Effects of human SAMHD1 polymorphisms on HIV-1 susceptibility

Virology

Volumn 460-461, Issue 1, 2014, Pages 34-44

  White, Tommy E ^a   Brandariz Nuñez, Alberto ^a   Valle Casuso, Jose Carlos ^a   Knowlton, Caitlin ^b   Kim, Baek ^b   Sawyer, Sara L ^c   Diaz Griffero, Felipe ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

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

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

DNTPs; HIV 1; LINE 1; SAMHD1; SNPs; Vpx

Indexed keywords

PROTEIN VPX; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BIODEGRADATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EQUINE INFECTIOUS ANEMIA VIRUS; GENE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; LONG INTERSPERSED REPEAT; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; RETROPOSON; SAMHD1 GENE; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES DIFFERENTIATION;

DNTPS; HIV-1; LINE-1; SAMHD1; SNPS; VPX;

ANIMALS; DEOXYRIBONUCLEOTIDES; HIV INFECTIONS; HIV-1; HIV-2; HUMANS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MONOMERIC GTP-BINDING PROTEINS; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84901447156     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.04.023     Document Type: Article

References (58)

1. Ahn J., Hao C., Yan J., DeLucia M., Mehrens J., Wang C., Gronenborn A.M., 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.
2. Arfi V., Riviere L., Jarrosson-Wuilleme L., Goujon C., Rigal D., Darlix J.L., Cimarelli A. Characterization of the early steps of infection of primary blood monocytes by human immunodeficiency virus type 1. J. Virol. 2008, 82:6557-6565.
3. Baldauf H.M., Pan X., Erikson E., Schmidt S., Daddacha W., Burggraf M., Schenkova K., Ambiel I., Wabnitz G., Gramberg T., Panitz S., Flory E., Landau N.R., Sertel S., Rutsch F., Lasitschka F., Kim B., Konig R., Fackler O.T., Keppler O.T. SAMHD1 restricts HIV-1 infection in resting CD4(+) T cells. Nat. Med 2012, 18(11):1682-1687.
4. Belshan M., Mahnke L.A., Ratner L. 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 2006, 346:118-126.
5. Bergamaschi A., Ayinde D., David A., Le Rouzic E., Morel M., Collin G., Descamps D., Damond F., Brun-Vezinet F., Nisole S., Margottin-Goguet F., Pancino G., Transy C. 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. 2009, 83:4854-4860.
6. Berger A., Sommer A.F., Zwarg J., Hamdorf M., Welzel K., Esly N., Panitz S., Reuter A., Ramos I., Jatiani A., Mulder L.C., Fernandez-Sesma A., Rutsch F., Simon V., Konig R., Flory E. SAMHD1-deficient CD14+ cells from individuals with Aicardi-Goutieres syndrome are highly susceptible to HIV-1 infection. PLoS Pathog. 2011, 7:e1002425.
7. Brandariz-Nunez A., Valle-Casuso J.C., White T.E., Laguette N., Benkirane M., Brojatsch J., Diaz-Griffero F. Role of SAMHD1 nuclear localization in restriction of HIV-1 and SIVmac. Retrovirology 2012, 9:49.
8. Brandariz-Nunez A., Valle-Casuso J.C., White T.E., Nguyen L., Bhattacharya A., Wang Z., Demeler B., Amie S., Knowlton C., Kim B., Ivanov D.N., Diaz-Griffero F. Contribution of oligomerization to the anti-HIV-1 properties of SAMHD1. Retrovirology 2013, 10:131.
9. Cribier A., Descours B., Valadao A.L., Laguette N., Benkirane M. Phosphorylation of SAMHD1 by cyclin A2/CDK1 regulates its restriction activity toward HIV-1. Cell Rep. 2013, 3:1036-1043.
10. 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.
11. Diaz-Griffero F., Hoschander S.A., Brojatsch J. Endocytosis is a critical step in entry of subgroup B avian leukosis viruses. J. Virol. 2002, 76:12866-12876.
12. Diaz-Griffero F., Perron M., McGee-Estrada K., Hanna R., Maillard P.V., Trono D., Sodroski J. A human TRIM5alpha B30.2/SPRY domain mutant gains the ability to restrict and prematurely uncoat B-tropic murine leukemia virus. Virology 2008, 378:233-242.
13. Fletcher T.M., Brichacek B., Sharova N., Newman M.A., Stivahtis G., Sharp P.M., Emerman M., Hahn B.H., Stevenson M. 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. 1996, 15:6155-6165.
14. Fregoso O.I., 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.
15. 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.
16. Gibbs J.S., Lackner A.A., Lang S.M., Simon M.A., Sehgal P.K., Daniel M.D., Desrosiers R.C. Progression to AIDS in the absence of a gene for Vpr or Vpx. J. Virol. 1995, 69:2378-2383.
17. Goldstone D.C., Ennis-Adeniran V., Hedden J.J., Groom H.C., Rice G.I., Christodoulou E., Walker P.A., Kelly G., Haire L.F., Yap M.W., de Carvalho L.P., Stoye J.P., Crow Y.J., Taylor I.A., Webb M. HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase. Nature 2011, 480:379-382.
18. Goncalves A., Karayel E., Rice G.I., Bennett K.L., Crow Y.J., Superti-Furga G., Burckstummer T. SAMHD1 is a nucleic-acid binding protein that is mislocalized due to Aicardi-Goutieres syndrome-associated mutations. Hum. Mutat 2012, 33(7):1116-1122.
19. Goodier J.L., Cheung L.E., Kazazian H.H. Mapping the LINE1 ORF1 protein interactome reveals associated inhibitors of human retrotransposition. Nucleic Acids Res. 2013, 41:7401-7419.
20. Goujon C., Arfi V., Pertel T., Luban J., Lienard J., Rigal D., Darlix J.L., 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.
21. Goujon C., Jarrosson-Wuilleme L., Bernaud J., Rigal D., Darlix J.L., Cimarelli A. 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. 2003, 77:9295-9304.
22. Goujon C., Riviere L., Jarrosson-Wuilleme L., Bernaud J., Rigal D., Darlix J.L., 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.
23. Hirsch V.M., Sharkey M.E., Brown C.R., Brichacek B., Goldstein S., Wakefield J., Byrum R., Elkins W.R., Hahn B.H., Lifson J.D., 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.
24. Hofmann H., Logue E.C., Bloch N., Daddacha W., Polsky S.B., Schultz M.L., Kim B., Landau N.R. The Vpx lentiviral accessory protein targets SAMHD1 for degradation in the nucleus. J. Virol 2012, 86(23):12552-12560.
25. Hrecka K., Hao C., Gierszewska M., Swanson S.K., Kesik-Brodacka M., Srivastava S., Florens L., Washburn M.P., Skowronski J. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 2011, 474:658-661.
26. Ji X., Wu Y., Yan J., Mehrens J., Yang H., DeLucia M., Hao C., Gronenborn A.M., Skowronski J., Ahn J., Xiong Y. Mechanism of allosteric activation of SAMHD1 by dGTP. Nat. Struct. Mol. Biol. 2013, 20:1304-1309.
27. 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.
28. Johnson W.E., Sawyer S.L. Molecular evolution of the antiretroviral TRIM5 gene. Immunogenetics 2009, 61:163-176.
29. Kappes J.C., Parkin J.S., Conway J.A., Kim J., Brouillette C.G., Shaw G.M., Hahn B.H. Intracellular transport and virion incorporation of Vpx requires interaction with other virus type-specific components. Virology 1993, 193:222-233.
30. Kaushik R., Zhu X., Stranska R., Wu Y., Stevenson M. A cellular restriction dictates the permissivity of nondividing monocytes/macrophages to lentivirus and gammaretrovirus infection. Cell Host Microbe 2009, 6:68-80.
31. Kim B., Nguyen L.A., Daddacha W., Hollenbaugh J.A. 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.
32. Laguette N., Rahm N., Sobhian B., Chable-Bessia C., Munch J., Snoeck J., Sauter D., Switzer W.M., Heneine W., Kirchhoff F., Delsuc F., Telenti A., Benkirane M. Evolutionary and functional analyses of the interaction between the myeloid restriction factor SAMHD1 and the lentiviral Vpx protein. Cell Host Microbe 2012, 11:205-217.
33. 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.
34. Lahouassa H., Daddacha W., Hofmann H., Ayinde D., Logue E.C., Dragin L., Bloch N., Maudet C., Bertrand M., Gramberg T., Pancino G., Priet S., Canard B., Laguette N., Benkirane M., Transy C., Landau N.R., Kim B., Margottin-Goguet F. SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat. Immunol. 2012, 13:621.
35. Lienlaf M., Hayashi F., Di Nunzio F., Tochio N., Kigawa T., Yokoyama S., Diaz-Griffero F. Contribution of E3-ubiquitin ligase activity to HIV-1 restriction by TRIM5alpha(rh): structure of the RING domain of TRIM5alpha. J. Virol. 2011, 85:8725-8737.
36. Lim E.S., Fregoso O.I., McCoy C.O., Matsen F.A., Malik H.S., 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.
37. Meyerson N.R., Sawyer S.L. Two-stepping through time: mammals and viruses. Trends Microbiol. 2011, 19:286-294.
38. Moran J.V., Holmes S.E., Naas T.P., DeBerardinis R.J., Boeke J.D., Kazazian H.H. High frequency retrotransposition in cultured mammalian cells. Cell 1996, 87:917-927.
39. Park I.W., Sodroski J. 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. 1995, 10:506-510.
40. Powell R.D., Holland P.J., Hollis T., Perrino F.W. Aicardi-Goutieres syndrome gene and HIV-1 restriction factor SAMHD1 is a dGTP-regulated deoxynucleotide triphosphohydrolase. J. Biol. Chem. 2011, 286:43596-43600.
41. Rice G.I., Bond J., Asipu A., Brunette R.L., Manfield I.W., Carr I.M., Fuller J.C., Jackson R.M., Lamb T., Briggs T.A., Ali M., Gornall H., Couthard L.R., Aeby A., Attard-Montalto S.P., Bertini E., Bodemer C., Brockmann K., Brueton L.A., Corry P.C., Desguerre I., Fazzi E., Cazorla A.G., Gener B., Hamel B.C., Heiberg A., Hunter M., van der Knaap M.S., Kumar R., Lagae L., Landrieu P.G., Lourenco C.M., Marom D., McDermott M.F., van der Merwe W., Orcesi S., Prendiville J.S., Rasmussen M., Shalev S.A., Soler D.M., Shinawi M., Spiegel R., Tan T.Y., Vanderver A., Wakeling E.L., Wassmer E., Whittaker E., Lebon P., Stetson D.B., Bonthron D.T., Crow Y.J. Mutations involved in Aicardi-Goutieres syndrome implicate SAMHD1 as regulator of the innate immune response. Nat. Genet. 2009, 41:829-832.
42. Schwende H., Fitzke E., Ambs P., Dieter P. Differences in the state of differentiation of THP-1 cells induced by phorbol ester and 1,25-dihydroxyvitamin D3. J. Leukoc. Biol. 1996, 59:555-561.
43. Selig L., Pages J.C., Tanchou V., Preveral S., Berlioz-Torrent C., Liu L.X., Erdtmann L., Darlix J., Benarous R., Benichou S. Interaction with the p6 domain of the gag precursor mediates incorporation into virions of Vpr and Vpx proteins from primate lentiviruses. J. Virol. 1999, 73:592-600.
44. Spragg C.J., Emerman M. Antagonism of SAMHD1 is actively maintained in natural infections of simian immunodeficiency virus. Proc. Natl. Acad. Sci. USA 2013.
45. Srivastava S., Swanson S.K., Manel N., Florens L., Washburn M.P., 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.
46. Sunseri N., O'Brien M., Bhardwaj N., Landau N.R. Human immunodeficiency virus type 1 modified to package simian immunodeficiency virus Vpx efficiently infects macrophages and dendritic cells. J. Virol. 2011, 85:6263-6274.
47. Wei W., Guo H., Gao Q., Markham R., Yu X.F. Variation of two primate lineage-specific residues in human SAMHD1 confers resistance to N terminus-targeted SIV Vpx proteins. J. Virol. 2014, 88:583-591.
48. Wei W., Guo H., Han X., Liu X., Zhou X., Zhang W., Yu X.F. A novel DCAF1-binding motif required for Vpx-mediated degradation of nuclear SAMHD1 and Vpr-induced G2 arrest. Cellular Microbiol. 2012, 14:1745-1756.
49. Welbourn S., Dutta S.M., Semmes O.J., Strebel K. Restriction of virus infection but not catalytic dNTPase activity are regulated by phosphorylation of SAMHD1. J. Virol. 2013.
50. White T.E., Brandariz-Nunez A., Valle-Casuso J.C., 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.
51. White T.E., Brandariz-Nunez A., Valle-Casuso J.C., Amie S., Nguyen L.A., 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.
52. Yan J., Kaur S., Delucia M., Hao C., Mehrens J., Wang C., Golczak M., Palczewski K., Gronenborn A.M., Ahn J., Skowronski J. Tetramerization of SAMHD1 is required for biological activity and inhibition of HIV infection. J. Biol. Chem. 2013, 288:10406-10417.
53. Yee J.K., Friedmann T., Burns J.C. Generation of high-titer pseudotyped retroviral vectors with very broad host range. Methods Cell Biol. 1994, 43(Part A):99-112.
54. Yu X.F., Ito S., Essex M., Lee T.H. A naturally immunogenic virion-associated protein specific for HIV-2 and SIV. Nature 1988, 335:262-265.
55. Yu X.F., Yu Q.C., Essex M., Lee T.H. The Vpx gene of simian immunodeficiency virus facilitates efficient viral replication in fresh lymphocytes and macrophage. J. Virol. 1991, 65:5088-5091.
56. Zhang C., de Silva S., Wang J.H., Wu L. Co-evolution of primate SAMHD1 and lentivirus Vpx leads to the loss of the Vpx gene in HIV-1 ancestor. PLoS One 2012, 7:e37477.
57. Zhao K., Du J., Han X., Goodier J.L., Li P., Zhou X., Wei W., Evans S.L., Li L., Zhang W., Cheung L.E., Wang G., Kazazian H.H., Yu X.F. Modulation of LINE-1 and Alu/SVA retrotransposition by Aicardi-Goutieres syndrome-related SAMHD1. Cell Rep. 2013, 4:1108-1115.
58. Zhu C., Gao W., Zhao K., Qin X., Zhang Y., Peng X., Zhang L., Dong Y., Zhang W., Li P., Wei W., Gong Y., Yu X.F. Structural insight into dGTP-dependent activation of tetrameric SAMHD1 deoxynucleoside triphosphate triphosphohydrolase. Nat. Commun. 2013, 4:2722.