Cyclin-dependent kinases as therapeutic targets for HIV-1 infection

References

• Weiss RA. Thirty years on: HIV receptor gymnastics and the prevention of infection. BCM Biol. 2013 May 21;11:57.
   Google Scholar
• Ambrose Z, Aiken C. HIV-1 uncoating: connection to nuclear entry and regulation by host proteins. Virology. 2014 Apr;454–455:371–379.
   PubMed Web of Science ®Google Scholar
• Francis AC, Marin M, Shi J, et al. Time-resolved imaging of single HIV-1 uncoating in vitro and in living cells. PLoS Pathog. 2016 Jun;12(6):e1005709.
   PubMed Web of Science ®Google Scholar
• Hu WS, Hughes SH. HIV-1 reverse transcription. Cold Spring Harb Perspect Med. 2012 Oct 1;2(10). pii:a006882.
   PubMed Web of Science ®Google Scholar
• Holmes M, Zhang F, Bieniasz PD. Single-cell and single-cycle analysis of HIV-1 replication. PLoS Pathog. 2015 Jun;11(6):e1004961.
   PubMed Web of Science ®Google Scholar
• Craigie R, Bushman FD. HIV DNA integration. Cold Spring Harb Perspect Med. 2012 Jul;2(7):a006890.
   Web of Science ®Google Scholar
• Marini B, Kertesz-Farkas A, Ali H, et al. Nuclear architecture dictates HIV-1 integration site selection. Nature. 2015 May 14;521(7551):227–231.
   PubMed Web of Science ®Google Scholar
• Sloan KE, Gleizes PE, Bohnsack MT. Nucleocytoplasmic transport of RNAs and RNA-protein complexes. J Mol Biol. 2016 May 22;428(10 Pt A):2040–2059.
   PubMed Web of Science ®Google Scholar
• De CE, Li G. Approved antiviral drugs over the past 50 years. Clin Microbiol Rev. 2016 Jul;29(3):695–747.
   PubMed Web of Science ®Google Scholar
• Jourjy J, Dahl K, Huesgen E. Antiretroviral treatment efficacy and safety in older HIV-infected adults. Pharmacotherapy. 2015 Dec;35(12):1140–1151.
   PubMed Web of Science ®Google Scholar
• Siliciano JD, Siliciano RF. A long-term latent reservoir for HIV-1: discovery and clinical implications. J Antimicrob Chemother. 2004 Jul;54(1):6–9.
   PubMed Web of Science ®Google Scholar
• Lenasi T, Contreras X, Peterlin BM. Transcriptional interference antagonizes proviral gene expression to promote HIV latency. Cell Host Microbe. 2008 Aug 14;4(2):123–133.
   PubMed Web of Science ®Google Scholar
• Shan L, Yang HC, Rabi SA, et al. Influence of host gene transcription level and orientation on HIV-1 latency in a primary-cell model. J Virol. 2011 Jun;85(11):5384–5393.
   PubMed Web of Science ®Google Scholar
• Hakre S, Chavez L, Shirakawa K, et al. Epigenetic regulation of HIV latency. Curr Opin HIV AIDS. 2011 Jan;6(1):19–24.
   PubMed Web of Science ®Google Scholar
• Lusic M, Giacca M. Regulation of HIV-1 latency by chromatin structure and nuclear architecture. J Mol Biol. 2015 Feb 13;427(3):688–694.
   PubMed Web of Science ®Google Scholar
• Bullen CK, Laird GM, Durand CM, et al. New ex vivo approaches distinguish effective and ineffective single agents for reversing HIV-1 latency in vivo. Nat Med. 2014 Ap;20(4):425–429.
   PubMed Web of Science ®Google Scholar
• Siliciano JD, Siliciano RF. Recent developments in the search for a cure for HIV-1 infection: targeting the latent reservoir for HIV-1. J Allergy Clin Immunol. 2014 Jul;134(1):12–19.
   PubMed Web of Science ®Google Scholar
• Ho YC, Shan L, Hosmane NN, et al. Replication-competent noninduced proviruses in the latent reservoir increase barrier to HIV-1 cure. Cell. 2013 Oct 24;155(3):540–551.
   PubMed Web of Science ®Google Scholar
• Iordanskiy S, Kashanchi F. Potential of radiation-induced cellular stress for reactivation of latent HIV-1 and killing of infected cells. AIDS Res Hum Retroviruses. 2016 Feb;32(2):120–124.
   PubMed Web of Science ®Google Scholar
• Lorenzo-Redondo R, Fryer HR, Bedford T, et al. Persistent HIV-1 replication maintains the tissue reservoir during therapy. Nature. 2016 Feb 4;530(7588):51–56.
   PubMed Web of Science ®Google Scholar
• Malumbres M. Cyclin-dependent kinases. Genome Biol. 2014;15(6):122.
   PubMed Web of Science ®Google Scholar
• Evans T, Rosenthal ET, Youngblom J, et al. Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell. 1983 Jun;33(2):389–396.
   PubMed Web of Science ®Google Scholar
• Fisher RP. The CDK network: linking cycles of cell division and gene expression. Genes Cancer. 2012 Nov;3(11–12):731–738.
   PubMedGoogle Scholar
• White TE, Brandariz-Nuñez A, Valle-Casuso JC, et al. The retroviral restriction ability of SAMHD1, but not its deoxynucleotide triphosphohydrolase activity, is regulated by phosphorylation. Cell Host Microbe. 2013 Apr 17;13(4):441–451.
   PubMed Web of Science ®Google Scholar
• Cribier A, Descours B, Valadão ALC, et al. Phosphorylation of SAMHD1 by cyclin A2/CDK1 regulates its restriction activity toward HIV-1. Cell Rep. 2013 Apr 25;3(4):1036–1043.
   PubMed Web of Science ®Google Scholar
• Pauls E, Ruiz A, Badia R, 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 Aug 15;193(4):1988–1997.
   PubMed Web of Science ®Google Scholar
• St GC, de SS, Hach JC, et al. Identification of cellular proteins interacting with the retroviral restriction factor SAMHD1. J Virol. 2014 May;88(10):5834–5844.
   PubMed Web of Science ®Google Scholar
• Kyei GB, Cheng X, Ramani R, et al. Cyclin L2 is a critical HIV dependency factor in macrophages that controls SAMHD1 abundance. Cell Host Microbe. 2015 Jan 14;17(1):98–106.
   PubMed Web of Science ®Google Scholar
• Nekhai S, Zhou M, Fernandez A, et al. HIV-1 Tat-associated RNA polymerase C-terminal domain kinase, CDK2, phosphorylates CDK7 and stimulates Tat-mediated transcription. Biochem J. 2002 Jun 15;364(Pt 3):649–657.
   PubMed Web of Science ®Google Scholar
• Ammosova T, Berro R, Jerebtsova M, et al. Phosphorylation of HIV-1 Tat by CDK2 in HIV-1 transcription. Retrovirology. 2006;3:78.
   PubMed Web of Science ®Google Scholar
• Breuer D, Kotelkin A, Ammosova T, et al. CDK2 regulates HIV-1 transcription by phosphorylation of CDK9 on serine 90. Retrovirology. 2012;9:94.
   PubMed Web of Science ®Google Scholar
• Kim YK, Bourgeois CF, Pearson R, et al. Recruitment of TFIIH to the HIV LTR is a rate-limiting step in the emergence of HIV from latency. EMBO J. 2006 Aug 9;25(15):3596–3604.
   PubMed Web of Science ®Google Scholar
• Zhou Q, Li T, Price DH. RNA polymerase II elongation control. Annu Rev Biochem. 2012;81:119–143.
   PubMed Web of Science ®Google Scholar
• Mbonye U, Karn J. Transcriptional control of HIV latency: cellular signaling pathways, epigenetics, happenstance and the hope for a cure. Virology. 2014 Apr;454–455:328–339.
   PubMed Web of Science ®Google Scholar
• Taube R, Peterlin M. Lost in transcription: molecular mechanisms that control HIV latency. Viruses. 2013 Mar;5(3):902–927.
   PubMed Web of Science ®Google Scholar
• Pak V, Eifler TT, Jäger S, et al. CDK11 in TREX/THOC regulates HIV mRNA 3ʹ end processing. Cell Host Microbe. 2015 Nov 11; 18(5):560–570.
   PubMed Web of Science ®Google Scholar
• Berro R, Pedati C, Kehn-Hall K, et al. CDK13, a new potential human immunodeficiency virus type 1 inhibitory factor regulating viral mRNA splicing. J Virol. 2008 Jul;82(14):7155–7166.
   PubMed Web of Science ®Google Scholar
• Fletcher TM III, Brichacek B, Sharova N, et al. 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 Nov 15;15(22):6155–6165.
   PubMed Web of Science ®Google Scholar
• Hrecka K, Hao C, Gierszewska M, et al. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature. 2011 Jun 30;474(7353):658–661.
   PubMed Web of Science ®Google Scholar
• Laguette N, Sobhian B, Casartelli N, et al. SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature. 2011 Jun 30;474(7353):654–657.
   PubMed Web of Science ®Google Scholar
• Tahirov TH, Babayeva ND, Varzavand K, et al. Crystal structure of HIV-1 Tat complexed with human P-TEFb. Nature. 2010 Jun 10; 465(7299):747–751.
   PubMed Web of Science ®Google Scholar
• Smith E, Lin C, Shilatifard A. The super elongation complex (SEC) and MLL in development and disease. Genes Dev. 2011 Apr 1;25(7):661–672.
   PubMed Web of Science ®Google Scholar
• Gudipaty SA, D’Orso I. Functional interplay between PPM1G and the transcription elongation machinery. RNA Dis. 2016;3(1). pii:e1215.
   PubMedGoogle Scholar
• Peng J, Zhu Y, Milton JT, et al. Identification of multiple cyclin subunits of human P-TEFb. Genes Dev. 1998;12(5):755–762.
   PubMed Web of Science ®Google Scholar
• Bisgrove DA, Mahmoudi T, Henklein P, et al. Conserved P-TEFb-interacting domain of BRD4 inhibits HIV transcription. Proc Natl Acad Sci U S A. 2007 Aug 21;104(34):13690–13695.
   PubMed Web of Science ®Google Scholar
• Li Z, Guo J, Wu Y, et al. The BET bromodomain inhibitor JQ1 activates HIV latency through antagonizing Brd4 inhibition of Tat-transactivation. Nucleic Acids Res. 2013 Jan 7;41(1):277–287.
   Web of Science ®Google Scholar
• Banerjee C, Archin N, Michaels D, et al. BET bromodomain inhibition as a novel strategy for reactivation of HIV-1. J Leukoc Biol. 2012 Dec;92(6):1147–1154.
   PubMed Web of Science ®Google Scholar
• Zhu J, Gaiha GD, John SP, et al. Reactivation of latent HIV-1 by inhibition of BRD4. Cell Rep. 2012 Oct 25;2(4):807–816.
   PubMed Web of Science ®Google Scholar
• Boehm D, Calvanese V, Dar RD, et al. BET bromodomain-targeting compounds reactivate HIV from latency via a Tat-independent mechanism. Cell Cycle. 2013 Feb 1;12(3):452–462.
   PubMed Web of Science ®Google Scholar
• He N, Liu M, Hsu J, et al. HIV-1 Tat and host AFF4 recruit two transcription elongation factors into a bifunctional complex for coordinated activation of HIV-1 transcription. Mol Cell. 2010 May 14;38(3):428–438.
   PubMed Web of Science ®Google Scholar
• Sobhian B, Laguette N, Yatim A, et al. HIV-1 Tat assembles a multifunctional transcription elongation complex and stably associates with the 7SK snRNP. Mol Cell. 2010 May 14;38(3):439–451.
   PubMed Web of Science ®Google Scholar
• Sedore SC, Byers SA, Biglione S, et al. Manipulation of P-TEFb control machinery by HIV: recruitment of P-TEFb from the large form by Tat and binding of HEXIM1 to TAR. Nucleic Acids Res. 2007;35(13):4347–4358.
   PubMed Web of Science ®Google Scholar
• Barboric M, Yik JH, Czudnochowski N, et al. Tat competes with HEXIM1 to increase the active pool of P-TEFb for HIV-1 transcription. Nucleic Acids Res. 2007 Mar 6;35:2003–2012.
   PubMed Web of Science ®Google Scholar
• Schulte A, Czudnochowski N, Barboric M, et al. Identification of a cyclin T-binding domain in Hexim1 and biochemical analysis of its binding competition with HIV-1 Tat. J Biol Chem. 2005 Jul 1;280(26):24968–24977.
   PubMed Web of Science ®Google Scholar
• D’Orso I, Jang GM, Pastuszak AW, et al. Transition step during assembly of HIV tat: P-TEFbTranscription complexes and transfer to TAR RNA. Mol Cell Biol. 2012 Dec;32(23):4780–4793.
   PubMed Web of Science ®Google Scholar
• McNamara RP, McCann JL, Gudipaty SA, et al. Transcription factors mediate the enzymatic disassembly of promoter-bound 7SK snRNP to locally recruit P-TEFb for transcription elongation. Cell Rep. 2013 Dec 12;5(5):1256–1268.
   PubMed Web of Science ®Google Scholar
• Kim YK, Mbonye U, Hokello J, et al. T-cell receptor signaling enhances transcriptional elongation from latent HIV proviruses by activating P-TEFb through an ERK-dependent pathway. J Mol Biol. 2011 Jul 29;410(5):896–916.
   PubMed Web of Science ®Google Scholar
• Sung TL, Rice AP. Effects of prostratin on Cyclin T1/P-TEFb function and the gene expression profile in primary resting CD4+ T cells. Retrovirology. 2006;3:66.
   PubMed Web of Science ®Google Scholar
• Herrmann CH, Carroll RG, Wei P, et al. Tat-associated kinase, TAK, activity is regulated by distinct mechanisms in peripheral blood lymphocytes and promonocytic cell lines. J Virol. 1998 Dec;72(12):9881–9888.
   PubMed Web of Science ®Google Scholar
• Ghose R, Liou LY, Herrmann CH, et al. Induction of TAK (cyclin T1/P-TEFb) in purified resting CD4(+) T lymphocytes by combination of cytokines. J Virol JID - 0113724. 2001 Dec;75(23):11336–11343.
   PubMed Web of Science ®Google Scholar
• Liu H, Herrmann CH. Differential localization and expression of the Cdk9 42k and 55k isoforms. J Cell Physiol. 2005 Apr;203(1):251–260.
   PubMed Web of Science ®Google Scholar
• Yu W, Ramakrishnan R, Wang Y, et al. Cyclin T1-dependent genes in activated CD4 T and macrophage cell lines appear enriched in HIV-1 co-factors. PLoS ONE. 2008 Sep 5;3(9):e3146.
   PubMed Web of Science ®Google Scholar
• Chiang K, Sung TL, Rice AP. Regulation of cyclin T1 and HIV-1 replication by microRNAs in resting CD4+ T lymphocytes. J Virol. 2012 Mar;86(6):3244–3252.
   PubMed Web of Science ®Google Scholar
• Haaland RE, Herrmann CH, Rice AP. Increased association of 7SK snRNA with Tat cofactor P-TEFb following activation of peripheral blood lymphocytes. Aids. 2003 Nov 21;17(17):2429–2436.
   PubMed Web of Science ®Google Scholar
• Ramakrishnan R, Dow EC, Rice AP. Characterization of Cdk9 T-loop phosphorylation in resting and activated CD4(+) T lymphocytes. J Leukoc Biol. 2009 Dec;86(6):1345–1350.
   PubMed Web of Science ®Google Scholar
• Larochelle S, Amat R, Glover-Cutter K, et al. Cyclin-dependent kinase control of the initiation-to-elongation switch of RNA polymerase II. Nat Struct Mol Biol. 2012 Nov;19(11):1108–1115.
   PubMed Web of Science ®Google Scholar
• Budhiraja S, Ramakrishnan R, Rice AP. Phosphatase PPM1A negatively regulates P-TEFb function in resting CD4T+ T cells and inhibits HIV-1 gene expression. Retrovirology. 2012;9:52.
   PubMed Web of Science ®Google Scholar
• Chen R, Liu M, Li H, et al. PP2B and PP1alpha cooperatively disrupt 7SK snRNP to release P-TEFb for transcription in response to Ca2+ signaling. Genes Dev. 2008 May 15;22(10):1356–1368.
   PubMed Web of Science ®Google Scholar
• Mbonye UR, Gokulrangan G, Datt M, et al. Phosphorylation of CDK9 at Ser175 enhances HIV transcription and is a marker of activated P-TEFb in CD4(+) T lymphocytes. PLoS Pathog. 2013 May;9(5):e1003338.
   PubMed Web of Science ®Google Scholar
• Liou LY, Herrmann CH, Rice AP. Transient induction of cyclin T1 during human macrophage differentiation regulates human immunodeficiency virus type 1 Tat transactivation function. J Virol. 2002 Nov;76(21):10579–10587.
   PubMed Web of Science ®Google Scholar
• Dong C, Kwas C, Wu L. Transcriptional restriction of human immunodeficiency virus type 1 gene expression in undifferentiated primary monocytes. J Virol. 2009 Apr;83(8):3518–3527.
   PubMed Web of Science ®Google Scholar
• Sung TL, Rice AP. miR-198 inhibits HIV-1 gene expression and replication in monocytes and its mechanism of action appears to involve repression of cyclin T1. PLoS Pathog. 2009 Jan;5(1):e1000263.
   PubMed Web of Science ®Google Scholar
• Wang Y, Rice AP. Interleukin-10 inhibits HIV-1 LTR-directed gene expression in human macrophages through the induction of cyclin T1 proteolysis. Virology. 2006 Sep 1;352(2):485–492.
   PubMed Web of Science ®Google Scholar
• Liou LY, Herrmann CH, Rice AP. Human immunodeficiency virus type 1 infection induces cyclin T1 expression in macrophages. J Virol. 2004 Aug;78(15):8114–8119.
   PubMed Web of Science ®Google Scholar
• Liou LY, Haaland RE, Herrmann CH, et al. Cyclin T1 but not cyclin T2a is induced by a post-transcriptional mechanism in PAMP-activated monocyte-derived macrophages. J Leukoc Biol. 2006 Feb;79(2):388–396.
   PubMed Web of Science ®Google Scholar
• Budhiraja S, Famiglietti M, Bosque A, et al. Cyclin T1 and CDK9 T-loop phosphorylation are downregulated during establishment of HIV-1 latency in primary resting memory CD4+ T cells. J Virol. 2013 Jan;87(2):1211–1220.
   PubMed Web of Science ®Google Scholar
• Bartholomeeusen K, Fujinaga K, Xiang Y, et al. HDAC inhibitors that release positive transcription elongation factor b (P-TEFb) from its inhibitory complex also activate HIV transcription. J Biol Chem. 2013 May 17;288(20):14400–14407.
   PubMed Web of Science ®Google Scholar
• Liu W, Ma Q, Wong K, et al. Brd4 and JMJD6-associated anti-pause enhancers in regulation of transcriptional pause release. Cell. 2013 Dec 19;155(7):1581–1595.
   PubMed Web of Science ®Google Scholar
• Ji X, Zhou Y, Pandit S, et al. SR proteins collaborate with 7SK and promoter-associated nascent RNA to release paused polymerase. Cell. 2013 May 9;153(4):855–868.
   PubMed Web of Science ®Google Scholar
• Dow EC, Liu H, Rice AP. T-loop phosphorylated Cdk9 localizes to nuclear speckle domains which may serve as sites of active P-TEFb function and exchange between the Brd4 and 7SK/HEXIM1 regulatory complexes. J Cell Physiol. 2010 Jul;224(1):84–93.
   PubMed Web of Science ®Google Scholar
• Fujinaga K, Luo Z, Peterlin BM. Genetic analysis of the structure and function of 7SK small nuclear ribonucleoprotein (snRNP) in cells. J Biol Chem. 2014 Jul 25;289(30):21181–21190.
   PubMed Web of Science ®Google Scholar
• Yang Z, Zhu Q, Luo K, et al. The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature JID - 0410462. 2001 Nov 15;414(6861):317–322.
   PubMed Web of Science ®Google Scholar
• Nguyen VT, Kiss T, Michels AA, et al. 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes. Nature JID - 0410462. 2001 Nov 15;414(6861):322–325.
   PubMed Web of Science ®Google Scholar
• Fujinaga K, Barboric M, Li Q, et al. PKC phosphorylates HEXIM1 and regulates P-TEFb activity. Nucleic Acids Res. 2012 Oct;40(18):9160–9170.
   PubMed Web of Science ®Google Scholar
• Cary DC, Fujinaga K, Peterlin BM. Molecular mechanisms of HIV latency. J Clin Invest. 2016 Feb;126(2):448–454.
   PubMed Web of Science ®Google Scholar
• Gudipaty SA, McNamara RP, Morton EL, et al. PPM1G binds 7SK RNA and hexim1 to block P-TEFb assembly into the 7SK snRNP and sustain transcription elongation. Mol Cell Biol. 2015 Nov;35(22):3810–3828.
   PubMed Web of Science ®Google Scholar
• Contreras X, Barboric M, Lenasi T, et al. HMBA releases P-TEFb from HEXIM1 and 7SK snRNA via PI3K/Akt and activates HIV transcription. PLoS Pathog. 2007 Oct 12;3(10):1459–1469.
   PubMed Web of Science ®Google Scholar
• Valente ST, Gilmartin GM, Mott C, et al. Inhibition of HIV-1 replication by eIF3f. Proc Natl Acad Sci U S A. 2009 Mar 17;106(11):4071–4078.
   PubMed Web of Science ®Google Scholar
• Shi J, Feng Y, Goulet AC, et al. The p34cdc2-related cyclin-dependent kinase 11 interacts with the p47 subunit of eukaryotic initiation factor 3 during apoptosis. J Biol Chem. 2003 Feb 14;278(7):5062–5071.
   PubMed Web of Science ®Google Scholar
• Tyagi M, Pearson RJ, Karn J. Establishment of HIV latency in primary CD4+ cells is due to epigenetic transcriptional silencing and P-TEFb restriction. J Virol. 2010 Jul;84(13):6425–6437.
   PubMed Web of Science ®Google Scholar
• Beans EJ, Fournogerakis D, Gauntlett C, et al. Highly potent, synthetically accessible prostratin analogs induce latent HIV expression in vitro and ex vivo. Proc Natl Acad Sci U S A. 2013 Jul 16;110(29):11698–11703.
   PubMed Web of Science ®Google Scholar
• Pandeló José JD, Bartholomeeusen K, Da Cunha RD, et al. Reactivation of latent HIV-1 by new semi-synthetic ingenol esters. Virology. 2014;462–463:328–339.
   PubMed Web of Science ®Google Scholar
• Spivak AM, Bosque A, Balch AH, et al. Ex vivo bioactivity and HIV-1 latency reversal by ingenol dibenzoate and panobinostat in resting CD4(+) T cells from aviremic patients. Antimicrob Agents Chemother. 2015 Oct;59(10):5984–5991.
   PubMed Web of Science ®Google Scholar
• Jiang G, Mendes EA, Kaiser P, et al. Synergistic reactivation of latent HIV expression by ingenol-3-angelate, PEP005, targeted NF-kB signaling in combination with JQ1 induced p-TEFb activation. PLoS Pathog. 2015 Jul;11(7):e 005066.
   Web of Science ®Google Scholar
• Jamaluddin MS, Hu PW, Danels YJ, et al. The broad spectrum histone deacetylase inhibitors vorinostat and panobinostat activate latent HIV in CD4+ T cells in part through phosphorylation of the T-loop of the CDK9 subunit of P-TEFb. AIDS Res Hum Retroviruses. 2016 Feb;32(2):169–173.
   PubMed Web of Science ®Google Scholar
• Ramakrishnan R, Liu H, Rice AP. SAHA (Vorinostat) induces CDK9 thr-186 (T-Loop) phosphorylation in resting CD4 T cells: implications for reactivation of latent HIV. AIDS Res Hum Retroviruses. 2015 Jan;31(1):137–141.
   PubMed Web of Science ®Google Scholar