1887

Abstract

It has been estimated that human immunodeficiency virus type 1 originated from the zoonotic transmission of simian immunodeficiency virus (SIV) of chimpanzees, SIVcpz, and that SIVcpz emerged by the recombination of two lineages of SIVs in Old World monkeys (SIVgsn/mon/mus in guenons and SIVrcm in red-capped mangabeys) and SIVcpz Nef is most closely related to SIVrcm Nef. These observations suggest that SIVrcm Nef had an advantage over SIVgsn/mon/mus during the evolution of SIVcpz in chimpanzees, although this advantage remains uncertain. Nef is a multifunctional protein which downregulates CD4 and coreceptor proteins from the surface of infected cells, presumably to limit superinfection. To assess the possibility that SIVrcm Nef was selected by its superior ability to downregulate viral entry receptors in chimpanzees, we compared its ability to down-modulate viral receptor proteins from humans, chimpanzees and red-capped mangabeys with Nef proteins from eight other different strains of SIVs. Surprisingly, the ability of SIVrcm Nef to downregulate CCR5, CCR2B and CXCR6 was comparable to or lower than SIVgsn/mon/mus Nef, indicating that ability to down-modulate chemokine receptors was not the selective pressure. However, SIVrcm Nef significantly downregulates chimpanzee CD4 over SIVgsn/mon/mus Nefs. Our findings suggest the possibility that the selection of SIVrcm Nef by ancestral SIVcpz is due to its superior capacity to down-modulate chimpanzees CD4 rather than coreceptor proteins.

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2015-09-01
2024-04-23
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References

  1. Bailes E., Gao F., Bibollet-Ruche F., Courgnaud V., Peeters M., Marx P.A., Hahn B.H., Sharp P.M. 2003; Hybrid origin of SIV in chimpanzees. Science 300:1713 [View Article][PubMed]
    [Google Scholar]
  2. Beer B.E., Foley B.T., Kuiken C.L., Tooze Z., Goeken R.M., Brown C.R., Hu J., St Claire M., Korber B.T., Hirsch V.M. 2001; Characterization of novel simian immunodeficiency viruses from red-capped mangabeys from Nigeria (SIVrcmNG409 and -NG411). J Virol 75:12014–12027 [View Article][PubMed]
    [Google Scholar]
  3. Berger E.A., Murphy P.M., Farber J.M. 1999; Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu Rev Immunol 17:657–700 [View Article][PubMed]
    [Google Scholar]
  4. Chen Z., Kwon D., Jin Z., Monard S., Telfer P., Jones M.S., Lu C.Y., Aguilar R.F., Ho D.D., Marx P.A. 1998; Natural infection of a homozygous delta24 CCR5 red-capped mangabey with an R2b-tropic simian immunodeficiency virus. J Exp Med 188:2057–2065 [View Article][PubMed]
    [Google Scholar]
  5. Choe H., Farzan M., Sun Y., Sullivan N., Rollins B., Ponath P.D., Wu L., Mackay C.R., LaRosa G., other authors. 1996; The β-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85:1135–1148 [View Article][PubMed]
    [Google Scholar]
  6. Courgnaud V., Salemi M., Pourrut X., Mpoudi-Ngole E., Abela B., Auzel P., Bibollet-Ruche F., Hahn B., Vandamme A.M., other authors. 2002; Characterization of a novel simian immunodeficiency virus with a vpu gene from greater spot-nosed monkeys (Cercopithecus nictitans) provides new insights into simian/human immunodeficiency virus phylogeny. J Virol 76:8298–8309 [View Article][PubMed]
    [Google Scholar]
  7. Courgnaud V., Abela B., Pourrut X., Mpoudi-Ngole E., Loul S., Delaporte E., Peeters M. 2003; Identification of a new simian immunodeficiency virus lineage with a vpu gene present among different cercopithecus monkeys (C. mona C. cephus, and C. nictitans) from Cameroon. J Virol 77:12523–12534 [View Article][PubMed]
    [Google Scholar]
  8. D'Souza G., Waschina S., Pande S., Bohl K., Kaleta C., Kost C. 2014; Less is more: selective advantages can explain the prevalent loss of biosynthetic genes in bacteria. Evolution 68:2559–2570 [View Article][PubMed]
    [Google Scholar]
  9. Deng H., Liu R., Ellmeier W., Choe S., Unutmaz D., Burkhart M., Di Marzio P., Marmon S., Sutton R.E., other authors. 1996; Identification of a major co-receptor for primary isolates of HIV-1. Nature 381:661–666 [View Article][PubMed]
    [Google Scholar]
  10. Diepolder H.M. 2009; New insights into the immunopathogenesis of chronic hepatitis C. Antiviral Res 82:103–109 [View Article][PubMed]
    [Google Scholar]
  11. Dragic T., Litwin V., Allaway G.P., Martin S.R., Huang Y., Nagashima K.A., Cayanan C., Maddon P.J., Koup R.A., other authors. 1996; HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 381:667–673 [View Article][PubMed]
    [Google Scholar]
  12. Fackler O.T., Moris A., Tibroni N., Giese S.I., Glass B., Schwartz O., Kräusslich H.G. 2006; Functional characterization of HIV-1 Nef mutants in the context of viral infection. Virology 351:322–339 [View Article][PubMed]
    [Google Scholar]
  13. Gao F., Bailes E., Robertson D.L., Chen Y., Rodenburg C.M., Michael S.F., Cummins L.B., Arthur L.O., Peeters M., other authors. 1999; Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes . Nature 397:436–441 [View Article][PubMed]
    [Google Scholar]
  14. Glushakova S., Münch J., Carl S., Greenough T.C., Sullivan J.L., Margolis L., Kirchhoff F. 2001; CD4 down-modulation by human immunodeficiency virus type 1 Nef correlates with the efficiency of viral replication and with CD4+T-cell depletion in human lymphoid tissue ex vivo . J Virol 75:10113–10117 [View Article][PubMed]
    [Google Scholar]
  15. Goldsmith M.A., Warmerdam M.T., Atchison R.E., Miller M.D., Greene W.C. 1995; Dissociation of the CD4 downregulation and viral infectivity enhancement functions of human immunodeficiency virus type 1 Nef. J Virol 69:4112–4121[PubMed]
    [Google Scholar]
  16. Grzesiek S., Stahl S.J., Wingfield P.T., Bax A. 1996; The CD4 determinant for downregulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR. Biochemistry 35:10256–10261 [View Article][PubMed]
    [Google Scholar]
  17. Haller C., Müller B., Fritz J.V., Lamas-Murua M., Stolp B., Pujol F.M., Keppler O.T., Fackler O.T. 2014; HIV-1 Nef and Vpu are functionally redundant broad-spectrum modulators of cell surface receptors, including tetraspanins. J Virol 88:14241–14257 [View Article][PubMed]
    [Google Scholar]
  18. Hrecka K., Swigut T., Schindler M., Kirchhoff F., Skowronski J. 2005; Nef proteins from diverse groups of primate lentiviruses downmodulate CXCR4 to inhibit migration to the chemokine stromal derived factor 1. J Virol 79:10650–10659 [View Article][PubMed]
    [Google Scholar]
  19. Hunter E. 1997; Viral entry and receptors. In Retroviruses pp. 71–119 Edited by Coffin J. M., Hughes S. H., Varmus H. E. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  20. Jia B., Serra-Moreno R., Neidermyer W., Rahmberg A., Mackey J., Fofana I.B., Johnson W.E., Westmoreland S., Evans D.T. 2009; Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathog 5:e1000429 [View Article][PubMed]
    [Google Scholar]
  21. Keele B.F., Van Heuverswyn F., Li Y., Bailes E., Takehisa J., Santiago M.L., Bibollet-Ruche F., Chen Y., Wain L.V., other authors. 2006; Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313:523–526 [View Article][PubMed]
    [Google Scholar]
  22. Keppler O.T., Tibroni N., Venzke S., Rauch S., Fackler O.T. 2006; Modulation of specific surface receptors and activation sensitization in primary resting CD4+T lymphocytes by the Nef protein of HIV-1. J Leukoc Biol 79:616–627 [View Article][PubMed]
    [Google Scholar]
  23. Kobayashi T., Ode H., Yoshida T., Sato K., Gee P., Yamamoto S.P., Ebina H., Strebel K., Sato H., Koyanagi Y. 2011; Identification of amino acids in the human tetherin transmembrane domain responsible for HIV-1 Vpu interaction and susceptibility. J Virol 85:932–945 [View Article][PubMed]
    [Google Scholar]
  24. Kobayashi T., Takeuchi J.S., Ren F., Matsuda K., Sato K., Kimura Y., Misawa N., Yoshikawa R., Nakano Y., other authors. 2014; Characterization of red-capped mangabey tetherin: implication for the co-evolution of primates and their lentiviruses. Sci Rep 4:5529 [View Article][PubMed]
    [Google Scholar]
  25. Landi A., Iannucci V., Van Nuffel A.V., Meuwissen P., Verhasselt B. 2011; One protein to rule them all: modulation of cell surface receptors and molecules by HIV Nef. Curr HIV Res 9:496–504 [View Article][PubMed]
    [Google Scholar]
  26. Li Y., Ndjango J.B., Learn G.H., Ramirez M.A., Keele B.F., Bibollet-Ruche F., Liu W., Easlick J.L., Decker J.M., other authors. 2012; Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir. J Virol 86:10776–10791 [View Article][PubMed]
    [Google Scholar]
  27. Lindwasser O.W., Smith W.J., Chaudhuri R., Yang P., Hurley J.H., Bonifacino J.S. 2008; A diacidic motif in human immunodeficiency virus type 1 Nef is a novel determinant of binding to AP-2. J Virol 82:1166–1174 [View Article][PubMed]
    [Google Scholar]
  28. Lu X., Yu H., Liu S.H., Brodsky F.M., Peterlin B.M. 1998; Interactions between HIV1 Nef and vacuolar ATPase facilitate the internalization of CD4. Immunity 8:647–656 [View Article][PubMed]
    [Google Scholar]
  29. Lundquist C.A., Tobiume M., Zhou J., Unutmaz D., Aiken C. 2002; Nef-mediated downregulation of CD4 enhances human immunodeficiency virus type 1 replication in primary T lymphocytes. J Virol 76:4625–4633 [View Article][PubMed]
    [Google Scholar]
  30. Michel N., Allespach I., Venzke S., Fackler O.T., Keppler O.T. 2005; The Nef protein of human immunodeficiency virus establishes superinfection immunity by a dual strategy to downregulate cell-surface CCR5 and CD4. Curr Biol 15:714–723 [View Article][PubMed]
    [Google Scholar]
  31. Moser B., Wolf M., Walz A., Loetscher P. 2004; Chemokines: multiple levels of leukocyte migration control. Trends Immunol 25:75–84 [View Article][PubMed]
    [Google Scholar]
  32. National Research Council 1996 Guide for the Care and Use of Laboratory Animals Washington, DC: National Academies Press;
    [Google Scholar]
  33. Nethe M., Berkhout B., van der Kuyl A.C. 2005; Retroviral superinfection resistance. Retrovirology 2:52 [View Article][PubMed]
    [Google Scholar]
  34. Olivieri K.C., Mukerji J., Gabuzda D. 2011; Nef-mediated enhancement of cellular activation and human immunodeficiency virus type 1 replication in primary T cells is dependent on association with p21-activated kinase 2. Retrovirology 8:64 [View Article][PubMed]
    [Google Scholar]
  35. Olson M.V. 1999; When less is more: gene loss as an engine of evolutionary change. Am J Hum Genet 64:18–23 [View Article][PubMed]
    [Google Scholar]
  36. Pease J.E., Williams T.J. 2006; The attraction of chemokines as a target for specific anti-inflammatory therapy. Br J Pharmacol 147:(Suppl 1)S212–S221 [View Article][PubMed]
    [Google Scholar]
  37. Pizzato M., Helander A., Popova E., Calistri A., Zamborlini A., Palù G., Göttlinger H.G. 2007; Dynamin 2 is required for the enhancement of HIV-1 infectivity by Nef. Proc Natl Acad Sci U S A 104:6812–6817 [View Article][PubMed]
    [Google Scholar]
  38. Preusser A., Briese L., Baur A.S., Willbold D. 2001; Direct in vitro binding of full-length human immunodeficiency virus type 1 Nef protein to CD4 cytoplasmic domain. J Virol 75:3960–3964 [View Article][PubMed]
    [Google Scholar]
  39. Ren X., Park S.Y., Bonifacino J.S., Hurley J.H. 2014; How HIV-1 Nef hijacks the AP-2 clathrin adaptor to downregulate CD4. eLife 3:e01754 [View Article][PubMed]
    [Google Scholar]
  40. Rollins B.J. 1997; Chemokines. Blood 90:909–928[PubMed]
    [Google Scholar]
  41. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425[PubMed]
    [Google Scholar]
  42. Sato K., Aoki J., Misawa N., Daikoku E., Sano K., Tanaka Y., Koyanagi Y. 2008; Modulation of human immunodeficiency virus type 1 infectivity through incorporation of tetraspanin proteins. J Virol 82:1021–1033 [View Article][PubMed]
    [Google Scholar]
  43. Sato K., Yamamoto S.P., Misawa N., Yoshida T., Miyazawa T., Koyanagi Y. 2009; Comparative study on the effect of human BST-2/Tetherin on HIV-1 release in cells of various species. Retrovirology 6:53 [View Article][PubMed]
    [Google Scholar]
  44. Sato K., Misawa N., Fukuhara M., Iwami S., An D.S., Ito M., Koyanagi Y. 2012; Vpu augments the initial burst phase of HIV-1 propagation and downregulates BST2 and CD4 in humanized mice. J Virol 86:5000–5013 [View Article][PubMed]
    [Google Scholar]
  45. Sato K., Misawa N., Iwami S., Satou Y., Matsuoka M., Ishizaka Y., Ito M., Aihara K., An D.S., Koyanagi Y. 2013; HIV-1 Vpr accelerates viral replication during acute infection by exploitation of proliferating CD4+T cells in vivo . PLoS Pathog 9:e1003812 [View Article][PubMed]
    [Google Scholar]
  46. Sato K., Takeuchi J.S., Misawa N., Izumi T., Kobayashi T., Kimura Y., Iwami S., Takaori-Kondo A., Hu W.S., other authors. 2014; APOBEC3D and APOBEC3F potently promote HIV-1 diversification and evolution in humanized mouse model. PLoS Pathog 10:e1004453 [View Article][PubMed]
    [Google Scholar]
  47. Sauter D., Schindler M., Specht A., Landford W.N., Münch J., Kim K.A., Votteler J., Schubert U., Bibollet-Ruche F., other authors. 2009; Tetherin-driven adaptation of Vpu and Nef function and the evolution of pandemic and nonpandemic HIV-1 strains. Cell Host Microbe 6:409–421 [View Article][PubMed]
    [Google Scholar]
  48. Schwartz O., Maréchal V., Le Gall S., Lemonnier F., Heard J.M. 1996; Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat Med 2:338–342 [View Article][PubMed]
    [Google Scholar]
  49. Sharp P.M., Hahn B.H. 2010; The evolution of HIV-1 and the origin of AIDS. Philos Trans R Soc Lond B Biol Sci 365:2487–2494 [View Article][PubMed]
    [Google Scholar]
  50. Sharp P.M., Shaw G.M., Hahn B.H. 2005; Simian immunodeficiency virus infection of chimpanzees. J Virol 79:3891–3902 [View Article][PubMed]
    [Google Scholar]
  51. Stumptner-Cuvelette P., Morchoisne S., Dugast M., Le Gall S., Raposo G., Schwartz O., Benaroch P. 2001; HIV-1 Nef impairs MHC class II antigen presentation and surface expression. Proc Natl Acad Sci U S A 98:12144–12149 [View Article][PubMed]
    [Google Scholar]
  52. Swigut T., Shohdy N., Skowronski J. 2001; Mechanism for down-regulation of CD28 by Nef. EMBO J 20:1593–1604 [View Article][PubMed]
    [Google Scholar]
  53. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
    [Google Scholar]
  54. Traub L.M. 2009; Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat Rev Mol Cell Biol 10:583–596 [View Article][PubMed]
    [Google Scholar]
  55. Trible R.P., Emert-Sedlak L., Smithgall T.E. 2006; HIV-1 Nef selectively activates Src family kinases Hck, Lyn, and c-Src through direct SH3 domain interaction. J Biol Chem 281:27029–27038 [View Article][PubMed]
    [Google Scholar]
  56. Van Heuverswyn F., Li Y., Bailes E., Neel C., Lafay B., Keele B.F., Shaw K.S., Takehisa J., Kraus M.H., other authors. 2007; Genetic diversity and phylogeographic clustering of SIVcpzPtt in wild chimpanzees in Cameroon. Virology 368:155–171 [View Article][PubMed]
    [Google Scholar]
  57. Venzke S., Michel N., Allespach I., Fackler O.T., Keppler O.T. 2006; Expression of Nef downregulates CXCR4, the major coreceptor of human immunodeficiency virus, from the surfaces of target cells and thereby enhances resistance to superinfection. J Virol 80:11141–11152 [View Article][PubMed]
    [Google Scholar]
  58. Vinton C., Klatt N.R., Harris L.D., Briant J.A., Sanders-Beer B.E., Herbert R., Woodward R., Silvestri G., Pandrea I., other authors. 2011; CD4-like immunological function by CD4- T cells in multiple natural hosts of simian immunodeficiency virus. J Virol 85:8702–8708 [View Article][PubMed]
    [Google Scholar]
  59. Yoshida T., Kawano Y., Sato K., Ando Y., Aoki J., Miura Y., Komano J., Tanaka Y., Koyanagi Y. 2008; A CD63 mutant inhibits T-cell tropic human immunodeficiency virus type 1 entry by disrupting CXCR4 trafficking to the plasma membrane. Traffic 9:540–558 [View Article][PubMed]
    [Google Scholar]
  60. Zhang F., Wilson S.J., Landford W.C., Virgen B., Gregory D., Johnson M.C., Munch J., Kirchhoff F., Bieniasz P.D., Hatziioannou T. 2009; Nef proteins from simian immunodeficiency viruses are tetherin antagonists. Cell Host Microbe 6:54–67 [View Article][PubMed]
    [Google Scholar]
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