SAMHD1 restricts HIV-1 cell-to-cell transmission and limits immune detection in monocyte-derived dendritic cells

Journal of Virology

Volumn 87, Issue 5, 2013, Pages 2846-2856

  Puigdomènech, Isabel ^a   Casartelli, Nicoletta ^a   Porrot, Françoise ^a   Schwartz, Olivier ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; INTERFERON; MYXOVIRUS RESISTANCE PROTEIN A; SAMHD1 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VPX PROTEIN;

ARTICLE; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INNATE IMMUNITY; MONOCYTE DERIVED DENDRITIC CELL; MXA GENE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; VIRUS CELL INTERACTION; VIRUS TRANSMISSION;

CELLS, CULTURED; COCULTURE TECHNIQUES; DENDRITIC CELLS; GTP-BINDING PROTEINS; HIV-1; HUMANS; INTERFERON TYPE I; MONOMERIC GTP-BINDING PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; T-LYMPHOCYTES; VIRAL REGULATORY AND ACCESSORY PROTEINS; VIRUS REPLICATION;

EID: 84874716238     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02514-12     Document Type: Article

References (60)

1. Hughes R, Towers G, Noursadeghi M. 2012. Innate immune interferon responses to human immunodeficiency virus-1 infection. Rev. Med. Virol. 22:257-266.
2. Neil SJ, Zang T, Bieniasz PD. 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425-430.
3. Sheehy AM, Gaddis NC, Choi JD, Malim MH. 2002. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418:646-650.
4. Ayinde D, Casartelli N, Schwartz O. 2012. Restricting HIV the SAMHD1 way: through nucleotide starvation. Nat. Rev. Microbiol. 10:675-680.
5. Hrecka K, Hao C, Gierszewska M, Swanson SK, Kesik-Brodacka M, Srivastava S, Florens L, Washburn MP, Skowronski J. 2011. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474:658-661.
6. Kaushik R, Zhu X, Stranska R, Wu Y, Stevenson M. 2009. A cellular restriction dictates the permissivity of nondividing monocytes/ macrophages to lentivirus and gammaretrovirus infection. Cell Host Microbe 6:68-80.
7. Laguette N, Sobhian B, Casartelli N, Ringeard M, Chable-Bessia C, Segeral E, Yatim A, Emiliani S, Schwartz O, Benkirane M. 2011. SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474:654-657.
8. Lim ES, Fregoso OI, McCoy CO, Matsen FA, Malik HS, Emerman M. 2012. The ability of primate lentiviruses to degrade the monocyte restriction factorSAMHD1preceded the birth of the viral accessory protein Vpx. Cell Host Microbe 11:194 -204.
9. Sharova N, Wu Y, Zhu X, Stranska R, Kaushik R, Sharkey M, Stevenson M. 2008. Primate lentiviral Vpx commandeers DDB1 to counteract a macrophage restriction. PLoS Pathog. 4:e1000057. doi:10.1371/journal .ppat.1000057.
10. Brandariz-Nunez A, Valle-Casuso JC, White TE, Laguette N, Benkirane M, Brojatsch J, Diaz-Griffero F. 2012. Role of SAMHD1 nuclear localization in restriction of HIV-1 and SIVmac. Retrovirology 9:49. doi:10 .1186/1742-4690-9-49.
11. Lahouassa H, Daddacha W, Hofmann H, Ayinde D, Logue EC, Dragin L, Bloch N, Maudet C, Bertrand M, Gramberg T, Pancino G, Priet S, Canard B, Laguette N, Benkirane M, Transy C, Landau NR, Kim B, Margottin-Goguet F. 2012. SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat. Immunol. 13:223-228.
12. Baldauf HM, Pan X, Erikson E, Schmidt S, Daddacha W, Burggraf M, Schenkova K, Ambiel I, Wabnitz G, Gramberg T, Panitz S, Flory E, Landau NR, Sertel S, Rutsch F, Lasitschka F, Kim B, Konig R, Fackler OT, Keppler OT. 2012. SAMHD1 restricts HIV-1 infection in resting CD4(+) T cells. Nat. Med. 18:1682-1689.
13. Descours B, Cribier A, Chable-Bessia C, Ayinde D, Rice G, Crow Y, Yatim A, Schwartz O, Laguette N, Benkirane M. 2012. SAMHD1 restricts HIV-1 reverse transcription in quiescent CD4+T-cells. Retrovirology 9:87. doi:10.1186/1742-4690-9-87.
14. Wu L. 2012. SAMHD1: a new contributor to HIV-1 restriction in resting CD4+ T-cells. Retrovirology 9:88. doi:10.1186/1742-4690-9-88.
15. Yan N, Lieberman J. 2012. SAMHD1 does it again, now in resting T cells. Nat. Med. 18:1611-1612.
16. Goldstone DC, Ennis-Adeniran V, Hedden JJ, Groom HC, Rice GI, Christodoulou E, Walker PA, Kelly G, Haire LF, Yap MW, de Carvalho LP, Stoye JP, Crow YJ, Taylor IA, Webb M. 2011. HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase. Nature 480:379-382.
17. Powell RD, Holland PJ, Hollis T, Perrino FW. 2011. Aicardi-Goutieres syndrome gene and HIV-1 restriction factor SAMHD1 is a dGTPregulated deoxynucleotide triphosphohydrolase. J. Biol. Chem. 286: 43596-43600.
18. Kim B, Nguyen LA, Daddacha W, Hollenbaugh JA. 2012. Tight interplay among SAMHD1 protein level, cellular dNTP levels, and HIV-1 proviral DNA synthesis kinetics in human primary monocyte-derived macrophages. J. Biol. Chem. 287:21570-21574.
19. Rice GI, Bond J, Asipu A, Brunette RL, Manfield IW, Carr IM, Fuller JC, Jackson RM, Lamb T, Briggs TA, Ali M, Gornall H, Couthard LR, Aeby A, Attard-Montalto SP, Bertini E, Bodemer C, Brockmann K, Brueton LA, Corry PC, Desguerre I, Fazzi E, Cazorla AG, Gener B, Hamel BC, Heiberg A, Hunter M, van der Knaap MS, Kumar R, Lagae L, Landrieu PG, Lourenco CM, Marom D, McDermott MF, van der Merwe W, Orcesi S, Prendiville JS, Rasmussen M, Shalev SA, Soler DM, Shinawi M, Spiegel R, Tan TY, Vanderver A, Wakeling EL, Wassmer E, Whittaker E, Lebon P, Stetson DB, Bonthron DT, Crow YJ. 2009. Mutations involved in Aicardi-Goutieres syndrome implicate SAMHD1 as regulator of the innate immune response. Nat. Genet. 41:829-832.
20. Berger A, Sommer AF, Zwarg J, Hamdorf M, Welzel K, Esly N, Panitz S, Reuter A, Ramos I, Jatiani A, Mulder LC, Fernandez-Sesma A, Rutsch F, Simon V, Konig R, Flory E. 2011. SAMHD1-deficient CD14+ cells from individuals with Aicardi-Goutieres syndrome are highly susceptible to HIV-1 infection. PLoS Pathog. 7:e1002425. doi:10.1371/journal .ppat.1002425.
21. Manel N, Hogstad B, Wang Y, Levy DE, Unutmaz D, Littman DR. 2010. Acryptic sensor for HIV-1 activates antiviral innate immunity in dendritic cells. Nature 467:214-217.
22. Pertel T, Reinhard C, Luban J. 2011. Vpx rescues HIV-1 transduction of dendritic cells from the antiviral state established by type 1 interferon. Retrovirology 8:49. doi:10.1186/1742-4690-8-49.
23. Sunseri N, O'Brien M, Bhardwaj N, Landau NR. 2011. Human immunodeficiency virus type 1 modified to package simian immunodeficiency virus Vpx efficiently infects macrophages and dendritic cells. J. Virol. 85: 6263-6274.
24. Chen P, Hubner W, Spinelli MA, Chen BK. 2007. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J. Virol. 81:12582-12595.
25. Jolly C, Kashefi K, Hollinshead M, Sattentau QJ. 2004. HIV-1 cell to cell transfer across an Env-induced, actin-dependent synapse. J. Exp. Med. 199:283-293.
26. Sourisseau M, Sol-Foulon N, Porrot F, Blanchet F, Schwartz O. 2007. Inefficient human immunodeficiency virus replication in mobile lymphocytes. J. Virol. 81:1000-1012.
27. Groot F, Welsch S, Sattentau QJ. 2008. Efficient HIV-1 transmission from macrophages to T cells across transient virological synapses. Blood 111:4660-4663.
28. Izquierdo-Useros N, Esteban O, Rodriguez-Plata MT, Erkizia I, Prado JG, Blanco J, Garcia-Parajo MF, Martinez-Picado J. 2011. Dynamic imaging of cell-free and cell-associated viral capture in mature dendritic cells. Traffic 12:1702-1713.
29. Wu L, KewalRamani VN. 2006. Dendritic-cell interactions with HIV: infection and viral dissemination. Nat. Rev. Immunol. 6:859-868.
30. Blanchet F, Moris A, Mitchell JP, Piguet V. 2011. A look at HIV journey: from dendritic cells to infection spread in CD4(+) T cells. Curr. Opin. HIV AIDS 6:391-397.
31. McDonald D, Wu L, Bohks SM, KewalRamani VN, Unutmaz D, Hope TJ. 2003. Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science 300:1295-1297.
32. Petit C, Buseyne F, Boccaccio C, Abastado JP, Heard JM, Schwartz O. 2001. Nef is required for efficient HIV-1 replication in cocultures of dendritic cells and lymphocytes. Virology 286:225-236.
33. Arhel N, Lehmann M, Clauss K, Nienhaus GU, Piguet V, Kirchhoff F. 2009. The inability to disrupt the immunological synapse between infected human T cells and APCs distinguishes HIV-1 from most other primate lentiviruses. J. Clin. Invest. 119:2965-2975.
34. Fackler OT, Alcover A, Schwartz O. 2007. Modulation of the immunological synapse: a key to HIV-1 pathogenesis? Nat. Rev. Immunol. 7:310-317.
35. Thoulouze MI, Sol-Foulon N, Blanchet F, Dautry-Varsat A, Schwartz O, Alcover A. 2006. Human immunodeficiency virus type 1 infection impairs the formation of the immunological synapse. Immunity 24:547-561.
36. Lepelley A, Louis S, Sourisseau M, Law HK, Pothlichet J, Schilte C, Chaperot L, Plumas J, Randall RE, Si-Tahar M, Mammano F, Albert ML, Schwartz O. 2011. Innate sensing of HIV-infected cells. PLoS Pathog. 7:e1001284. doi:10.1371/journal.ppat.1001284.
37. Vendrame D, Sourisseau M, Perrin V, Schwartz O, Mammano F. 2009. Partial inhibition of human immunodeficiency virus replication by type I interferons: impact of cell-to-cell viral transfer. J. Virol. 83:10527-10537.
38. Roesch F, Meziane O, Kula A, Nisole S, Porrot F, Anderson I, Mammano F, Fassati A, Marcello A, Benkirane M, Schwartz O. 2012. Hyperthermia stimulates HIV-1 replication. PLoS Pathog. 8:e1002792. doi: 10.1371/journal.ppat.1002792.
39. Goujon C, Jarrosson-Wuilleme L, Bernaud J, Rigal D, Darlix JL, Ci- marelli A. 2006. With a little help from a friend: increasing HIV transduction of monocyte-derived dendritic cells with virion-like particles of SIV- (MAC). Gene Ther. 13:991-994.
40. Fonteneau JF, Larsson M, Beignon AS, McKenna K, Dasilva I, Amara A, Liu YJ, Lifson JD, Littman DR, Bhardwaj N. 2004. Human immunodeficiency virus type 1 activates plasmacytoid dendritic cells and concomitantly induces the bystander maturation of myeloid dendritic cells. J. Virol. 78:5223-5232.
41. Haller O, Kochs G. 2011. Human MxA protein: an interferon-induced dynamin-like GTPase with broad antiviral activity. J. Interferon Cytokine Res. 31:79-87.
42. Cella M, Salio M, Sakakibara Y, Langen H, Julkunen I, Lanzavecchia A. 1999. Maturation, activation, and protection of dendritic cells induced by double-stranded RNA. J. Exp. Med. 189:821-829.
43. Nobile C, Petit C, Moris A, Skrabal K, Abastado JP, Mammano F, Schwartz O. 2005. Covert human immunodeficiency virus replication in dendritic cells and in DC-SIGN-expressing cells promotes long-term transmission to lymphocytes. J. Virol. 79:5386-5399.
44. Sigal A, Kim JT, Balazs AB, Dekel E, Mayo A, Milo R, Baltimore D. 2011. Cell-to-cell spread of HIV permits ongoing replication despite antiretroviral therapy. Nature 477:95-98.
45. Richardson MW, Carroll RG, Stremlau M, Korokhov N, Humeau LM, Silvestri G, Sodroski J, Riley JL. 2008. Mode of transmission affects the sensitivity of human immunodeficiency virus type 1 to restriction by rhesus TRIM5alpha. J. Virol. 82:11117-11128.
46. Casartelli N, Sourisseau M, Feldmann J, Guivel-Benhassine F, Mallet A, Marcelin AG, Guatelli J, Schwartz O. 2010. Tetherin restricts productive HIV-1 cell-to-cell transmission. PLoS Pathog. 6:e1000955. doi:10.1371 /journal.ppat.1000955.
47. Kuhl BD, Sloan RD, Donahue DA, Bar-Magen T, Liang C, Wainberg MA. 2010. Tetherin restricts direct cell-to-cell infection of HIV-1. Retrovirology 7:115. doi:10.1186/1742-4690-7-115.
48. Goncalves A, Karayel E, Rice GI, Bennett KL, Crow YJ, Superti-Furga G, Burckstummer T. 2012. SAMHD1 is a nucleic-acid binding protein that is mislocalized due to Aicardi-Goutieres syndrome-associated mutations. Hum. Mutat. 33:1116-1122.
49. White TE, Brandariz-Nunez A, Carlos Valle-Casuso J, Amie S, Nguyen L, Kim B, Brojatsch J, Diaz-Griffero F. 13 November2012. Contribution of SAM and HD domains to retroviral restriction mediated by human SAMHD1. Virology doi:10.1016/j.virol.2012.10.029. [Epub ahead of print.]
50. Fujita M, Nomaguchi M, Adachi A, Otsuka M. 2012. SAMHD1- dependent and -independent functions of HIV-2/SIV Vpx protein. Front. Microbiol. 3:297. doi:10.3389/fmicb.2012.00297.
51. Berger A, Munk C, Schweizer M, Cichutek K, Schule S, Flory E. 2010. Interaction of Vpx and apolipoprotein B mRNA-editing catalytic polypeptide 3 family member A (APOBEC3A) correlates with efficient lentivirus infection of monocytes. J. Biol. Chem. 285:12248-12254.
52. Berger G, Durand S, Fargier G, Nguyen XN, Cordeil S, Bouaziz S, Muriaux D, Darlix JL, Cimarelli A. 2011. APOBEC3A is a specific inhibitor of the early phases of HIV-1 infection in myeloid cells. PLoS Pathog. 7:e1002221. doi:10.1371/journal.ppat.1002221.
53. Servet C, Zitvogel L, Hosmalin A. 2002. Dendritic cells in innate immune responses against HIV. Curr. Mol. Med. 2:739-756.
54. Diamond TL, Roshal M, Jamburuthugoda VK, Reynolds HM, Merriam AR, Lee KY, Balakrishnan M, Bambara RA, Planelles V, Dewhurst S, Kim B. 2004. Macrophage tropism of HIV-1 depends on efficient cellular dNTP utilization by reverse transcriptase. J. Biol. Chem. 279:51545-51553.
55. Duvall MG, Lore K, Blaak H, Ambrozak DA, Adams WC, Santos K, Geldmacher C, Mascola JR, McMichael AJ, Jaye A, Whittle HC, Rowland- Jones SL, Koup RA. 2007. Dendritic cells are less susceptible to human immunodeficiency virus type 2 (HIV-2) infection than to HIV-1 infection. J. Virol. 81:13486-13498.
56. Doitsh G, Cavrois M, Lassen KG, Zepeda O, Yang Z, Santiago ML, Hebbeler AM, Greene WC. 2010. Abortive HIV infection mediates CD4 T cell depletion and inflammation in human lymphoid tissue. Cell 143: 789-801.
57. Manel N, Littman DR. 2011. Hiding in plain sight: how HIV evades innate immune responses. Cell 147:271-274.
58. Steinman RM, Hemmi H. 2006. Dendritic cells: translating innate to adaptive immunity. Curr. Top. Microbiol. Immunol. 311:17-58.
59. Buseyne F, Le Gall S, Boccaccio C, Abastado JP, Lifson JD, Arthur LO, Riviere Y, Heard JM, Schwartz O. 2001. MHC-I-restricted presentation of HIV-1 virion antigens without viral replication. Nat. Med. 7:344-349.
60. Beignon AS, McKenna K, Skoberne M, Manches O, DaSilva I, Kavanagh DG, Larsson M, Gorelick RJ, Lifson JD, Bhardwaj N. 2005. Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J. Clin. Invest. 115:3265-3275.