Vpx rescue of HIV-1 from the antiviral state in mature dendritic cells is independent of the intracellular deoxynucleotide concentration

Retrovirology

Volumn 11, Issue 1, 2014, Pages

  Reinhard, Christian ^a   Bottinelli, Dario ^a   Kim, Baek ^b   Luban, Jeremy ^a,c  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Dendritic cell; HIV 1; Integration; Interferon; Reverse transcription; SAMHD1; SIV; Vpx

Indexed keywords

CELL ENZYME; COMPLEMENTARY DNA; DEOXYRIBONUCLEOTIDE; LENTIVIRUS VECTOR; LIPOPOLYSACCHARIDE; PEVONEDISTAT; SAMHD1 PROTEIN; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN; VPRS PROTEIN; VPX PROTEIN;

ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; DENDRITIC CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LONG TERMINAL REPEAT; MONOCYTE; NONHUMAN; PROTEIN DEGRADATION; REVERSE TRANSCRIPTION; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL GENE DELIVERY SYSTEM; VIRUS LIKE AGENT;

HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; PRIMATES; SIMIAN IMMUNODEFICIENCY VIRUS;

DENDRITIC CELLS; HIV-1; HUMANS; MONOMERIC GTP-BINDING PROTEINS; PROTEOLYSIS; TRANSDUCTION, GENETIC; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 84893185403     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-11-12     Document Type: Article

References (71)

1. Duggal NK, Emerman M. Evolutionary conflicts between viruses and restriction factors shape immunity. Nat Rev Immunol 2012, 12:687-695. 10.1038/nri3295, 3690816, 22976433.
2. Malim MH, Emerman M. HIV-1 accessory proteins-ensuring viral survival in a hostile environment. Cell Host Microbe 2008, 3:388-398. 10.1016/j.chom.2008.04.008, 18541215.
3. Randall RE, Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 2008, 89:1-47. 10.1099/vir.0.83391-0, 18089727.
4. Iwasaki A. Innate immune recognition of HIV-1. Immunity 2012, 37:389-398. 10.1016/j.immuni.2012.08.011, 3578946, 22999945.
5. Kim B, Nguyen LA, Daddacha W, Hollenbaugh JA. 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 2012, 287:21570-21574. 10.1074/jbc.C112.374843, 3381122, 22589553.
6. Kennedy EM, Gavegnano C, Nguyen L, Slater R, Lucas A, Fromentin E, Schinazi RF, Kim B. Ribonucleoside triphosphates as substrate of human immunodeficiency virus type 1 reverse transcriptase in human macrophages. J Biol Chem 2010, 285:39380-39391. 10.1074/jbc.M110.178582, 2998149, 20924117.
7. Kennedy EM, Daddacha W, Slater R, Gavegnano C, Fromentin E, Schinazi RF, Kim B. Abundant non-canonical dUTP found in primary human macrophages drives its frequent incorporation by HIV-1 reverse transcriptase. J Biol Chem 2011, 286:25047-25055. 10.1074/jbc.M111.234047, 3137078, 21454906.
8. Kennedy EM, Amie SM, Bambara RA, Kim B. Frequent incorporation of ribonucleotides during HIV-1 reverse transcription and their attenuated repair in macrophages. J Biol Chem 2012, 287:14280-14288. 10.1074/jbc.M112.348482, 3340154, 22383524.
9. Goldstone DC, Ennis-Adeniran V, Hedden JJ, Groom HC, Rice GI, Christodoulou E, Walker PA, Kelly G, Haire LF, Yap MW, et al. HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase. Nature 2011, 480:379-382. 10.1038/nature10623, 22056990.
10. Gramberg T, Kahle T, Bloch N, Wittmann S, Mullers E, Daddacha W, Hofmann H, Kim B, Lindemann D, Landau NR. Restriction of diverse retroviruses by SAMHD1. Retrovirology 2013, 10:26. 10.1186/1742-4690-10-26, 3605129, 23497255.
11. Lahouassa H, Daddacha W, Hofmann H, Ayinde D, Logue EC, Dragin L, Bloch N, Maudet C, Bertrand M, Gramberg T, et al. SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat Immunol 2012, 13:223-228. 10.1038/ni.2236, 3771401, 22327569.
12. Hollenbaugh JA, Gee P, Baker J, Daly MB, Amie SM, Tate J, Kasai N, Kanemura Y, Kim DH, Ward BM, et al. Host factor SAMHD1 restricts DNA viruses in non-dividing myeloid cells. PLoS Pathog 2013, 9:e1003481. 10.1371/journal.ppat.1003481, 3694861, 23825958.
13. Laguette N, Sobhian B, Casartelli N, Ringeard M, Chable-Bessia C, Segeral 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 2011, 474:654-657. 10.1038/nature10117, 3595993, 21613998.
14. Hrecka K, Hao C, Gierszewska M, Swanson SK, Kesik-Brodacka M, Srivastava S, Florens L, Washburn MP, Skowronski J. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 2011, 474:658-661. 10.1038/nature10195, 3179858, 21720370.
15. Berger A, Sommer AF, Zwarg J, Hamdorf M, Welzel K, Esly N, Panitz S, Reuter A, Ramos I, Jatiani A, et al. SAMHD1-deficient CD14+ cells from individuals with Aicardi-Goutieres syndrome are highly susceptible to HIV-1 infection. PLoS Pathog 2011, 7:e1002425. 10.1371/journal.ppat.1002425, 3234228, 22174685.
16. Baldauf HM, Pan X, Erikson E, Schmidt S, Daddacha W, Burggraf M, Schenkova K, Ambiel I, Wabnitz G, Gramberg T, et al. SAMHD1 restricts HIV-1 infection in resting CD4 (+) T cells. Nat Med 2012, 18:1682-1687. 10.1038/nm.2964, 3828732, 22972397.
17. Descours B, Cribier A, Chable-Bessia C, Ayinde D, Rice G, Crow Y, Yatim A, Schwartz O, Laguette N, Benkirane M. SAMHD1 restricts HIV-1 reverse transcription in quiescent CD4 (+) T-cells. Retrovirology 2012, 9:87. 10.1186/1742-4690-9-87, 3494655, 23092122.
18. Tristem M, Marshall C, Karpas A, Hill F. Evolution of the primate lentiviruses: evidence from vpx and vpr. EMBO J 1992, 11:3405-3412. 556875, 1324171.
19. Sharp PM, Bailes E, Stevenson M, Emerman M, Hahn BH. Gene acquisition in HIV and SIV. Nature 1996, 383:586-587. 10.1038/383586a0, 8857532.
20. Lim ES, Fregoso OI, McCoy CO, Matsen FA, Malik HS, Emerman M. The ability of primate lentiviruses to degrade the monocyte restriction factor SAMHD1 preceded the birth of the viral accessory protein Vpx. Cell Host Microbe 2012, 11:194-204. 10.1016/j.chom.2012.01.004, 3288607, 22284954.
21. Paxton W, Connor RI, Landau NR. Incorporation of Vpr into human immunodeficiency virus type 1 virions: requirement for the p6 region of gag and mutational analysis. J Virol 1993, 67:7229-7237. 238185, 8230445.
22. Jin L, Zhou Y, Ratner L. HIV type 2 Vpx interaction with Gag and incorporation into virus-like particles. AIDS Res Hum Retroviruses 2001, 17:105-111. 10.1089/08892220150217193, 11177390.
23. Goujon C, Riviere L, Jarrosson-Wuilleme L, Bernaud J, Rigal D, Darlix JL, Cimarelli A. SIVSM/HIV-2 Vpx proteins promote retroviral escape from a proteasome-dependent restriction pathway present in human dendritic cells. Retrovirology 2007, 4:2. 10.1186/1742-4690-4-2, 1779362, 17212817.
24. 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, 8:1169-1175. 400930, 2743977.
25. Goujon C, Arfi V, Pertel T, Luban J, Lienard J, Rigal D, Darlix JL, Cimarelli A. Characterization of simian immunodeficiency virus SIVSM/human immunodeficiency virus type 2 Vpx function in human myeloid cells. J Virol 2008, 82:12335-12345. 10.1128/JVI.01181-08, 2593360, 18829761.
26. Gibbs JS, Regier DA, Desrosiers RC. Construction and in vitro properties of SIVmac mutants with deletions in "nonessential" genes. AIDS Res Hum Retroviruses 1994, 10:333-342. 10.1089/aid.1994.10.333, 8068413.
27. 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, 38:871-878. 10.1111/j.1348-0421.1994.tb02140.x, 7898386.
28. Schule S, Kloke BP, Kaiser JK, Heidmeier S, Panitz S, Wolfrum N, Cichutek K, Schweizer M. Restriction of HIV-1 replication in monocytes is abolished by Vpx of SIVsmmPBj. PloS One 2009, 4:e7098. 10.1371/journal.pone.0007098, 2741571, 19768115.
29. Fujita M, Otsuka M, Miyoshi M, Khamsri B, Nomaguchi M, Adachi A. Vpx is critical for reverse transcription of the human immunodeficiency virus type 2 genome in macrophages. J Virol 2008, 82:7752-7756. 10.1128/JVI.01003-07, 2493314, 18495778.
30. Gibbs JS, Lackner AA, Lang SM, Simon MA, Sehgal PK, Daniel MD, Desrosiers RC. Progression to AIDS in the absence of a gene for vpr or vpx. J Virol 1995, 69:2378-2383. 188910, 7884883.
31. Hirsch VM, Sharkey ME, Brown CR, Brichacek B, Goldstein S, Wakefield J, Byrum R, Elkins WR, Hahn BH, Lifson JD, Stevenson M. Vpx is required for dissemination and pathogenesis of SIV(SM) PBj: evidence of macrophage-dependent viral amplification. Nat Med 1998, 4:1401-1408. 10.1038/3992, 9846578.
32. Sharova N, Wu Y, Zhu X, Stranska R, Kaushik R, Sharkey M, Stevenson M. Primate lentiviral Vpx commandeers DDB1 to counteract a macrophage restriction. PLoS Pathog 2008, 4:e1000057. 10.1371/journal.ppat.1000057, 2323106, 18451984.
33. Srivastava S, Swanson SK, Manel N, Florens L, Washburn MP, Skowronski J. Lentiviral Vpx accessory factor targets VprBP/DCAF1 substrate adaptor for cullin 4 E3 ubiquitin ligase to enable macrophage infection. PLoS Pathog 2008, 4:e1000059. 10.1371/journal.ppat.1000059, 2330158, 18464893.
34. Ahn J, Hao C, Yan J, DeLucia M, Mehrens J, Wang C, Gronenborn AM, Skowronski J. HIV/simian immunodeficiency virus (SIV) accessory virulence factor Vpx loads the host cell restriction factor SAMHD1 onto the E3 ubiquitin ligase complex CRL4DCAF1. J Biol Chem 2012, 287:12550-12558. 10.1074/jbc.M112.340711, 3321004, 22362772.
35. Fregoso OI, 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 2013, 9:e1003496. 10.1371/journal.ppat.1003496, 3715410, 23874202.
36. 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, 3:1036-1043. 10.1016/j.celrep.2013.03.017, 23602554.
37. White TE, Brandariz-Nunez A, Valle-Casuso JC, Amie S, Nguyen LA, Kim B, Tuzova M, Diaz-Griffero F. The retroviral restriction ability of SAMHD1, but not its deoxynucleotide triphosphohydrolase activity, is regulated by phosphorylation. Cell Host Microbe 2013, 13:441-451. 10.1016/j.chom.2013.03.005, 23601106.
38. White TE, Brandariz-Nunez A, Carlos Valle-Casuso J, Amie S, Nguyen L, Kim B, Brojatsch J, Diaz-Griffero F. Contribution of SAM and HD domains to retroviral restriction mediated by human SAMHD1. Virology 2013, 436:81-90. 10.1016/j.virol.2012.10.029, 3767443, 23158101.
39. Welbourn S, Dutta SM, Semmes OJ, Strebel K. Restriction of virus infection but not catalytic dNTPase activity are regulated by phosphorylation of SAMHD1. J Virol 2013, 87:11516-11524. 10.1128/JVI.01642-13, 23966382.
40. 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 therapy 2006, 13:991-994. 10.1038/sj.gt.3302753, 16525481.
41. Pertel T, Reinhard C, Luban J. Vpx rescues HIV-1 transduction of dendritic cells from the antiviral state established by type 1 interferon. Retrovirology 2011, 8:49. 10.1186/1742-4690-8-49, 3130655, 21696578.
42. Goujon C, Schaller T, Galao RP, Amie SM, Kim B, Olivieri K, Neil SJ, Malim MH. Evidence for IFNalpha-induced, SAMHD1-independent inhibitors of early HIV-1 infection. Retrovirology 2013, 10:23. 10.1186/1742-4690-10-23, 3598776, 23442224.
43. Dragin L, Nguyen LA, Lahouassa H, Sourisce A, Kim B, Ramirez BC, Margottin-Goguet F. Interferon block to HIV-1 transduction in macrophages despite SAMHD1 degradation and high deoxynucleoside triphosphates supply. Retrovirology 2013, 10:30. 10.1186/1742-4690-10-30, 3599726, 23497353.
44. Pavlovic J, Haller O, Staeheli P. Human and mouse Mx proteins inhibit different steps of the influenza virus multiplication cycle. J Virol 1992, 66:2564-2569. 289059, 1548781.
45. St Gelais C, de Silva S, Amie SM, Coleman CM, Hoy H, Hollenbaugh JA, Kim B, Wu L. 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 2012, 9:105. 10.1186/1742-4690-9-105, 3527137, 23231760.
46. de Baey A, Lanzavecchia A. The role of aquaporins in dendritic cell macropinocytosis. J Exp Med 2000, 191:743-748. 10.1084/jem.191.4.743, 2195835, 10684866.
47. Diamond TL, Roshal M, Jamburuthugoda VK, Reynolds HM, Merriam AR, Lee KY, Balakrishnan M, Bambara RA, Planelles V, Dewhurst S, Kim B. Macrophage tropism of HIV-1 depends on efficient cellular dNTP utilization by reverse transcriptase. J Biol Chem 2004, 279:51545-51553. 10.1074/jbc.M408573200, 1351161, 15452123.
48. Soucy TA, Smith PG, Milhollen MA, Berger AJ, Gavin JM, Adhikari S, Brownell JE, Burke KE, Cardin DP, Critchley S, et al. An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature 2009, 458:732-736. 10.1038/nature07884, 19360080.
49. Stanley DJ, Bartholomeeusen K, Crosby DC, Kim DY, Kwon E, Yen L, Cartozo NC, Li M, Jager S, Mason-Herr J, et al. Inhibition of a NEDD8 Cascade Restores Restriction of HIV by APOBEC3G. PLoS Pathog 2012, 8:e1003085. 10.1371/journal.ppat.1003085, 3531493, 23300442.
50. Pertel T, Hausmann S, Morger D, Zuger S, Guerra J, Lascano J, Reinhard C, Santoni FA, Uchil PD, Chatel L, et al. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 2011, 472:361-365. 10.1038/nature09976, 3081621, 21512573.
51. 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, 467:214-217. 10.1038/nature09337, 3051279, 20829794.
52. De Iaco A, Santoni F, Vannier A, Guipponi M, Antonarakis S, Luban J. TNPO3 protects HIV-1 replication from CPSF6-mediated capsid stabilization in the host cell cytoplasm. Retrovirology 2013, 10:20. 10.1186/1742-4690-10-20, 3599327, 23414560.
53. Neagu MR, Ziegler P, Pertel T, Strambio-De-Castillia C, Grutter C, Martinetti G, Mazzucchelli L, Grutter M, Manz MG, Luban J. Potent inhibition of HIV-1 by TRIM5-cyclophilin fusion proteins engineered from human components. J Clin Invest 2009, 119:3035-3047. 10.1172/JCI39354, 2752079, 19741300.
54. Bloch N, OBrien M, Norton TD, Polsky SB, Bhardwaj N, Landau NR. HIV type 1 infection of plasmacytoid and myeloid dendritic cells is restricted by high levels of SAMHD1 and cannot be counteracted by Vpx. AIDS Res Hum Retroviruses 2013, 30:195-203.
55. Amie SM, Noble E, Kim B. Intracellular nucleotide levels and the control of retroviral infections. Virology 2013, 436:247-254. 10.1016/j.virol.2012.11.010, 23260109.
56. Beloglazova N, Flick R, Tchigvintsev A, Brown G, Popovic A, Nocek B, Yakunin AF. Nuclease activity of the human SAMHD1 protein implicated in the Aicardi-Goutieres syndrome and HIV-1 restriction. J Biol Chem 2013, 288:8101-8110. 10.1074/jbc.M112.431148, 23364794.
57. Berger G, Goujon C, Darlix JL, Cimarelli A. SIVMAC Vpx improves the transduction of dendritic cells with nonintegrative HIV-1-derived vectors. Gene Ther 2009, 16:159-163. 10.1038/gt.2008.128, 18668143.
58. Yan J, Kaur S, Delucia M, Hao C, Mehrens J, Wang C, Golczak M, Palczewski K, Gronenborn AM, Ahn J, Skowronski J. Tetramerization of SAMHD1 is required for biological activity and inhibition of HIV infection. J Biol Chem 2013, 288:10406-10417. 10.1074/jbc.M112.443796, 3624423, 23426366.
59. Delucia M, Mehrens J, Wu Y, Ahn J. HIV-2 and SIVmac accessory virulence factor Vpx down-regulates SAMHD1 catalysis prior to proteasome-dependent degradation. J Biol Chem 2013, 288:19116-19126. 10.1074/jbc.M113.469007, 23677995.
60. Zufferey R, Dull T, Mandel RJ, Bukovsky A, Quiroz D, Naldini L, Trono D. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 1998, 72:9873-9880. 110499, 9811723.
61. Berthoux L, Sebastian S, Sokolskaja E, Luban J. Lv1 inhibition of human immunodeficiency virus type 1 is counteracted by factors that stimulate synthesis or nuclear translocation of viral cDNA. J Virol 2004, 78:11739-11750. 10.1128/JVI.78.21.11739-11750.2004, 523245, 15479815.
62. He J, Chen Y, Farzan M, Choe H, Ohagen A, Gartner S, Busciglio J, Yang X, Hofmann W, Newman W, et al. CCR3 and CCR5 are co-receptors for HIV-1 infection of microglia. Nature 1997, 385:645-649. 10.1038/385645a0, 9024664.
63. Negre D, Mangeot PE, Duisit G, Blanchard S, Vidalain PO, Leissner P, Winter AJ, Rabourdin-Combe C, Mehtali M, Moullier P, et al. Characterization of novel safe lentiviral vectors derived from simian immunodeficiency virus (SIVmac251) that efficiently transduce mature human dendritic cells. Gene Ther 2000, 7:1613-1623. 10.1038/sj.gt.3301292, 11083469.
64. Zhang YJ, Hatziioannou T, Zang T, Braaten D, Luban J, Goff SP, Bieniasz PD. Envelope-dependent, cyclophilin-independent effects of glycosaminoglycans on human immunodeficiency virus type 1 attachment and infection. J Virol 2002, 76:6332-6343. 10.1128/JVI.76.12.6332-6343.2002, 136233, 12021366.
65. Mangeot PE, Duperrier K, Negre D, Boson B, Rigal D, Cosset FL, Darlix JL. High levels of transduction of human dendritic cells with optimized SIV vectors. Mol Ther 2002, 5:283-290. 10.1006/mthe.2002.0541, 11863418.
66. Kajaste-Rudnitski A, Marelli SS, Pultrone C, Pertel T, Uchil PD, Mechti N, Mothes W, Poli G, Luban J, Vicenzi E. TRIM22 inhibits HIV-1 transcription independently of its E3 ubiquitin ligase activity, Tat, and NF-kappaB-responsive long terminal repeat elements. J Virol 2011, 85:5183-5196. 10.1128/JVI.02302-10, 3126207, 21345949.
67. Pizzato M, Erlwein O, Bonsall D, Kaye S, Muir D, McClure MO. A one-step SYBR Green I-based product-enhanced reverse transcriptase assay for the quantitation of retroviruses in cell culture supernatants. J Virol Methods 2009, 156:1-7. 10.1016/j.jviromet.2008.10.012, 19022294.
68. Nikolic DS, Lehmann M, Felts R, Garcia E, Blanchet FP, Subramaniam S, Piguet V. HIV-1 activates Cdc42 and induces membrane extensions in immature dendritic cells to facilitate cell-to-cell virus propagation. Blood 2011, 118:4841-4852. 10.1182/blood-2010-09-305417, 3208294, 21562048.
69. Butler SL, Hansen MS, Bushman FD. A quantitative assay for HIV DNA integration in vivo. Nat Med 2001, 7:631-634. 10.1038/87979, 11329067.
70. Kappes JC, Parkin JS, Conway JA, Kim J, Brouillette CG, Shaw GM, Hahn BH. Intracellular transport and virion incorporation of vpx requires interaction with other virus type-specific components. Virology 1993, 193:222-233. 10.1006/viro.1993.1118, 8438567.
71. Simm M, Shahabuddin M, Chao W, Allan JS, Volsky DJ. Aberrant Gag protein composition of a human immunodeficiency virus type 1 vif mutant produced in primary lymphocytes. J Virol 1995, 69:4582-4586. 189210, 7769728.