The retroviral restriction ability of SAMHD1, but not its deoxynucleotide triphosphohydrolase activity, is regulated by phosphorylation

Cell Host and Microbe

Volumn 13, Issue 4, 2013, Pages 441-451

  White, Tommy E ^a   Brandariz Nuñez, Alberto ^a   Valle Casuso, Jose Carlos ^a   Amie, Sarah ^b   Nguyen, Laura Anh ^b   Kim, Baek ^b   Tuzova, Marina ^a   Diaz Griffero, Felipe ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

CELL ENZYME; CYCLIN DEPENDENT KINASE 1; DEOXYNUCLEOTIDE TRIPHOSPHOHYDROLASE; DEOXYRIBONUCLEOTIDE; HYDROLASE; SAMHD1 PROTEIN; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MONOCYTE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RETROVIRUS; RETROVIRUS INFECTION; VIRAL GENETICS; VIRUS CELL INTERACTION; VIRUS STRAIN;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84876369203     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2013.03.005     Document Type: Article

References (44)

1. J. Ahn, C. Hao, J. Yan, M. DeLucia, J. Mehrens, C. Wang, A.M. Gronenborn, and J. Skowronski 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 2012 12550 12558
2. V. Arfi, L. Rivière, L. Jarrosson-Wuillème, C. Goujon, D. Rigal, J.L. Darlix, and A. Cimarelli Characterization of the early steps of infection of primary blood monocytes by human immunodeficiency virus type 1 J. Virol. 82 2008 6557 6565
3. H.M. Baldauf, X. Pan, E. Erikson, S. Schmidt, W. Daddacha, M. Burggraf, K. Schenkova, I. Ambiel, G. Wabnitz, and T. Gramberg SAMHD1 restricts HIV-1 infection in resting CD4(+) T cells Nat. Med. 18 2012 1682 1687
4. N. Beloglazova, R. Flick, A. Tchigvintsev, G. Brown, A. Popovic, B. Nocek, and A.F. Yakunin Nuclease Activity of the Human SAMHD1 Protein Implicated in the Aicardi-Goutieres Syndrome and HIV-1 Restriction J. Biol. Chem. 288 2013 8101 8110
5. M. Belshan, L.A. Mahnke, and L. Ratner Conserved amino acids of the human immunodeficiency virus type 2 Vpx nuclear localization signal are critical for nuclear targeting of the viral preintegration complex in non-dividing cells Virology 346 2006 118 126
6. A. Bergamaschi, D. Ayinde, A. David, E. Le Rouzic, M. Morel, G. Collin, D. Descamps, F. Damond, F. Brun-Vezinet, and S. Nisole The human immunodeficiency virus type 2 Vpx protein usurps the CUL4A-DDB1 DCAF1 ubiquitin ligase to overcome a postentry block in macrophage infection J. Virol. 83 2009 4854 4860
7. A. Berger, A.F. Sommer, J. Zwarg, M. Hamdorf, K. Welzel, N. Esly, S. Panitz, A. Reuter, I. Ramos, and A. Jatiani SAMHD1-deficient CD14+ cells from individuals with Aicardi-Goutières syndrome are highly susceptible to HIV-1 infection PLoS Pathog. 7 2011 e1002425
8. J.D. Blethrow, J.S. Glavy, D.O. Morgan, and K.M. Shokat Covalent capture of kinase-specific phosphopeptides reveals Cdk1-cyclin B substrates Proc. Natl. Acad. Sci. USA 105 2008 1442 1447
9. A. Brandariz-Nuñez, J.C. Valle-Casuso, T.E. White, N. Laguette, M. Benkirane, J. Brojatsch, and F. Diaz-Griffero Role of SAMHD1 nuclear localization in restriction of HIV-1 and SIVmac Retrovirology 9 2012 49
10. H.C. Cheng, R.Z. Qi, H. Paudel, and H.J. Zhu Regulation and function of protein kinases and phosphatases Enzyme Res. 2011 2011 794089
11. B. Descours, A. Cribier, C. Chable-Bessia, D. Ayinde, G. Rice, Y. Crow, A. Yatim, O. Schwartz, N. Laguette, and M. Benkirane SAMHD1 restricts HIV-1 reverse transcription in quiescent CD4(+) T-cells Retrovirology 9 2012 87
12. F. Diaz-Griffero, M. Perron, K. McGee-Estrada, R. Hanna, P.V. Maillard, D. Trono, and J. Sodroski A human TRIM5alpha B30.2/SPRY domain mutant gains the ability to restrict and prematurely uncoat B-tropic murine leukemia virus Virology 378 2008 233 242
13. A. Errico, K. Deshmukh, Y. Tanaka, A. Pozniakovsky, and T. Hunt Identification of substrates for cyclin dependent kinases Adv. Enzyme Regul. 50 2010 375 399
14. T.M. Fletcher 3rd, B. Brichacek, N. Sharova, M.A. Newman, G. Stivahtis, P.M. Sharp, M. Emerman, B.H. Hahn, and M. Stevenson Nuclear import and cell cycle arrest functions of the HIV-1 Vpr protein are encoded by two separate genes in HIV-2/SIV(SM) EMBO J. 15 1996 6155 6165
15. M. Fujita, M. Otsuka, M. Miyoshi, B. Khamsri, M. Nomaguchi, and A. Adachi Vpx is critical for reverse transcription of the human immunodeficiency virus type 2 genome in macrophages J. Virol. 82 2008 7752 7756
16. J.S. Gibbs, A.A. Lackner, S.M. Lang, M.A. Simon, P.K. Sehgal, M.D. Daniel, and R.C. Desrosiers Progression to AIDS in the absence of a gene for vpr or vpx J. Virol. 69 1995 2378 2383
17. D.C. Goldstone, V. Ennis-Adeniran, J.J. Hedden, H.C. Groom, G.I. Rice, E. Christodoulou, P.A. Walker, G. Kelly, L.F. Haire, and M.W. Yap HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase Nature 480 2011 379 382
18. A. Goncalves, E. Karayel, G.I. Rice, K.L. Bennett, Y.J. Crow, G. Superti-Furga, and T. Bürckstümmer SAMHD1 is a nucleic-acid binding protein that is mislocalized due to aicardi-goutières syndrome-associated mutations Hum. Mutat. 33 2012 1116 1122
19. C. Goujon, L. Jarrosson-Wuilleme, J. Bernaud, D. Rigal, J.L. Darlix, and A. Cimarelli Heterologous human immunodeficiency virus type 1 lentiviral vectors packaging a simian immunodeficiency virus-derived genome display a specific postentry transduction defect in dendritic cells J. Virol. 77 2003 9295 9304
20. C. Goujon, L. Rivière, L. Jarrosson-Wuilleme, J. Bernaud, D. Rigal, J.L. Darlix, and A. Cimarelli SIVSM/HIV-2 Vpx proteins promote retroviral escape from a proteasome-dependent restriction pathway present in human dendritic cells Retrovirology 4 2007 2
21. C. Goujon, V. Arfi, T. Pertel, J. Luban, J. Lienard, D. Rigal, J.L. Darlix, and A. Cimarelli Characterization of simian immunodeficiency virus SIVSM/human immunodeficiency virus type 2 Vpx function in human myeloid cells J. Virol. 82 2008 12335 12345
22. R. Hass, H. Gunji, R. Datta, S. Kharbanda, A. Hartmann, R. Weichselbaum, and D. Kufe Differentiation and retrodifferentiation of human myeloid leukemia cells is associated with reversible induction of cell cycle-regulatory genes Cancer Res. 52 1992 1445 1450
23. V.M. Hirsch, M.E. Sharkey, C.R. Brown, B. Brichacek, S. Goldstein, J. Wakefield, R. Byrum, W.R. Elkins, B.H. Hahn, J.D. Lifson, and M. Stevenson Vpx is required for dissemination and pathogenesis of SIV(SM) PBj: evidence of macrophage-dependent viral amplification Nat. Med. 4 1998 1401 1408
24. K. Hrecka, C. Hao, M. Gierszewska, S.K. Swanson, M. Kesik-Brodacka, S. Srivastava, L. Florens, M.P. Washburn, and J. Skowronski Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein Nature 474 2011 658 661
25. L. Jin, Y. Zhou, and L. Ratner HIV type 2 Vpx interaction with Gag and incorporation into virus-like particles AIDS Res. Hum. Retroviruses 17 2001 105 111
26. J.C. Kappes, J.S. Parkin, J.A. Conway, J. Kim, C.G. Brouillette, G.M. Shaw, and B.H. Hahn Intracellular transport and virion incorporation of vpx requires interaction with other virus type-specific components Virology 193 1993 222 233
27. R. Kaushik, X. Zhu, R. Stranska, Y. Wu, and M. Stevenson A cellular restriction dictates the permissivity of nondividing monocytes/macrophages to lentivirus and gammaretrovirus infection Cell Host Microbe 6 2009 68 80
28. M.O. Kim, D.O. Moon, Y.H. Choi, J.D. Lee, N.D. Kim, and G.Y. Kim Platycodin D induces mitotic arrest in vitro, leading to endoreduplication, inhibition of proliferation and apoptosis in leukemia cells Int. J. Cancer 122 2008 2674 2681
29. B. Kim, L.A. Nguyen, W. Daddacha, and J.A. Hollenbaugh 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 2012 21570 21574
30. E. Kinoshita, E. Kinoshita-Kikuta, K. Takiyama, and T. Koike Phosphate-binding tag, a new tool to visualize phosphorylated proteins Mol. Cell. Proteomics 5 2006 749 757
31. N. Laguette, B. Sobhian, N. Casartelli, M. Ringeard, C. Chable-Bessia, E. Ségéral, A. Yatim, S. Emiliani, O. Schwartz, and M. Benkirane SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx Nature 474 2011 654 657
32. N. Laguette, N. Rahm, B. Sobhian, C. Chable-Bessia, J. Münch, J. Snoeck, D. Sauter, W.M. Switzer, W. Heneine, and F. Kirchhoff Evolutionary and functional analyses of the interaction between the myeloid restriction factor SAMHD1 and the lentiviral Vpx protein Cell Host Microbe 11 2012 205 217
33. H. Lahouassa, W. Daddacha, H. Hofmann, D. Ayinde, E.C. Logue, L. Dragin, N. Bloch, C. Maudet, M. Bertrand, and T. Gramberg SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates Nat. Immunol. 13 2012 223 228
34. E.S. Lim, O.I. Fregoso, C.O. McCoy, F.A. Matsen, H.S. Malik, and M. Emerman The ability of primate lentiviruses to degrade the monocyte restriction factor SAMHD1 preceded the birth of the viral accessory protein Vpx Cell Host Microbe 11 2012 194 204
35. I.W. Park, and J. Sodroski Amino acid sequence requirements for the incorporation of the Vpx protein of simian immunodeficiency virus into virion particles J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 10 1995 506 510
36. R.D. Powell, P.J. Holland, T. Hollis, and F.W. Perrino Aicardi-Goutieres syndrome gene and HIV-1 restriction factor SAMHD1 is a dGTP-regulated deoxynucleotide triphosphohydrolase J. Biol. Chem. 286 2011 43596 43600
37. H. Schwende, E. Fitzke, P. Ambs, and P. Dieter Differences in the state of differentiation of THP-1 cells induced by phorbol ester and 1,25-dihydroxyvitamin D3 J. Leukoc. Biol. 59 1996 555 561
38. L. Selig, J.C. Pages, V. Tanchou, S. Prévéral, C. Berlioz-Torrent, L.X. Liu, L. Erdtmann, J. Darlix, R. Benarous, and S. Benichou Interaction with the p6 domain of the gag precursor mediates incorporation into virions of Vpr and Vpx proteins from primate lentiviruses J. Virol. 73 1999 592 600
39. S. Srivastava, S.K. Swanson, N. Manel, L. Florens, M.P. Washburn, and J. Skowronski Lentiviral Vpx accessory factor targets VprBP/DCAF1 substrate adaptor for cullin 4 E3 ubiquitin ligase to enable macrophage infection PLoS Pathog. 4 2008 e1000059
40. N. Sunseri, M. O'Brien, N. Bhardwaj, and N.R. Landau Human immunodeficiency virus type 1 modified to package Simian immunodeficiency virus Vpx efficiently infects macrophages and dendritic cells J. Virol. 85 2011 6263 6274
41. K. Traore, M.A. Trush, M. George Jr., E.W. Spannhake, W. Anderson, and A. Asseffa Signal transduction of phorbol 12-myristate 13-acetate (PMA)-induced growth inhibition of human monocytic leukemia THP-1 cells is reactive oxygen dependent Leuk. Res. 29 2005 863 879
42. S. van den Heuvel, and E. Harlow Distinct roles for cyclin-dependent kinases in cell cycle control Science 262 1993 2050 2054
43. T.E. White, A. Brandariz-Nuñez, J. Carlos Valle-Casuso, S. Amie, L. Nguyen, B. Kim, J. Brojatsch, and F. Diaz-Griffero Contribution of SAM and HD domains to retroviral restriction mediated by human SAMHD1 Virology 436 2013 81 90
44. C. Zhang, S. de Silva, J.H. Wang, and L. Wu Co-evolution of primate SAMHD1 and lentivirus Vpx leads to the loss of the vpx gene in HIV-1 ancestor PLoS ONE 7 2012 e37477