Vpx overcomes a SAMHD1-independent block to HIV reverse transcription that is specific to resting CD4 T cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 10, 2017, Pages 2729-2734

  Baldauf, Hanna Mari ^a,b,c   Stegmann, Lena ^a   Schwarz, Sarah Marie ^a   Ambiel, Ina ^a,d   Trotard, Maud ^d   Martin, Margarethe ^a   Burggraf, Manja ^e   Lenzi, Gina M ^f   Lejk, Helena ^b,c   Pan, Xiaoyu ^d   Fregoso, Oliver I ^g,m   Lim, Efrem S ^g   Abraham, Libin ^d   Nguyen, Laura A ^f   Rutsch, Frank ^h   König, Renate ^e,i,j   Kim, Baek ^f   Emerman, Michael ^g   Fackler, Oliver T ^d,k   Keppler, Oliver T ^a,b,c,l  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^e PAUL EHRLICH INSTITUT   (Germany)

^f EMORY CENTER FOR AIDS RESEARCH   (United States)

^g USA   (United States)

^h UNIVERSITY HOSPITAL MÜNSTER   (Germany)

ⁱ BURNHAM INSTITUTE   (United States)

^j German Center for Infection Research (DZIF)   (Germany)

^k German Centre for Infection Research (DZIF)   (Germany)

^l German Center for Infection Research   (Germany)

^m UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

HIV; Resting CD4 T cells; Restriction factors; SAMHD1; Vpx

Indexed keywords

AMINO ACID; GUANINE NUCLEOTIDE BINDING PROTEIN; HYDROLASE; LENTIVIRAL X PROTEIN; SAM DOMAIN AND HD DOMAIN CONTAINING PROTEIN; UNCLASSIFIED DRUG; VIRAL PROTEIN; DEOXYNUCLEOSIDE TRIPHOSPHATE TRIPHOSPHOHYDROLASE SAMHD1; SAMHD1 PROTEIN, HUMAN; VIRUS RNA; VPX PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 2;

ALLELE; ARTICLE; BONE MARROW CELL; CD4+ T LYMPHOCYTE; CERCOCEBUS; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; LONG TERMINAL REPEAT; MACROPHAGE; MANDRILLUS; NONHUMAN; NONSENSE MUTATION; NUCLEAR IMPORT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION; TARGET CELL; VIRION; ANIMAL; GENETICS; HOST PATHOGEN INTERACTION; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MONOCYTE; PATHOGENICITY; RHESUS MONKEY; VIROLOGY; VIRUS GENOME; VIRUS REPLICATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; GENOME, VIRAL; HIV INFECTIONS; HIV-1; HIV-2; HOST-PATHOGEN INTERACTIONS; HUMANS; MACACA MULATTA; MONOCYTES; PROTEOLYSIS; REVERSE TRANSCRIPTION; RNA, VIRAL; SAM DOMAIN AND HD DOMAIN-CONTAINING PROTEIN 1; VIRAL REGULATORY AND ACCESSORY PROTEINS; VIRION; VIRUS REPLICATION;

EID: 85014681285     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1613635114     Document Type: Article

References (41)

1. Bakri Y, et al. (2001) The maturation of dendritic cells results in postintegration inhibition of HIV-1 replication. J Immunol 166(6):3780-3788.
2. Goujon C, et al. (2008) Characterization of simian immunodeficiency virus SIVSM/human immunodeficiency virus type 2 Vpx function in human myeloid cells. J Virol 82(24):12335-12345.
3. Goujon C, 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.
4. Kaushik R, Zhu X, Stranska R, Wu Y, Stevenson M (2009) A cellular restriction dictates the permissivity of nondividing monocytes/macrophages to lentivirus and gammaretrovirus infection. Cell Host Microbe 6(1):68-80.
5. Stevenson M, Stanwick TL, Dempsey MP, Lamonica CA (1990) HIV-1 replication is controlled at the level of T cell activation and proviral integration. EMBO J 9(5):1551-1560.
6. Zack JA, et al. (1990) HIV-1 entry into quiescent primary lymphocytes: Molecular analysis reveals a labile, latent viral structure. Cell 61(2):213-222.
7. Pan X, Baldauf HM, Keppler OT, Fackler OT (2013) Restrictions to HIV-1 replication in resting CD4+ T lymphocytes. Cell Res 23(7):876-885.
8. Bergamaschi A, 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(10):4854-4860.
9. Fujita M, et al. (2008) Vpx is critical for reverse transcription of the human immunodeficiency virus type 2 genome in macrophages. J Virol 82(15):7752-7756.
10. 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(13):6263-6274.
11. Baldauf HM, et al. (2012) SAMHD1 restricts HIV-1 infection in resting CD4(+) T cells. Nat Med 18(11):1682-1687.
12. Descours B, et al. (2012) SAMHD1 restricts HIV-1 reverse transcription in quiescent CD4(+) T-cells. Retrovirology 9:87.
13. 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.
14. Srivastava S, 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(5):e1000059.
15. 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(9):5088-5091.
16. Goldstone DC, et al. (2011) HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase. Nature 480(7377):379-382.
17. Hrecka K, et al. (2011) Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474(7353):658-661.
18. Laguette N, et al. (2011) SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474(7353):654-657.
19. Lahouassa H, et al. (2012) SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat Immunol 13(3):223-228.
20. Lim ES, et al. (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(2):194-204.
21. Cribier A, Descours B, Valadão AL, Laguette N, Benkirane M (2013) Phosphorylation of SAMHD1 by cyclin A2/CDK1 regulates its restriction activity toward HIV-1. Cell Reports 3(4):1036-1043.
22. White TE, et al. (2013) The retroviral restriction ability of SAMHD1, but not its deoxynucleotide triphosphohydrolase activity, is regulated by phosphorylation. Cell Host Microbe 13(4):441-451.
23. Schmidt S, et al. (2015) SAMHD1's protein expression profile in humans. J Leukoc Biol 98(1):5-14.
24. Reinhard C, Bottinelli D, Kim B, 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.
25. Plesa G, et al. (2007) Addition of deoxynucleosides enhances human immunodeficiency virus type 1 integration and 2LTR formation in resting CD4+ T cells. J Virol 81(24):13938-13942.
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(26):21570-21574.
27. Schaller T, Bauby H, Hué S, Malim MH, Goujon C (2014) New insights into an X-traordinary viral protein. Front Microbiol 5:126.
28. Berger A, et al. (2011) SAMHD1-deficient CD14+ cells from individuals with Aicardi-Goutières syndrome are highly susceptible to HIV-1 infection. PLoS Pathog 7(12):e1002425.
29. Schwefel D, et al. (2015) Molecular determinants for recognition of divergent SAMHD1 proteins by the lentiviral accessory protein Vpx. Cell Host Microbe 17(4):489-499.
30. Schwefel D, et al. (2014) Structural basis of lentiviral subversion of a cellular protein degradation pathway. Nature 505(7482):234-238.
31. Fregoso OI, et al. (2013) Evolutionary toggling of Vpx/Vpr specificity results in divergent recognition of the restriction factor SAMHD1. PLoS Pathog 9(7):e1003496.
32. Li J, et al. (2015) Characterization of the interactions between SIVrcm Vpx and redcapped mangabey SAMHD1. Biochem J 468(2):303-313.
33. Kewalramani VN, Emerman M (1996) Vpx association with mature core structures of HIV-2. Virology 218(1):159-168.
34. Ambrose Z, Aiken C (2014) HIV-1 uncoating: Connection to nuclear entry and regulation by host proteins. Virology 454-455:371-379.
35. Campbell EM, Hope TJ (2015) HIV-1 capsid: The multifaceted key player in HIV-1 infection. Nat Rev Microbiol 13(8):471-483.
36. Ayinde D, Casartelli N, Schwartz O (2012) Restricting HIV the SAMHD1 way: Through nucleotide starvation. Nat Rev Microbiol 10(10):675-680.
37. Gramberg T, Sunseri N, Landau NR (2010) Evidence for an activation domain at the amino terminus of simian immunodeficiency virus Vpx. J Virol 84(3):1387-1396.
38. Goffinet C, Allespach I, Keppler OT (2007) HIV-susceptible transgenic rats allow rapid preclinical testing of antiviral compounds targeting virus entry or reverse transcription. Proc Natl Acad Sci USA 104(3):1015-1020.
39. Keppler OT, et al. (2005) Rodent cells support key functions of the human immunodeficiency virus type 1 pathogenicity factor Nef. J Virol 79(3):1655-1665.
40. Pizzato M, et al. (2009) A one-step SYBR Green I-based product-enhanced reverse transcriptase assay for the quantitation of retroviruses in cell culture supernatants. J Virol Methods 156(1-2):1-7.
41. Diamond TL, et al. (2004) Macrophage tropism of HIV-1 depends on efficient cellular dNTP utilization by reverse transcriptase. J Biol Chem 279(49):51545-51553.