Identification of Critical Regions in Human SAMHD1 Required for Nuclear Localization and Vpx-Mediated Degradation

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Guo, Haoran ^a,b   Wei, Wei ^a,b   Wei, Zhenhong ^a   Liu, Xianjun ^a   Evans, Sean L ^b   Yang, Weiming ^c   Wang, Hong ^a   Guo, Ying ^a   Zhao, Ke ^a   Zhou, Jian Ying ^c   Yu, Xiao Fang ^a,b  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

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

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; KARYOPHERIN BETA1; NUCLEAR PROTEIN; PROTEIN VPX; STERILE ALPHA MOTIF AND HD DOMAIN CONTAINING PROTEIN 1; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DELETION MUTANT; NUCLEAR LOCALIZATION SIGNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MULTIMERIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; STRUCTURE ANALYSIS; WILD TYPE;

BETA KARYOPHERINS; CELL LINE; CELL NUCLEUS; CYTOPLASM; HEK293 CELLS; HUMANS; MONOMERIC GTP-BINDING PROTEINS; MUTATION; NUCLEAR LOCALIZATION SIGNALS; NUCLEAR PROTEINS; PROTEIN TRANSPORT; PROTEOLYSIS; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 84880063164     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066201     Document Type: Article

References (49)

1. 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.
2. Yu XF, Ito S, Essex M, Lee TH, (1988) A naturally immunogenic virion-associated protein specific for HIV-2 and SIV. Nature 335: 262-265.
3. Selig L, Pages JC, Tanchou V, Preveral S, Berlioz-Torrent C, et al. (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.
4. 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.
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. 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.
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, et al. (1993) Intracellular transport and virion incorporation of vpx requires interaction with other virus type-specific components. Virology 193: 222-233.
9. Marcon L, Michaels F, Hattori N, Fargnoli K, Gallo RC, et al. (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. Mangeot PE, Duperrier K, Negre D, Boson B, Rigal D, et al. (2002) High levels of transduction of human dendritic cells with optimized SIV vectors. Mol Ther 5: 283-290.
12. Goujon C, Riviere L, Jarrosson-Wuilleme L, Bernaud J, Rigal D, et al. (2007) SIVSM/HIV-2 Vpx proteins promote retroviral escape from a proteasome-dependent restriction pathway present in human dendritic cells. Retrovirology 4: 2.
13. Sharova N, Wu Y, Zhu X, Stranska R, Kaushik R, et al. (2008) Primate lentiviral Vpx commandeers DDB1 to counteract a macrophage restriction. PLoS Pathog 4: e1000057.
14. Fujita M, Otsuka M, Miyoshi M, Khamsri B, Nomaguchi M, et al. (2008) Vpx is critical for reverse transcription of the human immunodeficiency virus type 2 genome in macrophages. J Virol 82: 7752-7756.
15. 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.
16. Srivastava S, Swanson SK, Manel N, Florens L, Washburn MP, et al. (2008) Lentiviral Vpx accessory factor targets VprBP/DCAF1 substrate adaptor for cullin 4 E3 ubiquitin ligase to enable macrophage infection. PLoS Pathog 4: e1000059.
17. Descours B, Cribier A, Chable-Bessia C, Ayinde D, Rice G, et al. (2012) SAMHD1 restricts HIV-1 reverse transcription in quiescent CD4(+) T-cells. Retrovirology 9: 87.
18. St Gelais C, de Silva S, Amie SM, Coleman CM, Hoy H, et al. (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.
19. Baldauf HM, Pan X, Erikson E, Schmidt S, Daddacha W, et al. (2012) SAMHD1 restricts HIV-1 infection in resting CD4(+) T cells. Nat Med 18: 1682-1687.
20. Laguette N, Rahm N, Sobhian B, Chable-Bessia C, Munch J, et al. (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.
21. Lahouassa H, Daddacha W, Hofmann H, Ayinde D, Logue EC, et al. (2012) SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat Immunol 13: 223-228.
22. Laguette N, Sobhian B, Casartelli N, Ringeard M, Chable-Bessia C, et al. (2011) SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474: 654-657.
23. Hrecka K, Hao C, Gierszewska M, Swanson SK, Kesik-Brodacka M, et al. (2011) Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474: 658-661.
24. Berger A, Sommer AF, Zwarg J, Hamdorf M, Welzel K, et al. (2011) SAMHD1-deficient CD14+ cells from individuals with Aicardi-Goutieres syndrome are highly susceptible to HIV-1 infection. PLoS Pathog 7: e1002425.
25. White TE, Brandariz-Nunez A, Carlos Valle-Casuso J, Amie S, Nguyen L, et al. (2012) Contribution of SAM and HD domains to retroviral restriction mediated by human SAMHD1. Virology.
26. 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.
27. Powell RD, Holland PJ, Hollis T, Perrino FW, (2011) Aicardi-Goutieres syndrome gene and HIV-1 restriction factor SAMHD1 is a dGTP-regulated deoxynucleotide triphosphohydrolase. J Biol Chem 286: 43596-43600.
28. Goldstone DC, Ennis-Adeniran V, Hedden JJ, Groom HC, Rice GI, et al. (2011) HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase. Nature 480: 379-382.
29. Ahn J, Hao C, Yan J, DeLucia M, Mehrens J, et al. (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.
30. Berger G, Turpin J, Cordeil S, Tartour K, Nguyen XN, et al. (2012) Functional analysis of the relationship between Vpx and the restriction factor SAMHD1. J Biol Chem 287: 41210-41217.
31. Wei W, Guo H, Han X, Liu X, Zhou X, et al. (2012) A novel DCAF1-binding motif required for Vpx-mediated degradation of nuclear SAMHD1 and Vpr-induced G2 arrest. Cell Microbiol 14: 1745-1756.
32. Brandariz-Nunez A, Valle-Casuso JC, White TE, Laguette N, Benkirane M, et al. (2012) Role of SAMHD1 nuclear localization in restriction of HIV-1 and SIVmac. Retrovirology 9: 49.
33. Ayinde D, Casartelli N, Schwartz O, (2012) Restricting HIV the SAMHD1 way: through nucleotide starvation. Nat Rev Microbiol 10: 675-680.
34. Hofmann H, Logue EC, Bloch N, Daddacha W, Polsky SB, et al. (2012) The Vpx lentiviral accessory protein targets SAMHD1 for degradation in the nucleus. J Virol 86: 12552-12560.
35. Laguette N, Benkirane M, (2012) How SAMHD1 changes our view of viral restriction. Trends Immunol 33: 26-33.
36. Cox J, Mann M, (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26: 1367-1372.
37. Yu X, Yu Y, Liu B, Luo K, Kong W, et al. (2003) Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302: 1056-1060.
38. 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.
39. Bi Y, Lv Z, Wang Y, Hai T, Huo R, et al. (2011) WDR82, a key epigenetics-related factor, plays a crucial role in normal early embryonic development in mice. Biol Reprod 84: 756-764.
40. Harris CA, Andryuk PJ, Cline SW, Mathew S, Siekierka JJ, et al. (1995) Structure and mapping of the human thymopoietin (TMPO) gene and relationship of human TMPO beta to rat lamin-associated polypeptide 2. Genomics 28: 198-205.
41. Andersen JS, Lam YW, Leung AK, Ong SE, Lyon CE, et al. (2005) Nucleolar proteome dynamics. Nature 433: 77-83.
42. Yan J, Kaur S, DeLucia M, Hao C, Mehrens J, et al. (2013) Tetramerization of SAMHD1 is required for biological activity and inhibition of HIV infection. J Biol Chem 288: 10406-10417.
43. Yan N, Lieberman J, (2012) SAMHD1 does it again, now in resting T cells. Nat Med 18: 1611-1612.
44. Zhang L, Saadatmand J, Li X, Guo F, Niu M, et al. (2008) Function analysis of sequences in human APOBEC3G involved in Vif-mediated degradation. Virology 370: 113-121.
45. Conticello SG, Harris RS, Neuberger MS, (2003) The Vif protein of HIV triggers degradation of the human antiretroviral DNA deaminase APOBEC3G. Curr Biol 13: 2009-2013.
46. Patenaude AM, Orthwein A, Hu Y, Campo VA, Kavli B, et al. (2009) Active nuclear import and cytoplasmic retention of activation-induced deaminase. Nat Struct Mol Biol 16: 517-527.
47. Freitas N, Cunha C, (2009) Mechanisms and signals for the nuclear import of proteins. Curr Genomics 10: 550-557.
48. Dirk Görlich UK, (1999) Transport between the cell nucleus and the cytoplasm. Annual Review of Cell and Developmental Biology Vol. 15: 607-660.
49. Macara IG (2001) Transport into and out of the Nucleus. Microbiol Mol Biol Rev vol. 65 570-594.