New insights into an x-traordinary viral protein

Frontiers in Microbiology

Volumn 5, Issue APR, 2014, Pages

  Schaller, Torsten ^a   Bauby, Hélène ^a   Hué, Stéphane ^b   Malim, Michael H ^a   Goujon, Caroline ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

HIV 1; HIV 2; Interferon type I; Myeloid cells; Restriction factor; SAMHD1; SIVsmm; Vpx

Indexed keywords

APOLIPOPROTEIN B MRNA EDITING ENZYME CATALYTIC POLYPEPTIDE LIKE 3; CD14 ANTIGEN; CYCLIC GMP; CYCLIN DEPENDENT KINASE 1; CYTIDINE DEAMINASE; INTERFERON; LENTIVIRUS VECTOR; PARATHION; SAMHD1; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VIRUS PROTEIN; VPX PROTEIN;

ANTIVIRAL ACTIVITY; BINDING AFFINITY; CD4+ T LYMPHOCYTE; CELL CYCLE; CELL CYCLE CHECKPOINT; CERCOCEBUS; CERCOPITHECUS; EASTERN EQUINE ENCEPHALOMYELITIS VIRUS; EVOLUTION; FELINE IMMUNODEFICIENCY VIRUS; GENE MUTATION; GENE SILENCING; GENETIC POLYMORPHISM; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; INNATE IMMUNITY; LENTIVIRINAE; MACACA; MANDRILLUS; MASS SPECTROMETRY; MURINE LEUKEMIA VIRUS; MUTAGENESIS; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PHENOTYPE; PHYLOGENY; PROLINE RICH PROTEIN DOMAIN; PROTEIN DEGRADATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION; REVIEW; STRUCTURAL HOMOLOGY; ZINC FINGER MOTIF;

EID: 84899684361     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00126     Document Type: Review

References (140)

1. Accola, M. A., Bukovsky, A. A., Jones, M. S., and Gottlinger, H. G. (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. Ahn, J., Hao, C., Yan, J., Delucia, M., Mehrens, J., Wang, C., 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. doi: 10.1074/jbc.M112.340711
3. Akari, H., Sakuragi, J., Takebe, Y., Tomonaga, K., Kawamura, M., Fukasawa, M., et al. (1992). Biological characterization of human immunodeficiency virus type 1 and type 2 mutants in human peripheral blood mononuclear cells. Arch. Virol. 123, 157-167. doi: 10.1007/BF01317146
4. Angers, S., Li, T., Yi, X., Maccoss, M. J., Moon, R. T., and Zheng, N. (2006). Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature 443, 590-593. doi: 10.1038/nature05175
5. Baca-Regen, L., Heinzinger, N., Stevenson, M., and Gendelman, H. E. (1994). Alpha interferon-induced antiretroviral activities: restriction of viral nucleic acid synthesis and progeny virion production in human immunodeficiency virus type 1-infected monocytes. J. Virol. 68, 7559-7565.
6. Bailes, E., Gao, F., Bibollet-Ruche, F., Courgnaud, V., Peeters, M., Marx, P. A., et al. (2003). Hybrid origin of SIV in chimpanzees. Science 300, 1713. doi: 10.1126/science.1080657
7. Baldauf, H. M., Pan, X., Erikson, E., Schmidt, S., Daddacha, W., Burggraf, M., et al. (2012). SAMHD1 restricts HIV-1 infection in resting CD4(+) T cells. Nat. Med. 18, 1682-1689. doi: 10.1038/nm.2964
8. Beck-Engeser, G. B., Eilat, D., and Wabl, M. (2011). An autoimmune disease prevented by anti-retroviral drugs. Retrovirology 8, 91. doi: 10.1186/1742-4690-8-91
9. Beer, B. E., Foley, B. T., Kuiken, C. L., Tooze, Z., Goeken, R. M., Brown, C. R., et al. (2001). Characterization of novel simian immunodeficiency viruses from red-capped mangabeys from Nigeria (SIVrcmNG409 and -NG411). J. Virol. 75, 12014-12027. doi: 10.1128/JVI.75.24.12014-12027.2001
10. Behrendt, R., Schumann, T., Gerbaulet, A., Nguyen, L. A., Schubert, N., Alexopoulou, D., et al. (2013). Mouse SAMHD1 has antiretroviral activity and suppresses a spontaneous cell-intrinsic antiviral response. Cell Rep. 4, 689-696. doi: 10.1016/j.celrep.2013.07.037
11. Beloglazova, N., Flick, R., Tchigvintsev, A., Brown, G., Popovic, A., Nocek, B., et al. (2013). Nuclease activity of the human SAMHD1 protein implicated in the Aicardi-Goutieres syndrome and HIV-1 restriction. J. Biol. Chem. 288, 8101-8110. doi: 10.1074/jbc.M112.431148
12. Belshan, M., Kimata, J. T., Brown, C., Cheng, X., McCulley, A., Larsen, A., et al. (2012). Vpx is critical for SIVmne infection of pigtail macaques. Retrovirology 9, 32. doi: 10.1186/1742-4690-9-32
13. Belshan, M., Mahnke, L. A., and Ratner, L. (2006). 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, 118-126. doi: 10.1016/j.virol.2005.10.036
14. Belshan, M., and Ratner, L. (2003). Identification of the nuclear localization signal of human immunodeficiency virus type 2 Vpx. Virology 311, 7-15. doi: 10.1016/S0042-6822(03)00093-X
15. Bergamaschi, A., Ayinde, D., David, A., Le Rouzic, E., Morel, M., Collin, G., et al. (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. doi: 10.1128/JVI.00187-09
16. Berger, A., Munk, C., Schweizer, M., Cichutek, K., Schule, S., and Flory, E. (2010). Interaction of Vpx and apolipoprotein B mRNA-editing catalytic polypeptide 3 family member A (APOBEC3A) correlates with efficient lentivirus infection of monocytes. J. Biol. Chem. 285, 12248-12254. doi: 10.1074/jbc.M109.090977
17. Berger, A., Sommer, A. F., Zwarg, J., Hamdorf, M., Welzel, K., Esly, N., et al. (2011a). SAMHD1-deficient CD14+ cells from individuals with Aicardi-Goutieres syndrome are highly susceptible to HIV-1 infection. PLoS Pathog. 7:e1002425. doi: 10.1371/journal.ppat.1002425
18. Berger, G., Durand, S., Fargier, G., Nguyen, X. N., Cordeil, S., Bouaziz, S., et al. (2011b). APOBEC3A is a specific inhibitor of the early phases of HIV-1 infection in myeloid cells. PLoS Pathog. 7:e1002221. doi: 10.1371/journal.ppat.1002221
19. Berger, G., Turpin, J., Cordeil, S., Tartour, K., Nguyen, X. N., Mahieux, R., et al. (2012). Functional analysis of the relationship between Vpx and the restriction factor SAMHD1. J. Biol. Chem. 287, 41210-41217. doi: 10.1074/jbc.M112.403816
20. Bitzegeio, J., Sampias, M., Bieniasz, P. D., and Hatziioannou, T. (2013). Adaptation to the interferon-induced antiviral state by human and simian immunodeficiency viruses. J. Virol. 87, 3549-3560. doi: 10.1128/JVI.03219-12
21. Bloch, N., O'Brien, M., Norton, T. D., Polsky, S. B., Bhardwaj, N., and Landau, N. R. (2014). HIV Type 1 infection of plasmacytoid and myeloid dendritic cells is restricted by high levels of SAMHD1 and cannot be counteracted by Vpx. AIDS Res. Hum. Retroviruses 30, 195-203. doi: 10.1089/AID.2013.0119
22. Bogerd, H. P., Wiegand, H. L., Doehle, B. P., Lueders, K. K., and Cullen, B. R. (2006). APOBEC3A and APOBEC3B are potent inhibitors of LTR-retrotransposon function in human cells. Nucleic Acids Res. 34, 89-95. doi: 10.1093/nar/gkj416
23. Brandariz-Nunez, A., Valle-Casuso, J. C., White, T. E., Laguette, N., Benkirane, M., Brojatsch, J., et al. (2012). Role of SAMHD1 nuclear localization in restriction of HIV-1 and SIVmac. Retrovirology 9, 49. doi: 10.1186/1742-4690-9-49
24. Chahwan, C., and Chahwan, R. (2012). Aicardi-Goutieres syndrome: from patients to genes and beyond. Clin. Genet. 81, 413-420. doi: 10.1111/j.1399-0004.2011.01825.x
25. Chen, H., Lilley, C. E., Yu, Q., Lee, D. V., Chou, J., Narvaiza, I., et al. (2006). APOBEC3A is a potent inhibitor of adeno-associated virus and retrotransposons. Curr. Biol. 16, 480-485. doi: 10.1016/j.cub.2006.01.031
26. Cheney, K. M., and McKnight, A. (2010). Interferon-alpha mediates restriction of human immunodeficiency virus type-1 replication in primary human macrophages at an early stage of replication. PLoS ONE 5:e13521. doi: 10.1371/journal.pone.0013521
27. Cordeil, S., Nguyen, X. N., Berger, G., Durand, S., Ainouze, M., and Cimarelli, A. (2013). Evidence for a different susceptibility of primate lentiviruses to type I interferons. J. Virol. 87, 2587-2596. doi: 10.1128/JVI.02553-12
28. Cribier, A., Descours, B., Valadao, A. L., Laguette, N., and Benkirane, M. (2013). Phosphorylation of SAMHD1 by cyclin A2/CDK1 regulates its restriction activity toward HIV-1. Cell Rep. 3, 1036-1043. doi: 10.1016/j.celrep.2013.03.017
29. Crow, Y. J., Hayward, B. E., Parmar, R., Robins, P., Leitch, A., Ali, M., et al. (2006). Mutations in the gene encoding the 3'-5' DNA exonuclease TREX1 cause Aicardi-Goutieres syndrome at the AGS1 locus. Nat. Genet. 38, 917-920. doi: 10.1038/ng1845
30. Delucia, M., Mehrens, J., Wu, Y., and 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. doi: 10.1074/jbc.M113.469007
31. Depienne, C., Roques, P., Creminon, C., Fritsch, L., Casseron, R., Dormont, D., et al. (2000). Cellular distribution and karyophilic properties of matrix, integrase, and Vpr proteins from the human and simian immunodeficiency viruses. Exp. Cell Res. 260, 387-395. doi: 10.1006/excr.2000.5016
32. Descours, B., Cribier, A., Chable-Bessia, C., Ayinde, D., Rice, G., Crow, Y., et al. (2012). SAMHD1 restricts HIV-1 reverse transcription in quiescent CD4(+) T-cells. Retrovirology 9, 87. doi: 10.1186/1742-4690-9-87
33. Diamond, T. L., Roshal, M., Jamburuthugoda, V. K., Reynolds, H. M., Merriam, A. R., Lee, K. Y., et al. (2004). Macrophage tropism of HIV-1 depends on efficient cellular dNTP utilization by reverse transcriptase. J. Biol. Chem. 279, 51545-51553. doi: 10.1074/jbc.M408573200
34. Diamond, T. L., Souroullas, G., Weiss, K. K., Lee, K. Y., Bambara, R. A., Dewhurst, S., et al. (2003). Mechanistic understanding of an altered fidelity simian immunodeficiency virus reverse transcriptase mutation, V148I, identified in a pig-tailed macaque. J. Biol. Chem. 278, 29913-29924. doi: 10.1074/jbc.M211754200
35. Dragin, L., Nguyen, L. A., Lahouassa, H., Sourisce, A., Kim, B., Ramirez, B. C., et al. (2013). Interferon block to HIV-1 transduction in macrophages despite SAMHD1 degradation and high deoxynucleoside triphosphates supply. Retrovirology 10, 30. doi: 10.1186/1742-4690-10-30
36. Esbjornsson, J., Mansson, F., Kvist, A., Isberg, P. E., Nowroozalizadeh, S., Biague, A. J., et al. (2012). Inhibition of HIV-1 disease progression by contemporaneous HIV-2 infection. N. Engl. J. Med. 367, 224-232. doi: 10.1056/NEJMoa1113244
37. Etienne, L., Hahn, B. H., Sharp, P. M., Matsen, F. A., and Emerman, M. (2013). Gene loss and adaptation to hominids underlie the ancient origin of HIV-1. Cell Host Microbe 14, 85-92. doi: 10.1016/j.chom.2013.06.002
38. Fletcher, T. M. 3rd., Brichacek, B., Sharova, N., Newman, M. A., Stivahtis, G., Sharp, P. M., et al. (1996). 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, 6155-6165.
39. Franchini, G., Rusche, J. R., O'Keeffe, T. J., and Wong-Staal, F. (1988). The human immunodeficiency virus type 2 (HIV-2) contains a novel gene encoding a 16 kD protein associated with mature virions. AIDS Res. Hum. Retroviruses 4, 243-250. doi: 10.1089/aid.1988.4.243
40. Fregoso, O. I., Ahn, J., Wang, C., Mehrens, J., Skowronski, J., and Emerman, M. (2013). Evolutionary toggling of Vpx/Vpr specificity results in divergent recognition of the restriction factor SAMHD1. PLoS Pathog. 9:e1003496. doi: 10.1371/journal.ppat.1003496
41. Fujita, M., Otsuka, M., Miyoshi, M., Khamsri, B., Nomaguchi, M., and Adachi, A. (2008). Vpx is critical for reverse transcription of the human immunodeficiency virus type 2 genome in macrophages. J. Virol. 82, 7752-7756. doi: 10.1128/JVI.01003-07
42. Gibbs, J. S., Lackner, A. A., Lang, S. M., Simon, M. A., Sehgal, P. K., Daniel, M. D., et al. (1995). Progression to AIDS in the absence of a gene for vpr or vpx. J. Virol. 69, 2378-2383.
43. Gibbs, J. S., Regier, D. A., and Desrosiers, R. C. (1994). Construction and in vitro properties of SIVmac mutants with deletions in "nonessential" genes. AIDS Res. Hum. Retroviruses 10, 607-616. doi: 10.1089/aid.1994.10.607
44. Goldstone, D. C., Ennis-Adeniran, V., Hedden, J. J., Groom, H. C., Rice, G. I., Christodoulou, E., et al. (2011). HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase. Nature 480, 379-382. doi: 10.1038/nature10623
45. Goncalves, A., Karayel, E., Rice, G. I., Bennett, K. L., Crow, Y. J., Superti-Furga, G., et al. (2012). SAMHD1 is a nucleic-acid binding protein that is mislocalized due to aicardi-goutieres syndrome-associated mutations. Hum. Mutat. 33, 1116-1122. doi: 10.1002/humu.22087
46. Goujon, C., Arfi, V., Pertel, T., Luban, J., Lienard, J., Rigal, D., et al. (2008). Characterization of simian immunodeficiency virus SIVSM/human immunodeficiency virus type 2 Vpx function in human myeloid cells. J. Virol. 82, 12335-12345. doi: 10.1128/JVI.01181-08
47. Goujon, C., Jarrosson-Wuilleme, L., Bernaud, J., Rigal, D., Darlix, J. L., and Cimarelli, A. (2006). With a little help from a friend: increasing HIV transduction of monocyte-derived dendritic cells with virion-like particles of SIV(MAC). Gene Ther. 13, 991-994. doi: 10.1038/sj.gt.3302753
48. Goujon, C., and Malim, M. H. (2010). Characterization of the alpha interferon-induced postentry block to HIV-1 infection in primary human macrophages and T cells. J. Virol. 84, 9254-9266. doi: 10.1128/JVI.00854-10
49. Goujon, C., Riviere, L., Jarrosson-Wuilleme, L., Bernaud, J., Rigal, D., Darlix, J. L., 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. doi: 10.1186/1742-4690-4-2
50. Goujon, C., Schaller, T., Galao, R. P., Amie, S. M., Kim, B., Olivieri, K., et al. (2013). Evidence for IFNalpha-induced, SAMHD1-independent inhibitors of early HIV-1 infection. Retrovirology 10, 23. doi: 10.1186/1742-4690-10-23
51. Gramberg, T., Kahle, T., Bloch, N., Wittmann, S., Mullers, E., Daddacha, W., et al. (2013). Restriction of diverse retroviruses by SAMHD1. Retrovirology 10, 26. doi: 10.1186/1742-4690-10-26
52. Gramberg, T., Sunseri, N., and Landau, N. R. (2010). Evidence for an activation domain at the amino terminus of simian immunodeficiency virus Vpx. J. Virol. 84, 1387-1396. doi: 10.1128/JVI.01437-09
53. Guo, H., Wei, W., Wei, Z., Liu, X., Evans, S. L., Yang, W., et al. (2013). Identification of critical regions in human SAMHD1 required for nuclear localization and Vpx-mediated degradation. PLoS ONE 8:e66201. doi: 10.1371/journal.pone.0066201
54. Guyader, M., Emerman, M., Montagnier, L., and 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.
55. Henderson, L. E., Sowder, R. C., Copeland, T. D., Benveniste, R. E., and Oroszlan, S. (1988). Isolation and characterization of a novel protein (X-ORF product) from SIV and HIV-2. Science 241, 199-201. doi: 10.1126/science.3388031
56. Hirsch, V. M., Sharkey, M. E., Brown, C. R., Brichacek, B., Goldstein, S., Wakefield, J., et al. (1998). Vpx is required for dissemination and pathogenesis of SIV(SM) PBj: evidence of macrophage-dependent viral amplification. Nat. Med. 4, 1401-1408. doi: 10.1038/3992
57. Hofmann, H., Logue, E. C., Bloch, N., Daddacha, W., Polsky, S. B., Schultz, M. L., et al. (2012). The Vpx lentiviral accessory protein targets SAMHD1 for degradation in the nucleus. J. Virol. 86, 12552-12560. doi: 10.1128/JVI.01657-12
58. Hofmann, H., Norton, T. D., Schultz, M. L., Polsky, S. B., Sunseri, N., and Landau, N. R. (2013). Inhibition of CUL4A neddylation causes a reversible block to SAMHD1-mediated restriction of HIV-1. J. Virol. 87, 11741-11750. doi: 10.1128/JVI.02002-13
59. Hollenbaugh, J. A., Gee, P., Baker, J., Daly, M. B., Amie, S. M., Tate, J., et al. (2013). Host factor SAMHD1 restricts DNA viruses in non-dividing myeloid cells. PLoS Pathog. 9:e1003481. doi: 10.1371/journal.ppat.1003481
60. Hrecka, K., Hao, C., Gierszewska, M., Swanson, S. K., Kesik-Brodacka, M., Srivastava, S., et al. (2011). Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474, 658-661. doi: 10.1038/nature10195
61. Hu, J., Switzer, W. M., Foley, B. T., Robertson, D. L., Goeken, R. M., Korber, B. T., et al. (2003). Characterization and comparison of recombinant simian immunodeficiency virus from drill (Mandrillus leucophaeus) and mandrill (Mandrillus sphinx) isolates. J. Virol. 77, 4867-4880. doi: 10.1128/JVI.77.8.4867-4880.2003
62. Hu, W., Vander Heyden, N., and Ratner, L. (1989). Analysis of the function of viral protein X (VPX) of HIV-2. Virology 173, 624-630. doi: 10.1016/0042-6822(89)90574-6
63. Ji, X., Wu, Y., Yan, J., Mehrens, J., Yang, H., Delucia, M., et al. (2013). Mechanism of allosteric activation of SAMHD1 by dGTP. Nat. Struct. Mol. Biol. 20, 1304-1309. doi: 10.1038/nsmb.2692
64. Jin, M. J., Hui, H., Robertson, D. L., Muller, M. C., Barre-Sinoussi, F., Hirsch, V. M., et al. (1994). Mosaic genome structure of simian immunodeficiency virus from west African green monkeys. EMBO J. 13, 2935-2947.
65. Kappes, J. C., Conway, J. A., Lee, S. W., Shaw, G. M., and Hahn, B. H. (1991). Human immunodeficiency virus type 2 vpx protein augments viral infectivity. Virology 184, 197-209. doi: 10.1016/0042-6822(91)90836-Z
66. Kappes, J. C., Morrow, C. D., Lee, S. W., Jameson, B. A., Kent, S. B., Hood, L. E., et al. (1988). Identification of a novel retroviral gene unique to human immunodeficiency virus type 2 and simian immunodeficiency virus SIVMAC. J. Virol. 62, 3501-3505.
67. Kaushik, R., Zhu, X., Stranska, R., Wu, Y., and Stevenson, M. (2009). A cellular restriction dictates the permissivity of nondividing monocytes/macrophages to lentivirus and gammaretrovirus infection. Cell Host Microbe 6, 68-80. doi: 10.1016/j.chom.2009.05.022
68. Kawamura, M., Sakai, H., and Adachi, A. (1994). Human immunodeficiency virus Vpx is required for the early phase of replication in peripheral blood mononuclear cells. Microbiol. Immunol. 38, 871-878. doi: 10.1111/j.1348-0421.1994.tb02140.x
69. Kewalramani, V. N., and Emerman, M. (1996). Vpx association with mature core structures of HIV-2. Virology 218, 159-168. doi: 10.1006/viro.1996.0176
70. Kim, E. T., White, T. E., Brandariz-Nunez, A., Diaz-Griffero, F., and Weitzman, M. D. (2013). SAMHD1 restricts herpes simplex virus 1 in macrophages by limiting DNA replication. J. Virol. 87, 12949-12956. doi: 10.1128/JVI.02291-13
71. Koning, F. A., Goujon, C., Bauby, H., and Malim, M. H. (2011). Target cell-mediated editing of HIV-1 cDNA by APOBEC3 proteins in human macrophages. J. Virol. 85, 13448-13452. doi: 10.1128/JVI.00775-11
72. Koning, F. A., Newman, E. N., Kim, E. Y., Kunstman, K. J., Wolinsky, S. M., and Malim, M. H. (2009). Defining APOBEC3 expression patterns in human tissues and hematopoietic cell subsets. J. Virol. 83, 9474-9485. doi: 10.1128/JVI.01089-09
73. Korin, Y. D., and Zack, J. A. (1999). Nonproductive human immunodeficiency virus type 1 infection in nucleoside-treated G0 lymphocytes. J. Virol. 73, 6526-6532.
74. Kornbluth, R. S., Oh, P. S., Munis, J. R., Cleveland, P. H., and Richman, D. D. (1989). Interferons and bacterial lipopolysaccharide protect macrophages from productive infection by human immunodeficiency virus in vitro. J. Exp. Med. 169, 1137-1151. doi: 10.1084/jem.169.3.1137
75. Laguette, N., Rahm, N., Sobhian, B., Chable-Bessia, C., Munch, J., Snoeck, 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. doi: 10.1016/j.chom.2012.01.007
76. Laguette, N., Sobhian, B., Casartelli, N., Ringeard, M., Chable-Bessia, C., Segeral, E., et al. (2011). SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474, 654-657. doi: 10.1038/nature10117
77. Lahaye, X., Satoh, T., Gentili, M., Cerboni, S., Conrad, C., Hurbain, I., et al. (2013). The Capsids of HIV-1 and HIV-2 determine immune detection of the viral cDNA by the innate sensor cGAS in dendritic cells. Immunity 39, 1132-1142. doi: 10.1016/j.immuni.2013.11.002
78. Lahouassa, H., Daddacha, W., Hofmann, H., Ayinde, D., Logue, E. C., Dragin, L., 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. doi: 10.1038/ni.2236
79. Le Rouzic, E., Belaidouni, N., Estrabaud, E., Morel, M., Rain, J. C., Transy, C., et al. (2007). HIV1 Vpr arrests the cell cycle by recruiting DCAF1/VprBP, a receptor of the Cul4-DDB1 ubiquitin ligase. Cell Cycle 6, 182-188. doi: 10.4161/cc.6.2.3732
80. Lewis, P. F., and Emerman, M. (1994). Passage through mitosis is required for oncoretroviruses but not for the human immunodeficiency virus. J. Virol. 68, 510-516.
81. Li, N., Zhang, W., and Cao, X. (2000). Identification of human homologue of mouse IFN-gamma induced protein from human dendritic cells. Immunol. Lett. 74, 221-224. doi: 10.1016/S0165-2478(00)00276-5
82. Liao, W., Bao, Z., Cheng, C., Mok, Y. K., and Wong, W. S. (2008). Dendritic cell-derived interferon-gamma-induced protein mediates tumor necrosis factor-alpha stimulation of human lung fibroblasts. Proteomics 8, 2640-2650. doi: 10.1002/pmic.200700954
83. Lim, E. S., Fregoso, O. I., McCoy, C. O., Matsen, F. A., Malik, H. S., and Emerman, M. (2012). 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, 194-204. doi: 10.1016/j.chom.2012.01.004
84. Mahalingam, S., Van Tine, B., Santiago, M. L., Gao, F., Shaw, G. M., and Hahn, B. H. (2001). Functional analysis of the simian immunodeficiency virus Vpx protein: identification of packaging determinants and a novel nuclear targeting domain. J. Virol. 75, 362-374. doi: 10.1128/JVI.75.1.362-374.2001
85. Malim, M. H., and Bieniasz, P. D. (2012). HIV restriction factors and mechanisms of evasion. Cold Spring Harb. Perspect. Med. 2:a006940. doi: 10.1101/cshperspect.a006940
86. Manel, N., Hogstad, B., Wang, Y., Levy, D. E., Unutmaz, D., and Littman, D. R. (2010). A cryptic sensor for HIV-1 activates antiviral innate immunity in dendritic cells. Nature 467, 214-217. doi: 10.1038/nature09337
87. Mangeot, P. E., Duperrier, K., Negre, D., Boson, B., Rigal, D., Cosset, F. L., et al. (2002). High levels of transduction of human dendritic cells with optimized SIV vectors. Mol. Ther. 5, 283-290. doi: 10.1006/mthe.2002.0541
88. Muckenfuss, H., Hamdorf, M., Held, U., Perkovic, M., Lower, J., Cichutek, K., et al. (2006). APOBEC3 proteins inhibit human LINE-1 retrotransposition. J. Biol. Chem. 281, 22161-22172. doi: 10.1074/jbc.M601716200
89. Narvaiza, I., Linfesty, D. C., Greener, B. N., Hakata, Y., Pintel, D. J., Logue, E., et al. (2009). Deaminase-independent inhibition of parvoviruses by the APOBEC3A cytidine deaminase. PLoS Pathog. 5:e1000439. doi: 10.1371/journal.ppat.1000439
90. Neil, S., Martin, F., Ikeda, Y., and Collins, M. (2001). Postentry restriction to human immunodeficiency virus-based vector transduction in human monocytes. J. Virol. 75, 5448-5456. doi: 10.1128/JVI.75.12.5448-5456.2001
91. Pan, X., Baldauf, H. M., Keppler, O. T., and Fackler, O. T. (2013). Restrictions to HIV-1 replication in resting CD4+ T lymphocytes. Cell Res. 23, 876-885. doi: 10.1038/cr.2013.74
92. Pancio, H. A., Vander Heyden, N., and Ratner, L. (2000). The C-terminal proline-rich tail of human immunodeficiency virus type 2 Vpx is necessary for nuclear localization of the viral preintegration complex in nondividing cells. J. Virol. 74, 6162-6167. doi: 10.1128/JVI.74.13.6162-6167.2000
93. Park, I. W., and Sodroski, J. (1995). Functional analysis of the vpx, vpr, and nef genes of simian immunodeficiency virus. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 8, 335-344. doi: 10.1097/00042560-199504000-00003
94. Peng, G., Greenwell-Wild, T., Nares, S., Jin, W., Lei, K. J., Rangel, Z. G., et al. (2007). Myeloid differentiation and susceptibility to HIV-1 are linked to APOBEC3 expression. Blood 110, 393-400. doi: 10.1182/blood-2006-10-051763
95. Peng, G., Lei, K. J., Jin, W., Greenwell-Wild, T., and Wahl, S. M. (2006). Induction of APOBEC3 family proteins, a defensive maneuver underlying interferon-induced anti-HIV-1 activity. J. Exp. Med. 203, 41-46. doi: 10.1084/jem.20051512
96. Pertel, T., Reinhard, C., and Luban, J. (2011). Vpx rescues HIV-1 transduction of dendritic cells from the antiviral state established by type 1 interferon. Retrovirology 8, 49. doi: 10.1186/1742-4690-8-49
97. Powell, R. D., Holland, P. J., Hollis, T., and Perrino, F. W. (2011). Aicardi-Goutieres syndrome gene and HIV-1 restriction factor SAMHD1 is a dGTP-regulated deoxynucleotide triphosphohydrolase. J. Biol. Chem. 286, 43596-43600. doi: 10.1074/jbc.C111.317628
98. Rajendra Kumar, P., Singhal, P. K., Subba Rao, M. R., and Mahalingam, S. (2005). Phosphorylation by MAPK regulates simian immunodeficiency virus Vpx protein nuclear import and virus infectivity. J. Biol. Chem. 280, 8553-8563. doi: 10.1074/jbc.M407863200
99. Rajendra Kumar, P., Singhal, P. K., Vinod, S. S., and Mahalingam, S. (2003). A non-canonical transferable signal mediates nuclear import of simian immunodeficiency virus Vpx protein. J. Mol. Biol. 331, 1141-1156. doi: 10.1016/S0022-2836(03)00853-2
100. Refsland, E. W., Stenglein, M. D., Shindo, K., Albin, J. S., Brown, W. L., and Harris, R. S. (2010). Quantitative profiling of the full APOBEC3 mRNA repertoire in lymphocytes and tissues: implications for HIV-1 restriction. Nucleic Acids Res. 38, 4274-4284. doi: 10.1093/nar/gkq174
101. Rehwinkel, J., Maelfait, J., Bridgeman, A., Rigby, R., Hayward, B., Liberatore, R. A., et al. (2013). SAMHD1-dependent retroviral control and escape in mice. EMBO J. 32, 2454-2462. doi: 10.1038/emboj.2013.163
102. Reinhard, C., Bottinelli, D., Kim, B., and Luban, J. (2014). Vpx rescue of HIV-1 from the antiviral state in mature dendritic cells is independent of the intracellular deoxynucleotide concentration. Retrovirology 11, 12. doi: 10.1186/1742-4690-11-12
103. Rice, G. I., Bond, J., Asipu, A., Brunette, R. L., Manfield, I. W., Carr, I. M., et al. (2009). Mutations involved in Aicardi-Goutieres syndrome implicate SAMHD1 as regulator of the innate immune response. Nat. Genet. 41, 829-832. doi: 10.1038/ng.373
104. Roe, T., Reynolds, T. C., Yu, G., and Brown, P. O. (1993). Integration of murine leukemia virus DNA depends on mitosis. EMBO J. 12, 2099-2108.
105. Schwefel, D., Groom, H. C., Boucherit, V. C., Christodoulou, E., Walker, P. A., Stoye, J. P., et al. (2014). Structural basis of lentiviral subversion of a cellular protein degradation pathway. Nature 505, 234-238. doi: 10.1038/nature12815
106. Selig, L., Pages, J. C., Tanchou, V., Preveral, S., Berlioz-Torrent, C., Liu, L. X., 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.
107. Sharova, N., Wu, Y., Zhu, X., Stranska, R., Kaushik, R., Sharkey, M., et al. (2008). Primate lentiviral Vpx commandeers DDB1 to counteract a macrophage restriction. PLoS Pathog. 4:e1000057. doi: 10.1371/journal.ppat.1000057
108. Sharp, P. M., Bailes, E., Stevenson, M., Emerman, M., and Hahn, B. H. (1996). Gene acquisition in HIV and SIV. Nature 383, 586-587. doi: 10.1038/383586a0
109. Sharp, P. M., and Hahn, B. H. (2011). Origins of HIV and the AIDS pandemic. Cold Spring Harb. Perspect. Med. 1:a006841. doi: 10.1101/cshperspect.a006841
110. Shibata, R., Miura, T., Hayami, M., Ogawa, K., Sakai, H., Kiyomasu, T., et al. (1990). Mutational analysis of the human immunodeficiency virus type 2 (HIV-2) genome in relation to HIV-1 and simian immunodeficiency virus SIV (AGM). J. Virol. 64, 742-747.
111. Shirazi, Y., and Pitha, P. M. (1992). Alpha interferon inhibits early stages of the human immunodeficiency virus type 1 replication cycle. J. Virol. 66, 1321-1328.
112. Shirazi, Y., and Pitha, P. M. (1993). Interferon alpha-mediated inhibition of human immunodeficiency virus type 1 provirus synthesis in T-cells. Virology 193, 303-312. doi: 10.1006/viro.1993.1126
113. Singhal, P. K., Kumar, P. R., Rao, M. R., Kyasani, M., and Mahalingam, S. (2006a). Simian immunodeficiency virus Vpx is imported into the nucleus via importin alpha-dependent and -independent pathways. J. Virol. 80, 526-536. doi: 10.1128/JVI.80.1.526-536.2006
114. Singhal, P. K., Rajendra Kumar, P., Subba Rao, M. R., and Mahalingam, S. (2006b). Nuclear export of simian immunodeficiency virus Vpx protein. J. Virol. 80, 12271-12282. doi: 10.1128/JVI.00563-06
115. Sonza, S., Maerz, A., Deacon, N., Meanger, J., Mills, J., and Crowe, S. (1996). Human immunodeficiency virus type 1 replication is blocked prior to reverse transcription and integration in freshly isolated peripheral blood monocytes. J. Virol. 70, 3863-3869.
116. Spragg, C. J., and Emerman, M. (2013). Antagonism of SAMHD1 is actively maintained in natural infections of simian immunodeficiency virus. Proc. Natl. Acad. Sci. U.S.A. 110, 21136-21141. doi: 10.1073/pnas.1316839110
117. Srivastava, S., Swanson, S. K., Manel, N., Florens, L., Washburn, M. P., and 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. doi: 10.1371/journal.ppat.1000059
118. Stetson, D. B., Ko, J. S., Heidmann, T., and Medzhitov, R. (2008). Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 134, 587-598. doi: 10.1016/j.cell.2008.06.032
119. St Gelais, C., De Silva, S., Amie, S. M., Coleman, C. M., Hoy, H., Hollenbaugh, J. A., 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. doi: 10.1186/1742-4690-9-105
120. Sze, A., Belgnaoui, S. M., Olagnier, D., Lin, R., Hiscott, J., and Van Grevenynghe, J. (2013). Host restriction factor SAMHD1 limits human T cell leukemia virus type 1 infection of monocytes via STING-mediated apoptosis. Cell Host Microbe 14, 422-434. doi: 10.1016/j.chom.2013.09.009
121. Triques, K., and Stevenson, M. (2004). Characterization of restrictions to human immunodeficiency virus type 1 infection of monocytes. J. Virol. 78, 5523-5527. doi: 10.1128/JVI.78.10.5523-5527.2004
122. Tristem, M., Marshall, C., Karpas, A., and Hill, F. (1992). Evolution of the primate lentiviruses: evidence from vpx and vpr. EMBO J. 11, 3405-3412.
123. Tristem, M., Marshall, C., Karpas, A., Petrik, J., and Hill, F. (1990). Origin of vpx in lentiviruses. Nature 347, 341-342. doi: 10.1038/347341b0
124. Trobaugh, D. W., Gardner, C. L., Sun, C., Haddow, A. D., Wang, E., Chapnik, E., et al. (2013). RNA viruses can hijack vertebrate microRNAs to suppress innate immunity. Nature 506, 245-248. doi: 10.1038/nature12869
125. Tungler, V., Staroske, W., Kind, B., Dobrick, M., Kretschmer, S., Schmidt, F., et al. (2013). Single-stranded nucleic acids promote SAMHD1 complex formation. J. Mol. Med. (Berl). 91, 759-770. doi: 10.1007/s00109-013-0995-3
126. Ueno, F., Shiota, H., Miyaura, M., Yoshida, A., Sakurai, A., Tatsuki, J., et al. (2003). Vpx and Vpr proteins of HIV-2 up-regulate the viral infectivity by a distinct mechanism in lymphocytic cells. Microbes Infect. 5, 387-395. doi: 10.1016/S1286-4579(03)00042-X
127. Vartanian, J. P., Guetard, D., Henry, M., and Wain-Hobson, S. (2008). Evidence for editing of human papillomavirus DNA by APOBEC3 in benign and precancerous lesions. Science 320, 230-233. doi: 10.1126/science.1153201
128. Wei, W., Guo, H., Gao, Q., Markham, R., and Yu, X. F. (2014). Variation of two primate lineage-specific residues in human SAMHD1 confers resistance to N terminus-targeted SIV Vpx proteins. J. Virol. 88, 583-591. doi: 10.1128/JVI.02866-13
129. Wei, W., Guo, H., Han, X., Liu, X., Zhou, X., Zhang, W., 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. doi: 10.1111/j.1462-5822.2012.01835.x
130. Weiss, K. K., Chen, R., Skasko, M., Reynolds, H. M., Lee, K., Bambara, R. A., et al. (2004). A role for dNTP binding of human immunodeficiency virus type 1 reverse transcriptase in viral mutagenesis. Biochemistry 43, 4490-4500. doi: 10.1021/bi035258r
131. Welbourn, S., Dutta, S. M., Semmes, O. J., and Strebel, K. (2013). Restriction of virus infection but not catalytic dNTPase activity are regulated by phosphorylation of SAMHD1. J. Virol. 87, 11516-11524. doi: 10.1128/JVI.01642-13
132. Wertheim, J. O., and Worobey, M. (2007). A challenge to the ancient origin of SIVagm based on African green monkey mitochondrial genomes. PLoS Pathog. 3:e95. doi: 10.1371/journal.ppat.0030095
133. White, T. E., Brandariz-Nunez, A., Valle-Casuso, J. C., Amie, S., Nguyen, L. A., Kim, B., et al. (2013). The retroviral restriction ability of SAMHD1, but not its deoxynucleotide triphosphohydrolase activity, is regulated by phosphorylation. Cell Host Microbe 13, 441-451. doi: 10.1016/j.chom.2013.03.005
134. Wu, X., Conway, J. A., Kim, J., and Kappes, J. C. (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.
135. Yan, J., Kaur, S., Delucia, M., Hao, C., Mehrens, J., Wang, C., et al. (2013). Tetramerization of SAMHD1 is required for biological activity and inhibition of HIV infection. J. Biol. Chem. 288, 10406-10417. doi: 10.1074/jbc.M112.443796
136. Yu, H., Usmani, S. M., Borch, A., Kramer, J., Sturzel, C. M., Khalid, M., et al. (2013). The efficiency of Vpx-mediated SAMHD1 antagonism does not correlate with the potency of viral control in HIV-2-infected individuals. Retrovirology 10, 27. doi: 10.1186/1742-4690-10-27
137. Yu, X. F., Ito, S., Essex, M., and Lee, T. H. (1988). A naturally immunogenic virion-associated protein specific for HIV-2 and SIV. Nature 335, 262-265. doi: 10.1038/335262a0
138. Yu, X. F., Yu, Q. C., Essex, M., and Lee, T. H. (1991). The vpx gene of simian immunodeficiency virus facilitates efficient viral replication in fresh lymphocytes and macrophage. J. Virol. 65, 5088-5091.
139. Zhao, K., Du, J., Han, X., Goodier, J. L., Li, P., Zhou, X., et al. (2013). Modulation of LINE-1 and Alu/SVA retrotransposition by Aicardi-Goutieres syndrome-related SAMHD1. Cell Rep. 4, 1108-1115. doi: 10.1016/j.celrep.2013.08.019
140. Zhao, L. J., Mukherjee, S., and Narayan, O. (1994). Biochemical mechanism of HIV-I Vpr function. Specific interaction with a cellular protein. J. Biol. Chem. 269, 15577-15582.