SAMHD1 limits HIV-1 antigen presentation by monocyte-derived dendritic cells

Journal of Virology

Volumn 89, Issue 14, 2015, Pages 6994-7006

  Ayinde, Diana ^a,b   Bruel, Timothée ^a,b   Cardinaud, Sylvain ^c,d,e,f   Porrot, Françoise ^a,b   Prado, Julia G ^g   Moris, Arnaud ^c,d,e,h   Schwartza, Olivier ^b,f  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d INSERM   (France)

^e Assistance publique Hôpitaux de Paris   (France)

^f Vaccine Research Institute   (France)

^g HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

^h PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

SAMHD1 PROTEIN; UNCLASSIFIED DRUG; VIRAL PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; SAMHD1 PROTEIN, HUMAN;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; LIMIT OF QUANTITATION; MICROSCOPY; MOLECULAR CLONING; MONOCYTE; MONOCYTE DERIVED DENDRITIC CELL; NONHUMAN; PRIORITY JOURNAL; VIRUS ACTIVATION; VIRUS ENTRY; VIRUS PATHOGENESIS; VIRUS STRAIN; CD8+ T LYMPHOCYTE; CELL CULTURE; IMMUNOLOGY;

ANTIGEN PRESENTATION; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DENDRITIC CELLS; HIV ANTIGENS; HIV-1; HUMANS; MONOMERIC GTP-BINDING PROTEINS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84964697763     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00069-15     Document Type: Article

References (58)

1. McMichael AJ, Borrow P, Tomaras GD, Goonetilleke N, Haynes BF. 2010. The immune response during acute HIV-1 infection: clues for vaccine development. Nat Rev Immunol 10:11-23. http://dx.doi.org/10.1038/nri2674.
2. Jin X, Bauer DE, Tuttleton SE, Lewin S, Gettie A, Blanchard J, Irwin CE, Safrit JT, Mittler J, Weinberger L, Kostrikis LG, Zhang L, Perelson AS, Ho DD. 1999. Dramatic rise in plasma viremia after CD8(+) T cell depletion in simian immunodeficiency virus-infected macaques. J Exp Med 189:991-998. http://dx.doi.org/10.1084/jem.189.6.991.
3. Schmitz JE, Kuroda MJ, Santra S, Sasseville VG, Simon MA, Lifton MA, Racz P, Tenner-Racz K, Dalesandro M, Scallon BJ, Ghrayeb J, Forman MA, Montefiori DC, Rieber EP, Letvin NL, Reimann KA. 1999. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283:857-860. http://dx.doi.org/10.1126/science.283.5403.857.
4. 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. http://dx.doi.org/10.1038/85493.
5. Rodriguez-Plata MT, Urrutia A, Cardinaud S, Buzon MJ, Izquierdo-Useros N, Prado JG, Puertas MC, Erkizia I, Coulon PG, Cedeno S, Clotet B, Moris A, Martinez-Picado J. 2012. HIV-1 capture and antigen presentation by dendritic cells: enhanced viral capture does not correlate with better T cell activation. J Immunol 188:6036-6045. http://dx.doi.org/10.4049/jimmunol.1200267.
6. Granelli-Piperno A, Zhong L, Haslett P, Jacobson J, Steinman RM. 2000. Dendritic cells, infected with vesicular stomatitis virus-pseudotyped HIV-1, present viral antigens to CD4+ and CD8+ T cells from HIV-1- infected individuals. J Immunol 165:6620-6626. http://dx.doi.org/10.4049/jimmunol.165.11.6620.
7. 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. http://dx.doi.org/10.1038/nature10195.
8. 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. http://dx.doi.org/10.1038/nature10117.
9. Ayinde D, Casartelli N, Schwartz O. 2012. Restricting HIV the SAMHD1 way: through nucleotide starvation. Nat Rev Microbiol 10:675-680. http://dx.doi.org/10.1038/nrmicro2862.
10. 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. http://dx.doi.org/10.1074/jbc .C112.374843.
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. http://dx.doi.org/10.1038/ni.2236.
12. St Gelais C, de Silva S, Amie SM, Coleman CM, Hoy H, Hollenbaugh JA, Kim B, Wu L. 2012. SAMHD1 restricts HIV-1 infection in dendritic cells (DCs) by dNTP depletion, but its expression in DCs and primary CD4+ T-lymphocytes cannot be upregulated by interferons. Retrovirology 9:105. http://dx.doi.org/10.1186/1742-4690-9-105.
13. Ryoo J, Choi J, Oh C, Kim S, Seo M, Kim SY, Seo D, Kim J, White TE, Brandariz-Nunez A, Diaz-Griffero F, Yun CH, Hollenbaugh JA, Kim B, Baek D, Ahn K. 2014. The ribonuclease activity of SAMHD1 is required for HIV-1 restriction. Nat Med 20:936-941. http://dx.doi.org/10.1038/nm.3626.
14. Puigdomenech I, Casartelli N, Porrot F, Schwartz O. 2013. SAMHD1 restricts HIV-1 cell-to-cell transmission and limits immune detection in monocyte-derived dendritic cells. J Virol 87:2846-2856. http://dx.doi.org/10.1128/JVI.02514-12.
15. 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. http://dx.doi.org/10.1038/nature09337.
16. Galao RP, Le Tortorec A, Pickering S, Kueck T, Neil SJ. 2012. Innate sensing of HIV-1 assembly by Tetherin induces NFkappaB-dependent proinflammatory responses. Cell Host Microbe 12:633-644. http://dx.doi.org/10.1016/j.chom.2012.10.007.
17. Neil SJ, Zang T, Bieniasz PD. 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425-430. http://dx.doi.org/10.1038/nature06553.
18. Van Damme N, Goff D, Katsura C, Jorgenson RL, Mitchell R, Johnson MC, Stephens EB, Guatelli J. 2008. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 3:245-252. http://dx.doi.org/10.1016/j.chom.2008.03.001.
19. Collins KL, Chen BK, Kalams SA, Walker BD, Baltimore D. 1998. HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature 391:397-401. http://dx.doi.org/10.1038/34929.
20. Schwartz O, Marechal V, Le Gall S, Lemonnier F, Heard JM. 1996. Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat Med 2:338-342. http://dx.doi.org/10.1038/nm0396-338.
21. Tomiyama H, Akari H, Adachi A, Takiguchi M. 2002. Different effects of Nef-mediated HLA class I down-regulation on human immunodeficiency virus type 1-specific CD8(+) T-cell cytolytic activity and cytokine production. J Virol 76:7535-7543. http://dx.doi.org/10.1128/JVI.76.15.7535-7543.2002.
22. Yang OO, Nguyen PT, Kalams SA, Dorfman T, Gottlinger HG, Stewart S, Chen IS, Threlkeld S, Walker BD. 2002. Nef-mediated resistance of human immunodeficiency virus type 1 to antiviral cytotoxic T lymphocytes. J Virol 76:1626-1631. http://dx.doi.org/10.1128/JVI.76.4.1626-1631.2002.
23. Mangeat B, Turelli P, Caron G, Friedli M, Perrin L, Trono D. 2003. Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424:99-103. http://dx.doi.org/10 .1038/nature01709.
24. Marin M, Rose KM, Kozak SL, Kabat D. 2003. HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat Med 9:1398-1403. http://dx.doi.org/10.1038/nm946.
25. Zhang H, Yang B, Pomerantz RJ, Zhang C, Arunachalam SC, Gao L. 2003. The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424:94-98. http://dx.doi.org/10.1038/nature01707.
26. Casartelli N, Guivel-Benhassine F, Bouziat R, Brandler S, Schwartz O, Moris A. 2010. The antiviral factor APOBEC3G improves CTL recognition of cultured HIV-infected T cells. J Exp Med 207:39-49. http://dx.doi.org/10.1084/jem.20091933.
27. Ochsenbauer C, Edmonds TG, Ding H, Keele BF, Decker J, Salazar MG, Salazar-Gonzalez JF, Shattock R, Haynes BF, Shaw GM, Hahn BH, Kappes JC. 2012. Generation of transmitted/founder HIV-1 infectious molecular clones and characterization of their replication capacity in CD4 T lymphocytes and monocyte-derived macrophages. J Virol 86:2715-2728. http://dx.doi.org/10.1128/JVI.06157-11.
28. Moris A, Nobile C, Buseyne F, Porrot F, Abastado JP, Schwartz O. 2004. DC-SIGN promotes exogenous MHC-I-restricted HIV-1 antigen presentation. Blood 103:2648-2654. http://dx.doi.org/10.1182/blood-2003-07-2532.
29. Kløverpris HN, Payne RP, Sacha JB, Rasaiyaah JT, Chen F, Takiguchi M, Yang OO, Towers GJ, Goulder P, Prado JG. 2013. Early antigen presentation of protective HIV-1 KF11Gag and KK10Gag epitopes from incoming viral particles facilitates rapid recognition of infected cells by specific CD8+ T cells. J Virol 87:2628-2638. http://dx.doi.org/10.1128/JVI.02131-12.
30. Wildum S, Schindler M, Munch J, Kirchhoff F. 2006. Contribution of Vpu, Env, and Nef to CD4 down-modulation and resistance of human immunodeficiency virus type 1-infected T cells to superinfection. J Virol 80:8047-8059. http://dx.doi.org/10.1128/JVI.00252-06.
31. Goujon C, Jarrosson-Wuilleme L, Bernaud J, Rigal D, Darlix JL, Cimarelli 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. http://dx.doi.org/10.1038/sj.gt .3302753.
32. Cocchi F, DeVico AL, Lu W, Popovic M, Latinovic O, Sajadi MM, Redfield RR, Lafferty MK, Galli M, Garzino-Demo A, Gallo RC. 2012. Soluble factors from T cells inhibiting X4 strains of HIV are a mixture of beta chemokines and RNases. Proc Natl Acad Sci U S A 109:5411-5416. http://dx.doi.org/10.1073/pnas.1202240109.
33. Killian MS, Teque F, Walker RL, Meltzer PS, Killian JK. 2013. CD8(+) lymphocytes suppress human immunodeficiency virus 1 replication by secreting type I interferons. J Interferon Cytokine Res 33:632-645. http: //dx.doi.org/10.1089/jir.2012.0067.
34. Yang OO, Kalams SA, Trocha A, Cao H, Luster A, Johnson RP, Walker BD. 1997. Suppression of human immunodeficiency virus type 1 replication by CD8+ cells: evidence for HLA class I-restricted triggering of cytolytic and noncytolytic mechanisms. J Virol 71:3120-3128.
35. Yang OO, Kalams SA, Rosenzweig M, Trocha A, Jones N, Koziel M, Walker BD, Johnson RP. 1996. Efficient lysis of human immunodeficiency virus type 1-infected cells by cytotoxic T lymphocytes. J Virol 70: 5799-5806.
36. Betts MR, Brenchley JM, Price DA, De Rosa SC, Douek DC, Roederer M, Koup RA. 2003. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J Immunol Methods 281:65-78. http://dx.doi.org/10.1016/S0022-1759(03)00265-5.
37. Parrish NF, Gao F, Li H, Giorgi EE, Barbian HJ, Parrish EH, Zajic L, Iyer SS, Decker JM, Kumar A, Hora B, Berg A, Cai F, Hopper J, Denny TN, Ding H, Ochsenbauer C, Kappes JC, Galimidi RP, West AP, Jr, Bjorkman PJ, Wilen CB, Doms RW, O'Brien M, Bhardwaj N, Borrow P, Haynes BF, Muldoon M, Theiler JP, Korber B, Shaw GM, Hahn BH. 2013. Phenotypic properties of transmitted founder HIV-1. Proc Natl Acad SciUSA110:6626-6633. http://dx.doi.org/10.1073/pnas.1304288110.
38. Salazar-Gonzalez JF, Salazar MG, Keele BF, Learn GH, Giorgi EE, Li H, Decker JM, Wang S, Baalwa J, Kraus MH, Parrish NF, Shaw KS, Guffey MB, Bar KJ, Davis KL, Ochsenbauer-Jambor C, Kappes JC, Saag MS, Cohen MS, Mulenga J, Derdeyn CA, Allen S, Hunter E, Markowitz M, Hraber P, Perelson AS, Bhattacharya T, Haynes BF, Korber BT, Hahn BH, Shaw GM. 2009. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J Exp Med 206:1273-1289. http://dx.doi.org/10.1084/jem.20090378.
39. Mlcochova P, Watters SA, Towers GJ, Noursadeghi M, Gupta RK. 2014. Vpx complementation of "non-macrophage tropic" R5 viruses reveals robust entry of infectious HIV-1 cores into macrophages. Retrovirology 11:25. http://dx.doi.org/10.1186/1742-4690-11-25.
40. Le Gall S, Stamegna P, Walker BD. 2007. Portable flanking sequences modulate CTL epitope processing. J Clin Investig 117:3563-3575. http: //dx.doi.org/10.1172/JCI32047.
41. Petit C, Buseyne F, Boccaccio C, Abastado JP, Heard JM, Schwartz O. 2001. Nef is required for efficient HIV-1 replication in cocultures of den-dritic cells and lymphocytes. Virology 286:225-236. http://dx.doi.org/10 .1006/viro.2001.0984.
42. Maccormac LP, Jacque JM, Chain B. 2004. The functional consequences of delivery of HIV-1 Nef to dendritic cells using an adenoviral vector. Vaccine 22:528-535. http://dx.doi.org/10.1016/j.vaccine.2003.07.009.
43. Migueles SA, Osborne CM, Royce C, Compton AA, Joshi RP, Weeks KA, Rood JE, Berkley AM, Sacha JB, Cogliano-Shutta NA, Lloyd M, Roby G, Kwan R, McLaughlin M, Stallings S, Rehm C, O'Shea MA, Mican J, Packard BZ, Komoriya A, Palmer S, Wiegand AP, Maldarelli F, Coffin JM, Mellors JW, Hallahan CW, Follman DA, Connors M. 2008. Lytic granule loading of CD8+ T cells is required for HIV-infected cell elimination associated with immune control. Immunity 29:1009-1021. http://dx.doi.org/10.1016/j.immuni.2008.10.010.
44. Wiedemann A, Depoil D, Faroudi M, Valitutti S. 2006. Cytotoxic T lymphocytes kill multiple targets simultaneously via spatiotemporal uncoupling of lytic and stimulatory synapses. Proc Natl Acad Sci U S A 103:10985-10990. http://dx.doi.org/10.1073/pnas.0600651103.
45. Foley MH, Forcier T, McAndrew E, Gonzalez M, Chen H, Juelg B, Walker BD, Irvine DJ. 2014. High avidity CD8+ T cells efficiently eliminate motile HIV-infected targets and execute a locally focused program of anti-viral function. PLoS One 9:e87873. http://dx.doi.org/10.1371 /journal.pone.0087873.
46. Freel SA, Picking RA, Ferrari G, Ding H, Ochsenbauer C, Kappes JC, Kirchherr JL, Soderberg KA, Weinhold KJ, Cunningham CK, Denny TN, Crump JA, Cohen MS, McMichael AJ, Haynes BF, Tomaras GD. 2012. Initial HIV-1 antigen-specific CD8+ T cells in acute HIV-1 infection inhibit transmitted/founder virus replication. J Virol 86:6835-6846. http: //dx.doi.org/10.1128/JVI.00437-12.
47. Goonetilleke N, Liu MK, Salazar-Gonzalez JF, Ferrari G, Giorgi E, Ganusov VV, Keele BF, Learn GH, Turnbull EL, Salazar MG, Weinhold KJ, Moore S, Letvin N, Haynes BF, Cohen MS, Hraber P, Bhattacharya T, Borrow P, Perelson AS, Hahn BH, Shaw GM, Korber BT, McMichael AJ. 2009. The first T cell response to transmitted/founder virus contributes to the control of acute viremia in HIV-1 infection. J Exp Med 206: 1253-1272. http://dx.doi.org/10.1084/jem.20090365.
48. Calantone N, Wu F, Klase Z, Deleage C, Perkins M, Matsuda K, Thompson EA, Ortiz AM, Vinton CL, Ourmanov I, Lore K, Douek DC, Estes JD, Hirsch VM, Brenchley JM. 2014. Tissue myeloid cells in SIVinfected primates acquire viral DNA through phagocytosis of infected T cells. Immunity 41:493-502. http://dx.doi.org/10.1016/j.immuni.2014.08 .014.
49. Baxter AE, Russell RA, Duncan CJ, Moore MD, Willberg CB, Pablos JL, Finzi A, Kaufmann DE, Ochsenbauer C, Kappes JC, Groot F, Sattentau QJ. 2014. Macrophage infection via selective capture of HIV-1-infected CD4(+) T cells. Cell Host Microbe 16:711-721. http://dx.doi.org/10.1016/j.chom.2014.10.010.
50. Hoeffel G, Ripoche AC, Matheoud D, Nascimbeni M, Escriou N, Lebon P, Heshmati F, Guillet JG, Gannage M, Caillat-Zucman S, Casartelli N, Schwartz O, De la Salle H, Hanau D, Hosmalin A, Maranon C. 2007. Antigen crosspresentation by human plasmacytoid dendritic cells. Immunity 27:481-492. http://dx.doi.org/10.1016/j.immuni.2007.07.021.
51. Maranon C, Desoutter JF, Hoeffel G, Cohen W, Hanau D, Hosmalin A. 2004. Dendritic cells cross-present HIV antigens from live as well as apoptotic infected CD4+ T lymphocytes. Proc Natl Acad Sci U S A 101:6092-6097. http://dx.doi.org/10.1073/pnas.0304860101.
52. Gibbs JS, Lackner AA, Lang SM, Simon MA, Sehgal PK, Daniel MD, Desrosiers RC. 1995. Progression to AIDS in the absence of a gene for vpr or vpx. J Virol 69:2378-2383.
53. Hirsch VM, Sharkey ME, Brown CR, Brichacek B, Goldstein S, Wakefield J, Byrum R, Elkins WR, Hahn BH, Lifson JD, Stevenson M. 1998. Vpx is required for dissemination and pathogenesis of SIV(SM) PBj: evidence of macrophage-dependent viral amplification. Nat Med 4:1401-1408. http://dx.doi.org/10.1038/3992.
54. Westmoreland SV, Converse AP, Hrecka K, Hurley M, Knight H, Piatak M, Lifson J, Mansfield KG, Skowronski J, Desrosiers RC. 2014. SIV vpx is essential for macrophage infection but not for development of AIDS. PLoS One 9:e84463. http://dx.doi.org/10.1371/journal.pone .0084463.
55. 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 18:1682-1687. http://dx.doi.org/10.1038/nm .2964.
56. 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. http://dx.doi.org/10.1186/1742-4690-9-87.
57. Wu L. 2012. SAMHD1: a new contributor to HIV-1 restriction in resting CD4+ T-cells. Retrovirology 9:88. http://dx.doi.org/10.1186/1742-4690 -9-88.
58. Chauveau L, Puigdomenech I, Ayinde D, Roesch F, Porrot F, Bruni D, Visseaux B, Descamps D, Schwartz O. 2015. HIV-2 infects resting CD4+ T cells but not monocyte-derived dendritic cells. Retrovirology 12:2. http: //dx.doi.org/10.1186/s12977-014-0131-7.