HIV-2 infects resting CD4+ T cells but not monocyte-derived dendritic cells

Retrovirology

Volumn 12, Issue 1, 2015, Pages

  Chauveau, Lise ^a,b   Puigdomenech, Isabel ^a   Ayinde, Diana ^a   Roesch, Ferdinand ^a,b   Porrot, Fraç oise ^a   Bruni, Daniela ^c   Visseaux, Benoit ^d,e   Descamps, Diane ^d,e   Schwartz, Olivier ^a,f  

^a CNRS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c INSTITUT PASTEUR   (France)

^d UNIVERSITÉ PARIS DIDEROT   (France)

^e BICHAT HOSPITAL   (France)

^f HENRI MONDOR HOSPITAL   (France)

Author keywords

CD4+ lymphocytes; HIV 2; Interferon; Monocyte derived dendritic cells; SAMHD1; Vpx

Indexed keywords

CELL PROTEIN; MYXOVIRUS RESISTANCE PROTEIN A; SAMHD1 PROTEIN; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN; VPX PROTEIN; VPX PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 2;

ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; DISEASE ASSOCIATION; DNA SYNTHESIS; DOWN REGULATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 2 INFECTION; IN VITRO STUDY; INFECTION SENSITIVITY; MONOCYTE DERIVED DENDRITIC CELL; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PSEUDOTYPING; REVERSE TRANSCRIPTION; T LYMPHOCYTE ACTIVATION; VIRION; VIROGENESIS; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS INFECTIVITY; VIRUS RELEASE; VIRUS REPLICATION; CELL CULTURE; HUMAN IMMUNODEFICIENCY VIRUS 2; METABOLISM; PHYSIOLOGY; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; VESICULAR STOMATITIS VIRUS;

CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DENDRITIC CELLS; HIV-2; HUMANS; VIRAL REGULATORY AND ACCESSORY PROTEINS; VIRUS INTERNALIZATION; VIRUS REPLICATION;

EID: 84924280110     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-014-0131-7     Document Type: Article

References (71)

1. Nyamweya S, Hegedus A, Jaye A, Rowland-Jones S, Flanagan KL, Macallan DC. Comparing HIV-1 and HIV-2 infection: lessons for viral immunopathogenesis. Rev Med Virol. 2013;23(4):221-40.
2. Menendez-Arias L, Alvarez M. Antiretroviral therapy and drug resistance in human immunodeficiency virus type 2 infection. Antivir Res. 2014;102:70-86.
3. van der Loeff MF, Larke N, Kaye S, Berry N, Ariyoshi K, Alabi A, et al. Undetectable plasma viral load predicts normal survival in HIV-2-infected people in a West African village. Retrovirology. 2010;7:46.
4. Esbjornsson J, Mansson F, Kvist A, Isberg PE, Nowroozalizadeh S, Biague AJ, et al. Inhibition of HIV-1 disease progression by contemporaneous HIV-2 infection. N Engl J Med. 2012;367(3):224-32.
5. Thiebaut R, Matheron S, Taieb A, Brun-Vezinet F, Chene G, Autran B, immunology group of the ACOHIVc. Long-term nonprogressors and elite controllers in the ANRS CO5 HIV-2 cohort. Aids. 2011;25(6):865-7.
6. MacNeil A, Sarr AD, Sankale JL, Meloni ST, Mboup S, Kanki P. Direct evidence of lower viral replication rates in vivo in human immunodeficiency virus type 2 (HIV-2) infection than in HIV-1 infection. J Virol. 2007;81(10):5325-30.
7. Popper SJ, Sarr AD, Travers KU, Gueye-Ndiaye A, Mboup S, Essex ME, et al. Lower human immunodeficiency virus (HIV) type 2 viral load reflects the difference in pathogenicity of HIV-1 and HIV-2. J Infect Dis. 1999;180(4):1116-21.
8. Gottlieb GS, Hawes SE, Kiviat NB, Sow PS. Differences in proviral DNA load between HIV-1-infected and HIV-2-infected patients. AIDS. 2008;22(11):1379-80.
9. Gueudin M, Damond F, Braun J, Taieb A, Lemee V, Plantier JC, et al. Differences in proviral DNA load between HIV-1- and HIV-2-infected patients. AIDS. 2008;22(2):211-5.
10. Michel P, Balde AT, Roussilhon C, Aribot G, Sarthou JL, Gougeon ML. Reduced immune activation and T cell apoptosis in human immunodeficiency virus type 2 compared with type 1: correlation of T cell apoptosis with beta2 microglobulin concentration and disease evolution. J Infect Dis. 2000;181(1):64-75.
11. Thiebaut R, Charpentier C, Damond F, Taieb A, Antoine R, Capeau J, et al. Association of soluble CD14 and inflammatory biomarkers with HIV-2 disease progression. Clin Infect Dis. 2012;55(10):1417-25.
12. Leligdowicz A, Feldmann J, Jaye A, Cotten M, Dong T, McMichael A, et al. Direct relationship between virus load and systemic immune activation in HIV-2 infection. J Infect Dis. 2010;201(1):114-22.
13. Cavaleiro R, Tendeiro R, Foxall RB, Soares RS, Baptista AP, Gomes P, et al. Monocyte and myeloid dendritic cell activation occurs throughout HIV type 2 infection, an attenuated form of HIV disease. J Infect Dis. 2013;207(11):1730-42.
14. Kanki PJ, Rowland-Jones S. The protective effect of HIV-2 infection: implications for understanding HIV-1 immunity. AIDS (London, England). 2014;28(7):1065-7.
15. Esbjornsson J, Mansson F, Kvist A, Isberg PE, Nowroozalizadeh S, Biague AJ, et al. Effect of HIV-2 infection on HIV-1 disease progression and mortality. AIDS. 2014;28(4):614-5.
16. Rodriguez SK, Sarr AD, MacNeil A, Thakore-Meloni S, Gueye-Ndiaye A, Traore I, et al. Comparison of heterologous neutralizing antibody responses of human immunodeficiency virus type 1 (HIV-1)- and HIV-2-infected Senegalese patients: distinct patterns of breadth and magnitude distinguish HIV-1 and HIV-2 infections. J Virol. 2007;81(10):5331-8.
17. Shi Y, Brandin E, Vincic E, Jansson M, Blaxhult A, Gyllensten K, et al. Evolution of human immunodeficiency virus type 2 coreceptor usage, autologous neutralization, envelope sequence and glycosylation. J Gen Virol. 2005;86(Pt 12):3385-96.
18. Kong R, Li H, Georgiev I, Changela A, Bibollet-Ruche F, Decker JM, et al. Epitope mapping of broadly neutralizing HIV-2 human monoclonal antibodies. J Virol. 2012;86(22):12115-28.
19. Kong R, Li H, Bibollet-Ruche F, Decker JM, Zheng NN, Gottlieb GS, et al. Broad and potent neutralizing antibody responses elicited in natural HIV-2 infection. J Virol. 2012;86(2):947-60.
20. Whittle HC, Ariyoshi K, Rowland-Jones S. HIV-2 and T cell recognition. Curr Opin Immunol. 1998;10(4):382-7.
21. Duvall MG, Jaye A, Dong T, Brenchley JM, Alabi AS, Jeffries DJ, et al. Maintenance of HIV-specific CD4+ T cell help distinguishes HIV-2 from HIV-1 infection. J Immunol. 2006;176(11):6973-81.
22. Duvall MG, Precopio ML, Ambrozak DA, Jaye A, McMichael AJ, Whittle HC, et al. Polyfunctional T cell responses are a hallmark of HIV-2 infection. Eur J Immunol. 2008;38(2):350-63.
23. Cordeil S, Nguyen XN, Berger G, Durand S, Ainouze M, Cimarelli A. Evidence for a different susceptibility of primate lentiviruses to type I interferons. J Virol. 2013;87(5):2587-96.
24. Ylinen LM, Keckesova Z, Wilson SJ, Ranasinghe S, Towers GJ. Differential restriction of human immunodeficiency virus type 2 and simian immunodeficiency virus SIVmac by TRIM5alpha alleles. J Virol. 2005;79(18):11580-7.
25. Onyango CO, Leligdowicz A, Yokoyama M, Sato H, Song H, Nakayama EE, et al. HIV-2 capsids distinguish high and low virus load patients in a West African community cohort. Vaccine. 2010;28 Suppl 2:B60-7.
26. Harrison IP, McKnight A. Cellular entry via an actin and clathrin-dependent route is required for Lv2 restriction of HIV-2. Virology. 2011;415(1):47-55.
27. Marchant D, Neil SJ, Aubin K, Schmitz C, McKnight A. An envelope-determined, pH-independent endocytic route of viral entry determines the susceptibility of human immunodeficiency virus type 1 (HIV-1) and HIV-2 to Lv2 restriction. J Virol. 2005;79(15):9410-8.
28. Neil SJ. The antiviral activities of tetherin. Curr Top Microbiol Immunol. 2013;371:67-104.
29. Hotter D, Sauter D, Kirchhoff F. Emerging role of the host restriction factor tetherin in viral immune sensing. J Mol Biol. 2013;425(24):4956-64.
30. Marno KM, Ogunkolade BW, Pade C, Oliveira NM, O'Sullivan E, McKnight A. Novel restriction factor RNA-associated early-stage anti-viral factor (REAF) inhibits human and simian immunodeficiency viruses. Retrovirology. 2014;11:3.
31. Descours B, Cribier A, Chable-Bessia C, Ayinde D, Rice G, Crow Y, et al. SAMHD1 restricts HIV-1 reverse transcription in quiescent CD4(+) T-cells. Retrovirology. 2012;9:87.
32. Laguette N, Sobhian B, Casartelli N, Ringeard M, Chable-Bessia C, Segeral E, et al. SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature. 2011;474(7353):654-7.
33. Lahouassa H, Daddacha W, Hofmann H, Ayinde D, Logue EC, Dragin L, et al. SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat Immunol. 2012;13(3):223-8.
34. Ayinde D, Casartelli N, Schwartz O. Restricting HIV the SAMHD1 way: through nucleotide starvation. Nat Rev Microbiol. 2012;10(10):675-80.
35. Puigdomenech I, Casartelli N, Porrot F, Schwartz O. SAMHD1 restricts HIV-1 cell-to-cell transmission and limits immune detection in monocyte-derived dendritic cells. J Virol. 2013;87(5):2846-56.
36. Baldauf HM, Pan X, Erikson E, Schmidt S, Daddacha W, Burggraf M, et al. SAMHD1 restricts HIV-1 infection in resting CD4(+) T cells. Nat Med. 2012;18(11):1682-7.
37. Ryoo J, Choi J, Oh C, Kim S, Seo M, Kim SY, et al. The ribonuclease activity of SAMHD1 is required for HIV-1 restriction. Nat Med. 2014;20(8):936-41.
38. Cribier A, Descours B, Valadao AL, Laguette N, Benkirane M. Phosphorylation of SAMHD1 by cyclin A2/CDK1 regulates its restriction activity toward HIV-1. Cell reports. 2013;3(4):1036-43.
39. White TE, Brandariz-Nunez A, Valle-Casuso JC, Amie S, Nguyen LA, Kim B, et al. The retroviral restriction ability of SAMHD1, but not its deoxynucleotide triphosphohydrolase activity, is regulated by phosphorylation. Cell Host Microbe. 2013;13(4):441-51.
40. Welbourn S, Dutta SM, Semmes OJ, Strebel K. Restriction of virus infection but not catalytic dNTPase activity is regulated by phosphorylation of SAMHD1. J Virol. 2013;87(21):11516-24.
41. Yu H, Usmani SM, Borch A, Kramer J, Sturzel CM, Khalid M, et al. The efficiency of Vpx-mediated SAMHD1 antagonism does not correlate with the potency of viral control in HIV-2-infected individuals. Retrovirology. 2013;10:27.
42. Lahaye X, Satoh T, Gentili M, Cerboni S, Conrad C, Hurbain I, et al. The capsids of HIV-1 and HIV-2 determine immune detection of the viral cDNA by the innate sensor cGAS in dendritic cells. Immunity. 2013;39(6):1132-42.
43. Schaller T, Goujon C, Malim MH. AIDS/HIV. HIV interplay with SAMHD1. Science. 2012;335(6074):1313-4.
44. Manel N, Hogstad B, Wang Y, Levy DE, Unutmaz D, Littman DR. A cryptic sensor for HIV-1 activates antiviral innate immunity in dendritic cells. Nature. 2010;467(7312):214-7.
45. Manel N, Littman DR. Hiding in plain sight: how HIV evades innate immune responses. Cell. 2011;147(2):271-4.
46. Cheng X, Ratner L. HIV-2 Vpx protein interacts with interferon regulatory factor 5 (IRF5) and inhibits its function. J Biol Chem. 2014;289(13):9146-57.
47. Marchant D, Neil SJ, McKnight A. Human immunodeficiency virus types 1 and 2 have different replication kinetics in human primary macrophage culture. J Gen Virol. 2006;87(Pt 2):411-8.
48. Royle CM, Graham DR, Sharma S, Fuchs D, Boasso A. HIV-1 and HIV-2 differentially mature plasmacytoid dendritic cells into IFN-producing cells or APCs. J Immunol. 2014;193(7):3538-48.
49. Guyader M, Emerman M, Montagnier L, Peden K. VPX mutants of HIV-2 are infectious in established cell lines but display a severe defect in peripheral blood lymphocytes. EMBO J. 1989;8(4):1169-75.
50. Kawamura M, Sakai H, Adachi A. Human immunodeficiency virus Vpx is required for the early phase of replication in peripheral blood mononuclear cells. Microbiol Immunol. 1994;38(11):871-8.
51. Bergamaschi A, Ayinde D, David A, Le Rouzic E, Morel M, Collin G, et al. The human immunodeficiency virus type 2 Vpx protein usurps the CUL4A-DDB1 DCAF1 ubiquitin ligase to overcome a postentry block in macrophage infection. J Virol. 2009;83(10):4854-60.
52. Duvall MG, Lore K, Blaak H, Ambrozak DA, Adams WC, Santos K, et al. Dendritic cells are less susceptible to human immunodeficiency virus type 2 (HIV-2) infection than to HIV-1 infection. J Virol. 2007;81(24):13486-98.
53. Haller O, Kochs G. Human MxA protein: an interferon-induced dynamin-like GTPase with broad antiviral activity. J Interferon Cytokine Res. 2011;31(1):79-87.
54. Cavrois M, De Noronha C, Greene WC. A sensitive and specific enzyme-based assay detecting HIV-1 virion fusion in primary T lymphocytes. Nat Biotechnol. 2002;20(11):1151-4.
55. Reuter S, Kaumanns P, Buschhorn SB, Dittmar MT. Role of HIV-2 envelope in Lv2-mediated restriction. Virology. 2005;332(1):347-58.
56. Gueudin M, Braun J, Plantier JC, Simon F. HIV-1 and HIV-2 produce different amounts of 2-long terminal repeat circular DNA in vitro. AIDS. 2008;22(18):2543-5.
57. Miller MD, Warmerdam MT, Gaston I, Greene WC, Feinberg MB. The human immunodeficiency virus-1 nef gene product: a positive factor for viral infection and replication in primary lymphocytes and macrophages. J Exp Med. 1994;179(1):101-13.
58. Spina CA, Kwoh TJ, Chowers MY, Guatelli JC, Richman DD. The importance of nef in the induction of human immunodeficiency virus type 1 replication from primary quiescent CD4 lymphocytes. J Exp Med. 1994;179(1):115-23.
59. Amie SM, Daly MB, Noble E, Schinazi RF, Bambara RA, Kim B. Anti-HIV host factor SAMHD1 regulates viral sensitivity to nucleoside reverse transcriptase inhibitors via modulation of cellular deoxyribonucleoside triphosphate (dNTP) levels. J Biol Chem. 2013;288(28):20683-91.
60. Wu L. Cellular and Biochemical Mechanisms of the Retroviral Restriction Factor SAMHD1. ISRN biochemistry 2013 Jul 7. pii: 728392
61. Boyer PL, Clark PK, Hughes SH. HIV-1 and HIV-2 reverse transcriptases: different mechanisms of resistance to nucleoside reverse transcriptase inhibitors. J Virol. 2012;86(10):5885-94.
62. Neil SJ, Aasa-Chapman MM, Clapham PR, Nibbs RJ, McKnight A, Weiss RA. The promiscuous CC chemokine receptor D6 is a functional coreceptor for primary isolates of human immunodeficiency virus type 1 (HIV-1) and HIV-2 on astrocytes. J Virol. 2005;79(15):9618-24.
63. Segura E, Amigorena S. Cross-presentation by human dendritic cell subsets. Immunol Lett. 2013;158(1-2):73-8.
64. Gao D, Wu J, Wu YT, Du F, Aroh C, Yan N, et al. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science. 2013;341(6148):903-6.
65. Calantone N, Wu F, Klase Z, Deleage C, Perkins M, Matsuda K, et al. Tissue myeloid cells in SIV-infected primates acquire viral DNA through phagocytosis of infected T cells. Immunity. 2014;41(3):493-502.
66. Roquebert B, Damond F, Collin G, Matheron S, Peytavin G, Benard A, et al. HIV-2 integrase gene polymorphism and phenotypic susceptibility of HIV-2 clinical isolates to the integrase inhibitors raltegravir and elvitegravir in vitro. J Antimicrob Chemother. 2008;62(5):914-20.
67. Clavel F, Guetard D, Brun-Vezinet F, Chamaret S, Rey MA, Santos-Ferreira MO, et al. Isolation of a new human retrovirus from West African patients with AIDS. Science. 1986;233(4761):343-6.
68. Visseaux B, Hurtado-Nedelec M, Charpentier C, Collin G, Storto A, Matheron S, et al. Molecular determinants of HIV-2 R5-X4 tropism in the V3 loop: development of a new genotypic tool. J Infect Dis. 2012;205(1):111-20.
69. Goujon C, Jarrosson-Wuilleme L, Bernaud J, Rigal D, Darlix JL, Cimarelli A. With a little help from a friend: increasing HIV transduction of monocyte-derived dendritic cells with virion-like particles of SIV(MAC). Gene Ther. 2006;13(12):991-4.
70. Lepelley A, Louis S, Sourisseau M, Law HK, Pothlichet J, Schilte C, et al. Innate sensing of HIV-infected cells. PLoS Pathog. 2011;7(2):e1001284.
71. Avettand-Fenoel V, Damond F, Gueudin M, Matheron S, Mélard A, Collin G, et al. New sensitive one-step real-time duplex PCR method for group A and B HIV-2 RNA load. J Clin Microbiol. 2014;52(8):3017-22.