Degradation of SAMHD1 by Vpx is independent of uncoating

Journal of Virology

Volumn 89, Issue 10, 2015, Pages 5701-5713

  Jáuregui, Paula ^a   Logue, Eric C ^a,b   Schultz, Megan L ^a   Fung, Stephanie ^a   Landau, Nathaniel R ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; GAG PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; REGULATOR PROTEIN; STERILE ALPHA MOTIF DOMAIN AND HD DOMAIN CONTAINING PROTEIN 1; UNCLASSIFIED DRUG; VIRUS PROTEIN; VPX PROTEIN; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; SAMHD1 PROTEIN, HUMAN; VPX PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 2;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN TARGETING; VIRION; VIRUS CAPSID; VIRUS MUTATION; VIRUS UNCOATING; GENETICS; HEK293 CELL LINE; HELA CELL LINE; HOST PATHOGEN INTERACTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 2; METABOLISM; MUTATION; PATHOGENICITY; PHYSIOLOGY; PROTEIN PROCESSING; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; MIRIDAE; SIMIAN IMMUNODEFICIENCY VIRUS;

CAPSID PROTEINS; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HEK293 CELLS; HELA CELLS; HIV-1; HIV-2; HOST-PATHOGEN INTERACTIONS; HUMANS; MONOMERIC GTP-BINDING PROTEINS; MUTATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; RECOMBINANT FUSION PROTEINS; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL REGULATORY AND ACCESSORY PROTEINS; VIRUS REPLICATION; VIRUS UNCOATING;

EID: 84928539352     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03575-14     Document Type: Article

References (61)

1. 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.
2. 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.
3. 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.
4. 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.
5. 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.
6. 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.
7. 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.
8. 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/ni.2236.
9. Beloglazova N, Flick R, Tchigvintsev A, Brown G, Popovic A, Nocek B, Yakunin AF. 2013. Nuclease activity of the human SAMHD1 protein implicated in the Aicardi-Goutieres syndrome and HIV-1 restriction. J Biol Chem 288:8101-8110. http://dx.doi.org/10.1074/jbc.M112.431148.
10. Ryoo J, Choi J, Oh C, Kim S, Seo M, Kim SY, Seo D, Kim J, White TE, Brandariz-Nunez A, Diaz-Griffero F, Yun CH, Hollenbaugh JA, Kim B, Baek D, Ahn K. 2014. The ribonuclease activity of SAMHD1 is required for HIV-1 restriction. Nat Med 20:936-941. http://dx.doi.org/10.1038/nm.3626.
11. Rice GI, Bond J, Asipu A, Brunette RL, Manfield IW, Carr IM, Fuller JC, Jackson RM, Lamb T, Briggs TA, Ali M, Gornall H, Couthard LR, Aeby A, Attard-Montalto SP, Bertini E, Bodemer C, Brockmann K, Brueton LA, Corry PC, Desguerre I, Fazzi E, Cazorla AG, Gener B, Hamel BC, Heiberg A, Hunter M, van der Knaap MS, Kumar R, Lagae L, Landrieu PG, Lourenco CM, Marom D, McDermott MF, van der Merwe W, Orcesi S, Prendiville JS, Rasmussen M, Shalev SA, Soler DM, Shinawi M, Spiegel R, Tan TY, Vanderver A, Wakeling EL, Wassmer E, Whittaker E, Lebon P, Stetson DB, Bonthron DT, Crow YJ. 2009. Mutations involved in Aicardi-Goutieres syndrome implicate SAMHD1 as regulator of the innate immune response. Nat Genet 41:829-832. http://dx.doi.org/10.1038/ng.373.
12. Chahwan C, Chahwan R. 2012. Aicardi-Goutieres syndrome: from patients to genes and beyond. Clin Genet 81:413-420. http://dx.doi.org/10.1111/j.1399-0004.2011.01825.x.
13. 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/10.1016/j.chom.2012.01.004.
14. 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.
15. 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.
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. 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. 2009. 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 83:4854-4860. http://dx.doi.org/10.1128/JVI.00187-09.
18. Schaller T, Pollpeter D, Apolonia L, Goujon C, Malim MH. 2014. Nuclear import of SAMHD1 is mediated by a classical karyopherin alpha/beta1 dependent pathway and confers sensitivity to VpxMAC induced ubiquitination and proteasomal degradation. Retrovirology 11:29. http://dx.doi.org/10.1186/1742-4690-11-29.
19. Hofmann H, Norton TD, Schultz ML, Polsky SB, Sunseri N, Landau NR. 2013. Inhibition of CUL4A Neddylation causes a reversible block to SAMHD1-mediated restriction of HIV-1. J Virol 87:11741-11750. http://dx.doi.org/10.1128/JVI.02002-13.
20. Nakagawa T, Mondal K, Swanson PC. 2013. VprBP (DCAF1): a promiscuous substrate recognition subunit that incorporates into both RINGfamily CRL4 and HECT-family EDD/UBR5 E3 ubiquitin ligases. BMC Mol Biol 14:22. http://dx.doi.org/10.1186/1471-2199-14-22.
21. Wang X, Singh S, Jung HY, Yang G, Jun S, Sastry KJ, Park JI. 2013. HIV-1 Vpr protein inhibits telomerase activity via the EDD-DDB1-VPRBP E3 ligase complex. J Biol Chem 288:15474-15480. http://dx.doi.org/10.1074/jbc.M112.416735.
22. 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.
23. 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.
24. 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.
25. Sunseri N, O'Brien M, Bhardwaj N, Landau NR. 2011. Human immunodeficiency virus type 1 modified to package simian immunodeficiency virus Vpx efficiently infects macrophages and dendritic cells. J Virol 85: 6263-6274. http://dx.doi.org/10.1128/JVI.00346-11.
26. Schwefel D, Groom HC, Boucherit VC, Christodoulou E, Walker PA, Stoye JP, Bishop KN, Taylor IA. 2014. Structural basis of lentiviral subversion of a cellular protein degradation pathway. Nature 505:234-238.
27. DeLucia M, Mehrens J, Wu Y, Ahn J. 2013. HIV-2 and SIVmac accessory virulence factor Vpx down-regulates SAMHD1 enzyme catalysis prior to proteasome-dependent degradation. J Biol Chem 288:19116-19126. http://dx.doi.org/10.1074/jbc.M113.469007.
28. 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/10.1128/JVI.01657-12.
29. 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.
30. 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 SAMHD1 and Vpr-induced G2 arrest. Cell Microbiol 14:1745-1756. http://dx.doi.org/10.1111/j.1462-5822.2012.01835.x.
31. 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.
32. 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.
33. Bobadilla S, Sunseri N, Landau NR. 2013. Efficient transduction of myeloid cells by an HIV-1-derived lentiviral vector that packages the Vpx accessory protein. Gene Ther 20:514-520. http://dx.doi.org/10.1038/gt.2012.61.
34. Forshey BM, von Schwedler U, Sundquist WI, Aiken C. 2002. Formation of a human immunodeficiency virus type 1 core of optimal stability is crucial for viral replication. J Virol 76:5667-5677. http://dx.doi.org/10.1128/JVI.76.11.5667-5677.2002.
35. Forshey BM, Shi J, Aiken C. 2005. Structural requirements for recognition of the human immunodeficiency virus type 1 core during host restriction in owl monkey cells. J Virol 79:869-875. http://dx.doi.org/10.1128/JVI.79.2.869-875.2005.
36. 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.
37. Wei W, Guo H, Gao Q, Markham R, Yu XF. 2014. Variation of two primate lineage-specific residues in humanSAMHD1confers resistance to N terminus-targeted SIV Vpx proteins. J Virol 88:583-591. http://dx.doi.org/10.1128/JVI.02866-13.
38. Wyma DJ, Jiang J, Shi J, Zhou J, Lineberger JE, Miller MD, Aiken C. 2004. Coupling of human immunodeficiency virus type 1 fusion to virion maturation: a novel role of the gp41 cytoplasmic tail. J Virol 78:3429-3435. http://dx.doi.org/10.1128/JVI.78.7.3429-3435.2004.
39. Wiegers K, Rutter G, Kottler H, Tessmer U, Hohenberg H, Krausslich HG. 1998. Sequential steps in human immunodeficiency virus particle maturation revealed by alterations of individual Gag polyprotein cleavage sites. J Virol 72:2846-2854.
40. Woodward CL, Cheng SN, Jensen GJ. 12 November 2014. Electron cryo-tomography studies of maturing HIV-1 particles reveal the assembly pathway of the viral core. J Virol http://dx.doi.org/10.1128/JVI.02997-14.
41. White TE, Brandariz-Nunez 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.
42. 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.
43. Hulme AE, Perez O, Hope TJ. 2011. Complementary assays reveal a relationship between HIV-1 uncoating and reverse transcription. Proc Natl Acad Sci U S A 108:9975-9980. http://dx.doi.org/10.1073/pnas.1014522108.
44. Yang Y, Fricke T, Diaz-Griffero F. 2013. Inhibition of reverse transcriptase activity increases stability of the HIV-1 core. J Virol 87:683-687. http://dx.doi.org/10.1128/JVI.01228-12.
45. Schaller T, Ocwieja KE, Rasaiyaah J, Price AJ, Brady TL, Roth SL, Hue S, Fletcher AJ, Lee K, KewalRamani VN, Noursadeghi M, Jenner RG, James LC, Bushman FD, Towers GJ. 2011. HIV-1 capsid-cyclophilin interactions determine nuclear import pathway, integration targeting and replication efficiency. PLoS Pathog 7:e1002439. http://dx.doi.org/10.1371/journal.ppat.1002439.
46. De Iaco A, Luban J. 2014. Cyclophilin A promotes HIV-1 reverse transcription but its effect on transduction correlates best with its effect on nuclear entry of viral cDNA. Retrovirology 11:11. http://dx.doi.org/10.1186/1742-4690-11-11.
47. Collin M, Gordon S. 1994. The kinetics of human immunodeficiency virus reverse transcription are slower in primary human macrophages than in a lymphoid cell line. Virology 200:114-120. http://dx.doi.org/10.1006/viro.1994.1169.
48. Hollenbaugh JA, Tao S, Lenzi GM, Ryu S, Kim DH, Diaz-Griffero F, Schinazi RF, Kim B. 2014. dNTP pool modulation dynamics by SAMHD1 protein in monocyte-derived macrophages. Retrovirology 11: 63. http://dx.doi.org/10.1186/s12977-014-0063-2.
49. Kewalramani VN, Emerman M. 1996. Vpx association with mature core structures of HIV-2. Virology 218:159-168. http://dx.doi.org/10.1006/viro.1996.0176.
50. Yu X, Matsuda Z, Yu QC, Lee TH, Essex M. 1993. Vpx of simian immunodeficiency virus is localized primarily outside the virus core in mature virions. J Virol 67:4386-4390.
51. Shah VB, Shi J, Hout DR, Oztop I, Krishnan L, Ahn J, Shotwell MS, Engelman A, Aiken C. 2013. The host proteins transportin SR2/TNPO3 and cyclophilin A exert opposing effects on HIV-1 uncoating. J Virol 87:422-432. http://dx.doi.org/10.1128/JVI.07177-11.
52. Fricke T, Brandariz-Nunez A, Wang X, Smith AB, III, Diaz-Griffero F. 2013. Human cytosolic extracts stabilize the HIV-1 core. J Virol 87:10587-10597. http://dx.doi.org/10.1128/JVI.01705-13.
53. Shi J, Zhou J, Shah VB, Aiken C, Whitby K. 2011. Small-molecule inhibition of human immunodeficiency virus type 1 infection by virus capsid destabilization. J Virol 85:542-549. http://dx.doi.org/10.1128/JVI.01406-10.
54. Sharifi HJ, Furuya AK, Jellinger RM, Nekorchuk MD, de Noronha CM. 2014. Cullin4A and cullin4B are interchangeable for HIV Vpr and Vpx action through the CRL4 ubiquitin ligase complex. J Virol 88:6944-6958. http://dx.doi.org/10.1128/JVI.00241-14.
55. Pertel T, Reinhard C, Luban J. 2011. Vpx rescues HIV-1 transduction of dendritic cells from the antiviral state established by type 1 interferon. Retrovirology 8:49. http://dx.doi.org/10.1186/1742-4690-8-49.
56. Miller MD, Farnet CM, Bushman FD. 1997. Human immunodeficiency virus type 1 preintegration complexes: studies of organization and composition. J Virol 71:5382-5390.
57. Fassati A, Goff SP. 2001. Characterization of intracellular reverse transcription complexes of human immunodeficiency virus type 1. J Virol 75:3626-3635. http://dx.doi.org/10.1128/JVI.75.8.3626-3635.2001.
58. Xu H, Franks T, Gibson G, Huber K, Rahm N, De Castillia CS, Luban J, Aiken C, Watkins S, Sluis-Cremer N, Ambrose Z. 2013. Evidence for biphasic uncoating during HIV-1 infection from a novel imaging assay. Retrovirology 10:70. http://dx.doi.org/10.1186/1742-4690-10-70.
59. Arhel NJ, Souquere-Besse S, Munier S, Souque P, Guadagnini S, Rutherford S, Prevost MC, Allen TD, Charneau P. 2007. HIV-1 DNA Flap formation promotes uncoating of the pre-integration complex at the nuclear pore. EMBO J 26:3025-3037. http://dx.doi.org/10.1038/sj.emboj.7601740.
60. Hulme AE, Kelley Z, Okocha Z, Hope TJ. 22 October 2014. Identification of capsid mutations that alter the rate of HIV-1 uncoating in infected cells. J Virol http://dx.doi.org/10.1128/JVI.03043-14.
61. Hakata Y, Miyazama M, Landau NR. 2014. Interactions with DCAF1 and DDB1 in the CRL4 E3 ubiquitin ligase are required for Vpr-mediated G2 arrest. Virol J 11:108. http://dx.doi.org/10.1186/1743-422X-11-108.