985
Views
17
CrossRef citations to date
0
Altmetric
Review

Roles of CDKs in RNA polymerase II transcription of the HIV-1 genome

Pages 111-117 | Received 17 Sep 2018, Accepted 23 Oct 2018, Published online: 15 Nov 2018

References

  • Mbonye U, Karn J. The molecular basis for human immunodeficiency virus latency. Annu Rev Virol. 2017;4:261–285.
  • Mbonye U, Karn J. Transcriptional control of HIV latency: cellular signaling pathways, epigenetics, happenstance and the hope for a cure. Virology. 2014;454-455:328–339.
  • Giffin MJ, Stroud JC, Bates DL, et al. Structure of NFAT1 bound as a dimer to the HIV-1 LTR kappa B element. Nat Struct Biol. 2003;10:800–806.
  • Bosque A, Planelles V. Induction of HIV-1 latency and reactivation in primary memory CD4+ T cells. Blood. 2009;113:58–65.
  • Bosque A, Planelles V. Studies of HIV-1 latency in an ex vivo model that uses primary central memory T cells. Methods. 2011;53:54–61.
  • 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;410:896–916.
  • 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;25:3596–3604.
  • Adelman K, Lis JT. Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans. Nat Rev Genet. 2012;13:720–731.
  • Peterlin BM, Price DH. Controlling the elongation phase of transcription with P-TEFb. Mol Cell. 2006;23:297–305.
  • Zhou Q, Li T, Price DH. RNA polymerase II elongation control. Annu Rev Biochem. 2012;81:119–143.
  • 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;35:4347–4358.
  • 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.
  • 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;280:24968–24977.
  • 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;38:439–451.
  • Luo Z, Lin C, Shilatifard A. The super elongation complex (SEC) family in transcriptional control. Nat Rev Mol Cell Biol. 2012;13:543–547.
  • 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;38:428–438.
  • Fujinaga K, Irwin D, Huang Y, et al. Dynamics of human immunodeficiency virus transcription: P-TEFb phosphorylates RD and dissociates negative effectors from the transactivation response element. Mol Cell Biol. 2004;24:787–795.
  • Yamaguchi Y, Inukai N, Narita T, et al. Evidence that negative elongation factor represses transcription elongation through binding to a DRB sensitivity-inducing factor/RNA polymerase II complex and RNA. Mol Cell Biol. 2002;22:2918–2927.
  • Zhang Z, Klatt A, Gilmour DS, et al. Negative elongation factor NELF represses human immunodeficiency virus transcription by pausing the RNA polymerase II complex. J Biol Chem. 2007;282:16981–16988.
  • Bourgeois CF, Kim YK, Churcher MJ, et al. Spt5 cooperates with human immunodeficiency virus type 1 Tat by preventing premature RNA release at terminator sequences. Mol Cell Biol. 2002;22:1079–1093.
  • Yamada T, Yamaguchi Y, Inukai N, et al. P-TEFb-mediated phosphorylation of hSpt5 C-terminal repeats is critical for processive transcription elongation. Mol Cell. 2006;21:227–237.
  • Herrmann CH, Rice AP. Lentivirus Tat proteins specifically associate with a cellular protein kinase, TAK, that hyperphosphorylates the carboxyl- terminal domain of the large subunit of RNA polymerase II: candidate for a Tat cofactor. J Virol. 1995;69:1612–1620.
  • Zhu Y, Pe’ery T, Peng J, et al. Transcriptional elongation factor p-TEFb is required for HIV-1 Tat transactivation in vitro. Genes Dev. 1997;11:2622–2632.
  • Czudnochowski N, Bosken CA, Geyer M. Serine-7 but not serine-5 phosphorylation primes RNA polymerase II CTD for P-TEFb recognition. Nat Commun. 2012;3:842.
  • Cho EJ, Takagi T, Moore CR, et al. mRNA capping enzyme is recruited to the transcription complex by phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev. 1997;11:3319–3326.
  • Hirose Y, Tacke R, Manley JL. Phosphorylated RNA polymerase II stimulates pre-mRNA splicing. Genes Dev. 1999;13:1234–1239.
  • Komarnitsky P, Cho EJ, Buratowski S, et al. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev. 2000;14:2452–2460.
  • Filippakopoulos P, Picaud S, Mangos M, et al. Histone recognition and large-scale structural analysis of the human bromodomain family. Cell. 2012;149:214–231.
  • Yang Z, Yik JH, Chen R, et al. Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein BRD4. Mol Cell. 2005;19:535–545.
  • Bisgrove DA, Mahmoudi T, Henklein P, et al. Conserved P-TEFb-interacting domain of BRD4 inhibits HIV transcription. Proc Natl Acad Sci USA. 2007;104:13690–13695.
  • Li Z, Fernández-Borges N, Younas N, et al. The KAT5-acetyl-histone4-BRD4 axis silences HIV-1 transcription and promotes viral latency. PLoS Pathog. 2018;14:e1007012.
  • 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.
  • 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;72:9881–9888.
  • 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;75:11336–11343.
  • Chiang K, Sungb TL, Rice AP. Regulation of cyclin T1 and HIV-1 replication by microRNAs in resting CD4+ T lymphocytes. J Virol. 2012;86:3244–3252.
  • O’Keeffe B, Fong Y, Chen D, et al. Requirement for a kinase-specific chaperone pathway in the production of a Cdk9/Cyclin T1 heterodimer responsible for P-TEFb-mediated Tat stimulation of HIV-1 Transcription. J Biol Chem. 2000;275:279–287.
  • Mbonye U, Wang B, Gokulrangan G, et al. Cyclin-dependent kinase 7 (CDK7)-mediated phosphorylation of the CDK9 activation loop promotes P-TEFb assembly with Tat and proviral HIV reactivation. J Biol Chem. 2018;293:10009–10025.
  • Malumbres M. Cyclin-dependent kinases. Genome Biol. 2014;15:122.
  • Ramakrishnan R, Dow EC, Rice AP. Characterization of Cdk9 T-loop phosphorylation in resting and activated CD4(+) T lymphocytes. J Leukoc Biol. 2009;86:1345–1350.
  • 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;19:1108–1115.
  • Budhiraja S, Ramakrishnan R, Rice AP, et al. Phosphatase PPM1A negatively regulates P-TEFb function in resting CD4T+ T cells and inhibits HIV-1 gene expression. Retrovirology. 2012;9:52.
  • 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;22:1356–1368.
  • 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;5:1256–1268.
  • Tyagi M, Iordanskiy S, Ammosova T, et al. Reactivation of latent HIV-1 provirus via targeting protein phosphatase-1. Retrovirology. 2015;12:63.
  • 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;3:e3146.
  • Valente ST, Gilmartin GM, Mott C, et al. Inhibition of HIV-1 replication by eIF3f. Proc Natl Acad Sci USA. 2009;106:4071–4078.
  • Shi J, Feng Y, Goulet A-C, 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;278:5062–5071.
  • Pak V, Eifler TT, Jäger S, et al. CDK11 in TREX/THOC Regulates HIV mRNA 3′ End Processing. Cell Host Microbe. 2015;18:560–570.
  • Ammosova T, Berro R, Jerebtsova M, et al. Phosphorylation of HIV-1 Tat by CDK2 in HIV-1 transcription. Retrovirology. 2006;3:78.
  • Ivanov A, Lin X, Ammosova T, et al. HIV-1 Tat phosphorylation on Ser-16 residue modulates HIV-1 transcription. Retrovirology. 2018;15:39.
  • Breuer D, Stebbings R, Berry N, et al. CDK2 regulates HIV-1 transcription by phosphorylation of CDK9 on serine 90. Retrovirology. 2012;9:94.
  • Allen BL, Taatjes DJ. The Mediator complex: a central integrator of transcription. Nat Rev Mol Cell Biol. 2015;16:155–166.
  • Galbraith MD, Donner AJ, Espinosa JM. CDK8: a positive regulator of transcription. Transcription. 2010;1:4–12.
  • Chen M, Liang J, Ji H, et al. CDK8/19 mediator kinases potentiate induction of transcription by NFkappaB. Proc Natl Acad Sci USA. 2017;114:10208–10213.
  • Gold MO, Rice AP. Targeting of CDK8 to a promoter-proximal RNA element demonstrates catalysis-dependent activation of gene expression. Nucleic Acids Res. 1998;26:3784–3788.
  • Schachter MM, Merrick KA, Larochelle S, et al. A Cdk7-Cdk4 T-loop phosphorylation cascade promotes G1 progression. Mol Cell. 2013;50:250–260.
  • Pace MJ, Agosto L, Graf EH, et al. HIV reservoirs and latency models. Virology. 2011;411:344–354.
  • Karn J. The molecular biology of HIV latency: breaking and restoring the Tat-dependent transcriptional circuit. Curr Opin HIV AIDS. 2011;6:4–11.
  • Lassen K, Han YF, Zhou Y, et al. The multifactorial nature of HIV-1 latency. Trends Mol Med. 2004;10:525–531.
  • Lenasi T, Contreras X, Peterlin BM. Transcriptional interference antagonizes proviral gene expression to promote HIV latency. Cell Host Microbe. 2008;4:123–133.
  • Shan L, Yang H-C, Rabi SA, et al. Influence of host gene transcription level and orientation on HIV-1 latency in a primary-cell model. J Virol. 2011;85:5384–5393.
  • Hakre S, Chavez L, Shirakawa K, et al. Epigenetic regulation of HIV latency. Curr Opin HIV AIDS. 2011;6:19–24.
  • 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;84:6425–6437.
  • 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 USA. 2013;110:11698–11703.
  • Pandelo 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.
  • 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;59:5984–5991.
  • 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;11:e1005066.
  • Lusic M, Giacca M. Regulation of HIV-1 latency by chromatin structure and nuclear architecture. J Mol Biol. 2015;427:688–694.
  • 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.
  • 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;31:137–141.
  • Lu H, Yu D, Hansen AS, et al. Phase-separation mechanism for C-terminal hyperphosphorylation of RNA polymerase II. Nature. 2018;558:318–323.
  • Banani SF, Lee HO, Hyman AA, et al. Biomolecular condensates: organizers of cellular biochemistry. Nat Rev Mol Cell Biol. 2017;18:285–298.
  • Hnisz D, Shrinivas K, Young RA, et al. A phase separation model for transcriptional control. Cell. 2017;169:13–23.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.