Cyclin D3-dependent control of the dNTP pool and HIV-1 replication in human macrophages

References

• Gao WY, Cara A, Gallo RC, Lori F. Low levels of deoxynucleotides in peripheral blood lymphocytes: a strategy to inhibit human immunodeficiency virus type 1 replication. Proc Natl Acad Sci USA 1993; 90:8925–8; PMID:7692440; http://dx.doi.org/10.1073/pnas.90.19.8925
   PubMed Web of Science ®Google Scholar
• Meyerhans A, Vartanian JP, Hultgren C, Plikat U, Karlsson A, Wang L, Eriksson S, Wain-Hobson S. Restriction and enhancement of human immunodeficiency virus type 1 replication by modulation of intracellular deoxynucleoside triphosphate pools. J Virol 1994; 68:535–40; PMID:8254768
   PubMed Web of Science ®Google Scholar
• Lori F, Malykh A, Cara A, Sun D, Weinstein JN, Lisziewicz J, Gallo RC. Hydroxyurea as an inhibitor of human immunodeficiency virus-type 1 replication. Science 1994; 266:801–5; PMID:7973634; http://dx.doi.org/10.1126/science.7973634
   PubMed Web of Science ®Google Scholar
• Goldstone DC, Ennis-Adeniran V, Hedden JJ, Groom HC, Rice GI, Christodoulou E, Walker PA, Kelly G, Haire LF, Yap MW, et al. HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase. Nature 2011; 480:379–82; PMID:22056990; http://dx.doi.org/10.1038/nature10623
   PubMed Web of Science ®Google Scholar
• Lahouassa H, Daddacha W, Hofmann H, Ayinde D, Logue EC, Dragin L, Bloch N, Maudet C, Bertrand M, Gramberg T, et al. SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat Immunol 2012; 13:223–8; PMID:22327569; http://dx.doi.org/10.1038/ni.2236
   PubMed Web of Science ®Google Scholar
• Hrecka K, Hao C, Gierszewska M, Swanson SK, Kesik-Brodacka M, Srivastava S, Florens L, Washburn MP, Skowronski J. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 2011; 474:658–61; PMID:21720370; http://dx.doi.org/10.1038/nature10195
   PubMed Web of Science ®Google Scholar
• 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; 474:654–7; PMID:21613998; http://dx.doi.org/10.1038/nature10117
   PubMed Web of Science ®Google Scholar
• Baldauf HM, Pan X, Erikson E, Schmidt S, Daddacha W, Burggraf M, Schenkova K, Ambiel I, Wabnitz G, Gramberg T, et al. SAMHD1 restricts HIV-1 infection in resting CD4(+) T cells. Nat Med 2012; 18:1682–9; PMID:22972397; http://dx.doi.org/10.1038/nm.2964
   PubMed Web of Science ®Google Scholar
• Hollenbaugh JA, Gee P, Baker J, Daly MB, Amie SM, Tate J, Kasai N, Kanemura Y, Kim DH, Ward BM, et al. Host factor SAMHD1 restricts DNA viruses in non-dividing myeloid cells. PLoS Pathog 2013; 9:e1003481; PMID:23825958; http://dx.doi.org/10.1371/journal.ppat.1003481
   PubMed Web of Science ®Google Scholar
• Pauls E, Ballana E, Este JA. Nucleotide embargo by SAMHD1: a strategy to block retroviral infection. Antiviral Res 2013; 97:180–2; PMID:23266292; http://dx.doi.org/10.1016/j.antiviral.2012.12.009
   PubMed Web of Science ®Google Scholar
• St Gelais C, de Silva S, Amie SM, Coleman CM, Hoy H, Hollenbaugh JA, Kim B, Wu L. 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 2012; 9:105; PMID:23231760; http://dx.doi.org/10.1186/1742-4690-9-105
   PubMed Web of Science ®Google Scholar
• 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; PMID:23092122; http://dx.doi.org/10.1186/1742-4690-9-87
   PubMed Web of Science ®Google Scholar
• Behrendt R, Schumann T, Gerbaulet A, Nguyen LA, Schubert N, Alexopoulou D, Berka U, Lienenklaus S, Peschke K, Gibbert K, et al. Mouse SAMHD1 has antiretroviral activity and suppresses a spontaneous cell-intrinsic antiviral response. Cell Rep 2013; 4:689–96; PMID:23972988; http://dx.doi.org/10.1016/j.celrep.2013.07.037
   PubMed Web of Science ®Google Scholar
• Rehwinkel J, Maelfait J, Bridgeman A, Rigby R, Hayward B, Liberatore RA, Bieniasz PD, Towers GJ, Moita LF, Crow YJ, et al. SAMHD1-dependent retroviral control and escape in mice. EMBO J 2013; 32:2454–62; PMID:23872947; http://dx.doi.org/10.1038/emboj.2013.163
   PubMed Web of Science ®Google Scholar
• Franzolin E, Pontarin G, Rampazzo C, Miazzi C, Ferraro P, Palumbo E, Reichard P, Bianchi V. The deoxynucleotide triphosphohydrolase SAMHD1 is a major regulator of DNA precursor pools in mammalian cells. Proc Natl Acad Sci U S A 2013; 110:14272–7; PMID:23858451; http://dx.doi.org/10.1073/pnas.1312033110
   PubMed Web of Science ®Google Scholar
• Cribier A, Descours B, Valadão Ana Luiza C, Laguette N, Benkirane M. Phosphorylation of SAMHD1 by cyclin A2/CDK1 regulates its restriction activity toward HIV-1. Cell Rep 2013; 3:1036–43; PMID:23602554; http://dx.doi.org/10.1016/j.celrep.2013.03.017
   PubMed Web of Science ®Google Scholar
• Welbourn S, Dutta SM, Semmes OJ, Strebel K. Restriction of virus infection but not catalytic dNTPase activity is regulated by phosphorylation of SAMHD1. J Virol 2013; 87:11516–24; PMID:23966382; http://dx.doi.org/10.1128/JVI.01642-13
   PubMed Web of Science ®Google Scholar
• White Tommy E, Brandariz-Nuñez A, Valle-Casuso Jose C, Amie S, Nguyen Laura 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; 13:441–51; PMID:23601106; http://dx.doi.org/10.1016/j.chom.2013.03.005
   PubMed Web of Science ®Google Scholar
• Pauls E, Ruiz A, Badia R, Permanyer M, Gubern A, Riveira-Munoz E, Torres-Torronteras J, Alvarez M, Mothe B, Brander C, et al. Cell cycle control and HIV-1 susceptibility are linked by CDK6-dependent CDK2 phosphorylation of SAMHD1 in myeloid and lymphoid cells. J Immunol 2014; 193:1988–97; PMID:25015816; http://dx.doi.org/10.4049/jimmunol.1400873
   PubMed Web of Science ®Google Scholar
• St Gelais C, de Silva S, Hach JC, White TE, Diaz-Griffero F, Yount JS, Wu L. Identification of cellular proteins interacting with the retroviral restriction factor SAMHD1. J Virol 2014; 88:5834–44; PMID:24623419; http://dx.doi.org/10.1128/JVI.00155-14
   PubMed Web of Science ®Google Scholar
• Pauls E, Badia R, Torres-Torronteras J, Ruiz A, Permanyer M, Riveira-Munoz E, Clotet B, Marti R, Ballana E, Este JA. Palbociclib, a selective inhibitor of cyclin-dependent kinase4/6, blocks HIV-1 reverse transcription through the control of sterile alpha motif and HD domain-containing protein-1 activity. AIDS 2014; 28:2213–23; PMID:25036183; http://dx.doi.org/10.1097/QAD.0000000000000399
   PubMed Web of Science ®Google Scholar
• Pauls E, Ruiz A, Riveira-Munoz E, Permanyer M, Badia R, Clotet B, Keppler OT, Ballana E, Este JA. p21 regulates the HIV-1 restriction factor SAMHD1. Proc Natl Acad Sci U S A 2014; 111:E1322–4; PMID:24610778; http://dx.doi.org/10.1073/pnas.1322059111
   PubMed Web of Science ®Google Scholar
• Wells AD, Morawski PA. New roles for cyclin-dependent kinases in T cell biology: linking cell division and differentiation. Nat Rev Immunol 2014; 14:261–70; PMID:24603166; http://dx.doi.org/10.1038/nri3625
   PubMed Web of Science ®Google Scholar
• Kohrt D, Crary J, Zimmer M, Patrick AN, Ford HL, Hinds PW, Grossel MJ. CDK6 binds and promotes the degradation of the EYA2 protein. Cell Cycle 2014; 13:62–71; PMID:24196439; http://dx.doi.org/10.4161/cc.26755
   PubMed Web of Science ®Google Scholar
• Grossel MJ, Hinds PW. From cell cycle to differentiation: an expanding role for Cdk6. Cell Cycle 2005; 5:266–70; PMID:16410727; http://dx.doi.org/10.4161/cc.5.3.2385
   PubMed Web of Science ®Google Scholar
• Miyazaki T, Arai S. Two distinct controls of mitotic Cdk1/Cyclin B1 activity requisite for cell growth prior to cell division. Cell Cycle 2007; 6:1418–24; PMID:17592253; http://dx.doi.org/10.4161/cc.6.12.4409
   PubMed Web of Science ®Google Scholar
• Malumbres M, Harlow E, Hunt T, Hunter T, Lahti JM, Manning G, Morgan DO, Tsai LH, Wolgemuth DJ. Cyclin-dependent kinases: a family portrait. Nat Cell Biol 2009; 11:1275–6; PMID:19884882; http://dx.doi.org/10.1038/ncb1109-1275
   PubMed Web of Science ®Google Scholar
• Ballana E, Este JA. Insights from host genomics into HIV infection and disease: identification of host targets for drug development. Antivir Res 2013; 100:473–786; PMID:24084487; http://dx.doi.org/10.1016/j.antiviral.2013.09.017
   PubMed Web of Science ®Google Scholar
• Sawai CM, Freund J, Oh P, Ndiaye-Lobry D, Bretz JC, Strikoudis A, Genesca L, Trimarchi T, Kelliher MA, Clark M, et al. Therapeutic targeting of the cyclin D3:CDK4/6 complex in T cell leukemia. Cancer Cell 2012; 22:452–65; PMID:23079656; http://dx.doi.org/10.1016/j.ccr.2012.09.016
   PubMed Web of Science ®Google Scholar
• Paternot S, Colleoni B, Bisteau X, Roger PP. The CDK4/CDK6 inhibitor PD0332991 paradoxically stabilizes activated cyclin D3-CDK4/6 complexes. Cell Cycle 2014; 13:2879–88; PMID:25486476; http://dx.doi.org/10.4161/15384101.2014.946841
   PubMed Web of Science ®Google Scholar
• Ryoo J, Choi J, Oh C, Kim S, Seo M, Kim SY, Seo D, Kim J, White TE, Brandariz-Nunez A, et al. The ribonuclease activity of SAMHD1 is required for HIV-1 restriction. Nat Med 2014; 20:936–41; PMID:25038827; http://dx.doi.org/10.1038/nm.3626
   PubMed Web of Science ®Google Scholar
• Hofmann H, Norton TD, Schultz ML, Polsky SB, Sunseri N, Landau NR. Inhibition of CUL4A Neddylation causes a reversible block to SAMHD1-mediated restriction of HIV-1. J Virol 2013; 87:11741–50; PMID:23986575; http://dx.doi.org/10.1128/JVI.02002-13
   PubMed Web of Science ®Google Scholar
• Kyei GB, Cheng X, Ramani R, Ratner L. Cyclin L2 is a critical HIV dependency factor in macrophages that controls SAMHD1 abundance. Cell Host Microbe 2014; 17:1–9
   Web of Science ®Google Scholar
• Ballana E, Badia R, Terradas G, Torres-Torronteras J, Ruiz A, Pauls E, Riveira-Muñoz E, Clotet B, Martí R, Esté JA. SAMHD1 specifically affects the antiviral potency of thymidine analog HIV reverse transcriptase inhibitors. Antimicrob Agents Chemoth 2014; 58:4804–13; PMID:24913159; http://dx.doi.org/10.1128/AAC.03145-14
   PubMed Web of Science ®Google Scholar
• Descours B, Cribier A, Chable-Bessia C, Ayinde D, Rice G, Crow Y, Yatim A, Schawartz O, Laguette N, Benkirane M. SAMHD1 restricts HIV-1 reverse transcription in quiescent CD4+ T-cells. Retrovirology 2012; 9:87; PMID:23092122; http://dx.doi.org/10.1186/1742-4690-9-87
   PubMed Web of Science ®Google Scholar
• Blanco J, Barretina J, Clotet B, Este JA. R5 HIV gp120-mediated cellular contacts induce the death of single CCR5-expressing CD4 T cells by a gp41-dependent mechanism. J Leukoc Biol 2004; 76:804–11; PMID:15258189; http://dx.doi.org/10.1189/jlb.0204100
   PubMed Web of Science ®Google Scholar
• Pauls E, Jimenez E, Ruiz A, Permanyer M, Ballana E, Costa H, Nascimiento R, Parkhouse RM, Pena R, Riveiro-Munoz E, et al. Restriction of HIV-1 replication in primary macrophages by IL-12 and IL-18 through the upregulation of SAMHD1. J Immunol 2013; 190:4736–41; PMID:23526823; http://dx.doi.org/10.4049/jimmunol.1203226
   PubMed Web of Science ®Google Scholar
• Ruiz A, Pauls E, Badia R, Riveira-Munoz E, Clotet B, Ballana E, Este JA. Characterization of the influence of mediator complex in HIV-1 transcription. J Biol Chem 2014; 289:27665–76; PMID:25100719; http://dx.doi.org/10.1074/jbc.M114.570341
   PubMed Web of Science ®Google Scholar
• Mangeot PE, Negre D, Dubois B, Winter AJ, Leissner P, Mehtali M, Kaiserlian D, Cosset FL, Darlix JL. Development of minimal lentivirus vectors derived from simian immunodeficiency virus (SIVmac251) and their use for gene transfer into human dendritic cells. J Virol 2000; 74:8307–15; PMID:10954529; http://dx.doi.org/10.1128/JVI.74.18.8307-8315.2000
   PubMed Web of Science ®Google Scholar
• Badia R, Pauls E, Riveira-Munoz E, Clotet B, Este JA, Ballana E. Zinc-finger endonuclease targeting PSIP-1 inhibits HIV-1 integration. Antimicrob Agents Chemoth 2014; 58:4318–27; PMID:24820090; http://dx.doi.org/10.1128/AAC.02690-14
   PubMed Web of Science ®Google Scholar
• Gonzalez-Vioque E, Torres-Torronteras J, Andreu AL, Marti R. Limited dCTP availability accounts for mitochondrial DNA depletion in mitochondrial neurogastrointestinal encephalomyopathy (MNGIE). PLoS Genet 2011; 7:e1002035; PMID:21483760; http://dx.doi.org/10.1371/journal.pgen.1002035
   PubMed Web of Science ®Google Scholar