Evol. 46 (2016), 233–240.
95. Wain, L.V., Bailes, E., Bibollet-Ruche, F., Decker, J.M., Keele, B.F., Van Heuverswyn, F., Li, Y., Takehisa, J., Ngole, E.M., Shaw, G.M., et al. Adaptation of HIV-1 to its human host. Mol. Biol. Evol. 24 (2007), 1853–1860.
96. Wertheim, J.O., Worobey, M., Dating the age of the SIV lineages that gave rise to HIV-1 and HIV-2. PLoS Comput. Biol., 5, 2009, e1000377.
97. Wooley, D.P., Smith, R.A., Czajak, S., Desrosiers, R.C., Direct demonstration of retroviral recombination in a rhesus monkey. J. Virol. 71 (1997), 9650–9653.
98. Worobey, M., Gemmel, M., Teuwen, D.E., Haselkorn, T., Kunstman, K., Bunce, M., Muyembe, J.J., Kabongo, J.-M.M., Kalengayi, R.M., Van Marck, E., et al. Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960. Nature 455 (2008), 661–664.
99. Worobey, M., Telfer, P., Souquière, S., Hunter, M., Coleman, C.A., Metzger, M.J., Reed, P., Makuwa, M., Hearn, G., Honarvar, S., et al. Island biogeography reveals the deep history of SIV. Science, 329, 2010, 1487.
100. Yamada, E., Nakaoka, S., Klein, L., Reith, E., Langer, S., Hopfensperger, K., Iwami, S., Schreiber, G., Kirchhoff, F., Koyanagi, Y., et al. Human-Specific Adaptations in Vpu Conferring Anti-tetherin Activity Are Critical for Efficient Early HIV-1 Replication in vivo. Cell Host Microbe 23 (2018), 110–120.e7.
101. Yang, S.J., Lopez, L.A., Exline, C.M., Haworth, K.G., Cannon, P.M., Lack of adaptation to human tetherin in HIV-1 group O and P. Retrovirology, 8, 2011, 78.
102. Ylinen, L.M.J., Keckesova, Z., Wilson, S.J., Ranasinghe, S., Towers, G.J., Differential restriction of human immunodeficiency virus Type 2 and simian immunodeficiency virus SIVmac by TRIM5α alleles. J. Virol. 79 (2005), 11580–11587.
103. Zhang, F., Wilson, S.J., Landford, W.C., Virgen, B., Gregory, D., Johnson, M.C., Munch, J., Kirchhoff, F., Bieniasz, P.D., Hatziioannou, T., Nef proteins from simian immunodeficiency viruses are tetherin antagonists. Cell Host Microbe 6 (2009), 54–67.
104. Zhang, Z., Gu, Q., de Manuel Montero, M., Bravo, I.G., Marques-Bonet, T., Häussinger, D., Münk, C., Stably expressed APOBEC3H forms a barrier for cross-species transmission of simian immunodeficiency virus of chimpanzee to humans. PLoS Pathog., 13, 2017, e1006746.
105. Zhou, H., Xu, M., Huang, Q., Gates, A.T., Zhang, X.D., Castle, J.C., Stec, E., Ferrer, M., Strulovici, B., Hazuda, D.J., et al. Genome-scale RNAi screen for host factors required for HIV replication. Cell Host Microbe 4 (2008), 495–504.