Variation of two primate lineage-specific residues in human SAMHD1 confers resistance to N terminus-targeted SIV Vpx proteins

Journal of Virology

Volumn 88, Issue 1, 2014, Pages 583-591

  Wei, Wei ^a,c,d   Guo, Haoran ^a,c,d   Gao, Qimeng ^c   Markham, Richard ^c   Yua, Xiao Fang ^b,c,d  

^a TIANJIN UNIVERSITY   (China)

^b THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^d SynBio Research Platform   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; PROTEIN VPX; STERILE ALPHA MOTIF AND HD DOMAIN CONTAINING PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; APE; ARTICLE; CERCOPITHECIDAE; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; HUMAN VERSUS ANIMAL COMPARISON; MOLECULAR RECOGNITION; NONHUMAN; PRIMATE; PRIORITY JOURNAL; PROTEIN TARGETING; RESIDUE ANALYSIS; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; SPECIES DIFFERENCE; VIRUS STRAIN;

AMINO ACID SEQUENCE; ANIMALS; HEK293 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MONOMERIC GTP-BINDING PROTEINS; PHYLOGENY; PRIMATES; RNA INTERFERENCE; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 84890888389     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02866-13     Document Type: Article

References (48)

1. Accola MA, Bukovsky AA, Jones MS, Gottlinger HG. 1999. A conserved dileucine-containing motif in p6(gag) governs the particle association of Vpx and Vpr of simian immunodeficiency viruses SIV(mac) and SIV(agm). J. Virol. 73:9992-9999.
2. Henderson LE, Sowder RC, Copeland TD, Benveniste RE, Oroszlan S. 1988. Isolation and characterization of a novel protein (X-ORF product) from SIV and HIV-2. Science 241:199-201. http://dx.doi.org/10.1126/science.3388031.
3. Paxton W, Connor RI, Landau NR. 1993. Incorporation of Vpr into human immunodeficiency virus type 1 virions: requirement for the p6 region of gag and mutational analysis. J. Virol. 67:7229-7237.
4. Selig L, Pages JC, Tanchou V, Preveral S, Berlioz-Torrent C, Liu LX, Erdtmann L, Darlix J, Benarous R, Benichou S. 1999. Interaction with the p6 domain of the gag precursor mediates incorporation into virions of Vpr and Vpx proteins from primate lentiviruses. J. Virol. 73:592-600.
5. Wu X, Conway JA, Kim J, Kappes JC. 1994. Localization of the Vpx packaging signal within the C terminus of the human immunodeficiency virus type 2 Gag precursor protein. J. Virol. 68:6161-6169.
6. Yu XF, Ito S, Essex M, Lee TH. 1988. A naturally immunogenic virionassociated protein specific for HIV-2 and SIV. Nature 335:262-265. http://dx.doi.org/10.1038/335262a0.
7. Guyader M, Emerman M, Montagnier L, Peden K. 1989. VPX mutants of HIV-2 are infectious in established cell lines but display a severe defect in peripheral blood lymphocytes. EMBO J. 8:1169-1175.
8. Kappes JC, Parkin JS, Conway JA, Kim J, Brouillette CG, Shaw GM, Hahn BH. 1993. Intracellular transport and virion incorporation of vpx requires interaction with other virus type-specific components. Virology 193:222-233. http://dx.doi.org/10.1006/viro.1993.1118.
9. Marcon L, Michaels F, Hattori N, Fargnoli K, Gallo RC, Franchini G. 1991. Dispensable role of the human immunodeficiency virus type 2 Vpx protein in viral replication. J. Virol. 65:3938-3942.
10. Yu XF, Yu QC, Essex M, Lee TH. 1991. The vpx gene of simian immunodeficiency virus facilitates efficient viral replication in fresh lymphocytes and macrophage. J. Virol. 65:5088-5091.
11. Goujon C, Riviere L, Jarrosson-Wuilleme L, Bernaud J, Rigal D, Darlix JL, Cimarelli A. 2007. SIVSM/HIV-2 Vpx proteins promote retroviral escape from a proteasome-dependent restriction pathway present in human dendritic cells. Retrovirology 4:2. http://dx.doi.org/10.1186/1742-4690-4-2.
12. Mangeot PE, Duperrier K, Negre D, Boson B, Rigal D, Cosset FL, Darlix JL. 2002. High levels of transduction of human dendritic cells with optimized SIV vectors. Mol. Ther. 5:283-290. http://dx.doi.org/10.1006/mthe.2002.0541.
13. Fujita M, Otsuka M, Miyoshi M, Khamsri B, Nomaguchi M, Adachi A. 2008. Vpx is critical for reverse transcription of the human immunodeficiency virus type 2 genome in macrophages. J. Virol. 82:7752-7756. http://dx.doi.org/10.1128/JVI.01003-07.
14. Gramberg T, Sunseri N, Landau NR. 2010. Evidence for an activation domain at the amino terminus of simian immunodeficiency virus Vpx. J. Virol. 84:1387-1396. http://dx.doi.org/10.1128/JVI.01437-09.
15. 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. http://dx.doi.org/10 .1371/journal.ppat.1000057.
16. Srivastava S, Swanson SK, Manel N, Florens L, Washburn MP, Skowronski J. 2008. Lentiviral Vpx accessory factor targets VprBP/DCAF1 substrate adaptor for cullin 4 E3 ubiquitin ligase to enable macrophage infection. PLoS Pathog. 4:e1000059. http://dx.doi.org/10.1371/journal .ppat.1000059.
17. 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.
18. 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. http://dx.doi.org/10 .1371/journal.ppat.1002425.
19. 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.
20. 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.
21. Laguette N, Rahm N, Sobhian B, Chable-Bessia C, Munch J, Snoeck J, Sauter D, Switzer WM, Heneine W, Kirchhoff F, Delsuc F, Telenti A, Benkirane M. 2012. Evolutionary and functional analyses of the interaction between the myeloid restriction factor SAMHD1 and the lentiviral Vpx protein. Cell Host Microbe 11:205-217. http://dx.doi.org/10.1016/j .chom.2012.01.007.
22. 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.
23. 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/nrg3215.
24. + T-lymphocytes cannot be upregulated by interferons. Retrovirology 9:105. http://dx.doi.org/10.1186/1742-4690-9-105.
25. Zhao K, Du J, Han X, Goodier JL, Li P, Zhou X, Wei W, Evans SL, Li L, Zhang W, Cheung LE, Wang G, Kazazian HH, Jr, Yu XF. 2013. Modulation of LINE-1 and Alu/SVA retrotransposition by Aicardi-Goutieres syndrome-related SAMHD1. Cell Rep. 4:1108-1115. http://dx .doi.org/10.1016/j.celrep.2013.08.019.
26. 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. http://dx.doi.org/10.1038/nature10623.
27. 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.
28. 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. http://dx.doi.org/10.1074/jbc.C111.317628.
29. White TE, Brandariz-Nuñez A, Carlos Valle-Casuso J, Amie S, Nguyen L, Kim B, Brojatsch J, Diaz-Griffero F. 2013. Contribution of SAM and HD domains to retroviral restriction mediated by human SAMHD1. Virology 436:81-90. http://dx.doi.org/10.1016/j.virol.2012.10.029.
30. Yan J, Kaur S, DeLucia M, Hao C, Mehrens J, Wang C, Golczak M, Palczewski K, Gronenborn AM, Ahn J, Skowronski J. 2013. Tetramerization of SAMHD1 is required for biological activity and inhibition of HIV infection. J. Biol. Chem. 288:10406-10417. http://dx.doi.org/10 .1074/jbc.M112.443796.
31. Zhu Chunfeng GW, Zhao Ke Qing Xiaohong Zhang Yinjie Peng Xin Zhang Lei Dong Yuhui Zhang Wenyan Li Peng Wei Wei Gong Yong Yu Xiao-Fang. 2013. Structural insight into dGTP-dependent activation of tetramericSAMHD1deoxynucleoside triphosphate triphosphohydrolase. Nat. Commun. 4:2722.
32. Cribier A, Descours B, Valadao AL, Laguette N, Benkirane M. 2013. Phosphorylation of SAMHD1 by cyclin A2/CDK1 regulates its restriction activity toward HIV-1. Cell Rep. 3:1036-1043. http://dx.doi.org/10.1016/j.celrep.2013.03.017.
33. Welbourn S, Dutta SM, Semmes OJ, Strebel K. 2013. Restriction of virus infection but not catalytic dNTPase activity is regulated by phosphorylation of SAMHD1. J. Virol. 87:11516-11524. http://dx.doi.org/10.1128/JVI.01642-13.
34. White TE, Brandariz-Nuñez A, Valle-Casuso JC, Amie S, Nguyen LA, Kim B, Tuzova M, Diaz-Griffero F. 2013. The retroviral restriction ability of SAMHD1, but not its deoxynucleotide triphosphohydrolase activity, is regulated by phosphorylation. Cell Host Microbe 13:441-451. http://dx.doi.org/10.1016/j.chom.2013.03.005.
35. Ahn J, Hao C, Yan J, DeLucia M, Mehrens J, Wang C, Gronenborn AM, Skowronski J. 2012. 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. 287:12550-12558. http://dx.doi.org/10.1074/jbc.M112.340711.
36. 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.
37. Berger G, Turpin J, Cordeil S, Tartour K, Nguyen XN, Mahieux R, Cimarelli A. 2012. Functional analysis of the relationship between Vpx and the restriction factor SAMHD1. J. Biol. Chem. 287:41210-41217. http://dx.doi.org/10.1074/jbc.M112.403816.
38. Brandariz-Nuñez 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. http://dx .doi.org/10.1186/1742-4690-9-49.
39. Hofmann H, Logue EC, Bloch N, Daddacha W, Polsky SB, Schultz ML, Kim B, Landau NR. 2012. The Vpx lentiviral accessory protein targets SAMHD1 for degradation in the nucleus. J. Virol. 86:12552-12560. http://dx.doi.org/10.1186/1742-4690-9-49.
40. Laguette N, Benkirane M. 2012. How SAMHD1 changes our view of viral restriction. Trends Immunol. 33:26-33. http://dx.doi.org/10.1016/j.it .2011.11.002.
41. Wei W, Guo H, Han X, Liu X, Zhou X, Zhang W, Yu XF. 2012. A novel DCAF1-binding motif required for Vpx-mediated degradation of nuclear SAMHD1and Vpr-inducedG2 arrest. Cell Microbiol. 14:1745-1756. http://dx.doi.org/10.1111/j.1462-5822.2012.01835.x.
42. Fregoso OI, Ahn J, Wang C, Mehrens J, Skowronski J, Emerman M. 2013. Evolutionary toggling of Vpx/Vpr specificity results in divergent recognition of the restriction factor SAMHD1. PLoS Pathog. 9:e1003496. http://dx.doi.org/10.1371/journal.ppat.1003496.
43. 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. http://dx.doi.org/10.1371/journal.ppat .1003496.
44. Zhang C, de Silva S, Wang JH, Wu L. 2012. Co-evolution of primate SAMHD1 and lentivirus Vpx leads to the loss of the vpx gene in HIV-1 ancestor. PLoS One 7:e37477. http://dx.doi.org/10.1371/journal.pone .0037477.
45. Guo H, Wei W, Wei Z, Liu X, Evans SL, Yang W, Wang H, Guo Y, Zhao K, Zhou JY, Yu XF. 2013. Identification of critical regions in human SAMHD1 required for nuclear localization and Vpx-mediated degradation. PLoS One 8(7):e66201. http://dx.doi.org/10.1371/journal.pone .0066201.
46. Zhang W, Du J, Evans SL, Yu Y, Yu XF. 2012. T-cell differentiation factor CBF-beta regulates HIV-1 Vif-mediated evasion of host restriction. Nature 481:376-379. http://dx.doi.org/10.1016/j.chom.2012.01.004.
47. Guo H, Wei W, Wei Z, Liu X, Evans SL, Yang W, Wang H, Guo Y, Zhao K, Zhou JY, Yu XF. 2013. Identification of critical regions in human SAMHD1 required for nuclear localization and Vpx-mediated degradation. PLoS One 8:e66201. http://dx.doi.org/10.1371/journal.pone .0066201.
48. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599. http://dx.doi.org/10.1093/molbev/msm092.