Small molecules targeted to a non-catalytic "RVxF" binding site of protein phosphatase-1 inhibit HIV-1

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Ammosova, Tatiana ^a,b,c   Platonov, Maxim ^d,e   Yedavalli, Venkat R K ^f   Obukhov, Yuri ^b   Gordeuk, Victor R ^a,g   Jeang, Kuan Teh ^f   Kovalskyy, Dmytro ^d,e   Nekhai, Sergei ^a,b,c  

^a HOWARD UNIVERSITY   (United States)

^b HOWARD UNIVERSITY   (United States)

^c HOWARD UNIVERSITY COLLEGE OF MEDICINE   (United States)

^d TARAS SHEVCHENKO NATIONAL UNIVERSITY OF KYIV   (Ukraine)

^e INSTITUTE OF MOLECULAR BIOLOGY AND GENETICS   (Ukraine)

^f NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^g UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1H4 COMPOUND; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN NIPP1; PROTEIN PNUTS; PROTEOME; REGULATOR PROTEIN; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL NUCLEUS; CELL STRAIN HEK293; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG MECHANISM; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IC 50; IMMUNOPRECIPITATION; IN VITRO STUDY; MASS SPECTROMETRY; NONHUMAN; PREDICTION; PROTEIN ANALYSIS; PROTEIN DEPHOSPHORYLATION; PROTEIN INTERACTION; VIRUS REPLICATION; VIRUS TRANSCRIPTION; WESTERN BLOTTING;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANTI-HIV AGENTS; BINDING SITES; BIOCATALYSIS; CELL NUCLEUS; CELLS, CULTURED; DNA-BINDING PROTEINS; HIV-1; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRACELLULAR SPACE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PEPTIDES; PROTEIN BINDING; PROTEIN PHOSPHATASE 1; PROTEIN TRANSPORT; RNA-BINDING PROTEINS; SMALL MOLECULE LIBRARIES; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TRANSCRIPTION, GENETIC; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84863088961     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039481     Document Type: Article

References (47)

1. Berkhout B, Silverman RH, Jeang KT, (1989) Tat trans-activates the human immunodeficiency virus through a nascent RNA target. Cell 59: 273-282.
2. Nekhai S, Jeang KT, (2006) Transcriptional and post-transcriptional regulation of HIV-1 gene expression: role of cellular factors for Tat and Rev. Future Microbiol 1: 417-426.
3. Ammosova T, Jerebtsova M, Beullens M, Voloshin Y, Ray PE, et al. (2003) Nuclear protein phosphatase-1 regulates HIV-1 transcription. J Biol Chem 278: 32189-32194.
4. Washington K, Ammosova T, Beullens M, Jerebtsova M, Kumar A, et al. (2002) Protein phosphatase-1 dephosphorylates the C-terminal domain of RNA polymerase-II. J Biol Chem 277: 40442-40448.
5. Ammosova T, Yedavalli VR, Niu X, Jerebtsova M, Van Eynde A, et al. (2011) Expression of a protein phosphatase 1 inhibitor, cdNIPP1, increases CDK9 threonine 186 phosphorylation and inhibits HIV-1 transcription. J Biol Chem 286: 3798-3804.
6. Ammosova T, Jerebtsova M, Beullens M, Lesage B, Jackson A, et al. (2005) Nuclear targeting of protein phosphatase-1 by HIV-1 Tat protein. J Biol Chem 280: 36364-36371.
7. Bollen M, Beullens M, (2002) Signaling by protein phosphatases in the nucleus. Trends Cell Biol 12: 138-145.
8. Hendrickx A, Beullens M, Ceulemans H, Den Abt T, Van Eynde A, et al. (2009) Docking motif-guided mapping of the interactome of protein phosphatase-1. Chem Biol 16: 365-371.
9. Barboric M, Lenasi T, Chen H, Johansen EB, Guo S, et al. (2009) 7SK snRNP/P-TEFb couples transcription elongation with alternative splicing and is essential for vertebrate development. Proc Natl Acad Sci U S A 106: 7798-7803.
10. Jeronimo C, Forget D, Bouchard A, Li Q, Chua G, et al. (2007) Systematic analysis of the protein interaction network for the human transcription machinery reveals the identity of the 7SK capping enzyme. Mol Cell 27: 262-274.
11. Sedore SC, Byers SA, Biglione S, Price JP, Maury WJ, et al. (2007) 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 35: 4347-4358.
12. Chen R, Liu M, Li H, Xue Y, Ramey WN, et al. (2008) PP2B and PP1alpha cooperatively disrupt 7SK snRNP to release P-TEFb for transcription in response to Ca2+ signaling. Genes Dev 22: 1356-1368.
13. Ammosova T, Obukhov Y, Kotelkin A, Breuer D, Beullens M, et al. (2011) Protein Phosphatase-1 Activates CDK9 by Dephosphorylating Ser175. PLOS One 6: e18985.
14. Egloff MP, Johnson DF, Moorhead G, Cohen PT, Cohen P, et al. (1997) Structural basis for the recognition of regulatory subunits by the catalytic subunit of protein phosphatase 1. Embo J 16: 1876-1887.
15. Nekhai S, Bhat UG, Ammosova T, Radhakrishnan SK, Jerebtsova M, et al. (2007) A novel anticancer agent ARC antagonizes HIV-1 and HCV. Oncogene 26: 3899-3903.
16. Ammosova T, Berro R, Kashanchi F, Nekhai S, (2005) RNA interference directed to CDK2 inhibits HIV-1 transcription. Virology 341: 171-178.
17. Chelius D, Bondarenko PV, (2002) Quantitative profiling of proteins in complex mixtures using liquid chromatography and mass spectrometry. J Proteome Res 1: 317-323.
18. Lesage B, Beullens M, Pedelini L, Garcia-Gimeno MA, Waelkens E, et al. (2007) A complex of catalytically inactive protein phosphatase-1 sandwiched between Sds22 and inhibitor-3. Biochemistry 46: 8909-8919.
19. Nekhai S, Jeang KT, (2009) Human immunodeficiency virus type 1 Tat and Rev as potential targets for drug development; LaFemina RL, editor. Washington, DC: ASM Press. 15 p.
20. Okamoto H, Cujec TP, Okamoto M, Peterlin BM, Baba M, et al. (2000) Inhibition of the RNA-dependent transactivation and replication of human immunodeficiency virus type 1 by a fluoroquinoline derivative K-37. Virology 272: 402-408.
21. Parolin C, Gatto B, Del Vecchio C, Pecere T, Tramontano E, et al. (2003) New anti-human immunodeficiency virus type 1 6-aminoquinolones: mechanism of action. Antimicrob Agents Chemother 47: 889-896.
22. Richter S, Parolin C, Gatto B, Del Vecchio C, Brocca-Cofano E, et al. (2004) Inhibition of human immunodeficiency virus type 1 tat-trans-activation-responsive region interaction by an antiviral quinolone derivative. Antimicrob Agents Chemother 48: 1895-1899.
23. Massari S, Daelemans D, Barreca ML, Knezevich A, Sabatini S, et al. (2010) A 1,8-naphthyridone derivative targets the HIV-1 Tat-mediated transcription and potently inhibits the HIV-1 replication. J Med Chem 53: 641-648.
24. Ivanova G, Reigadas S, Ittig D, Arzumanov A, Andreola ML, et al. (2007) Tricyclo-DNA containing oligonucleotides as steric block inhibitors of human immunodeficiency virus type 1 tat-dependent trans-activation and HIV-1 infectivity. Oligonucleotides 17: 54-65.
25. Iguchi T, Ishikawa H, Matumoto H, Mizuno M, Goto K, et al. (2005) Amino disaccharides having an alpha-(1->4) or a beta-(1->4) linkage, their synthesis and evaluation as a potential inhibitor for HIV-1 TAR-Tat. Nucleic Acids Symp Ser (Oxf) pp. 169-170.
26. Yuan D, He M, Pang R, Lin SS, Li Z, et al. (2007) The design, synthesis, and biological evaluation of novel substituted purines as HIV-1 Tat-TAR inhibitors. Bioorg Med Chem 15: 265-272.
27. He M, Yuan D, Lin W, Pang R, Yu X, et al. (2005) Synthesis and assay of isoquinoline derivatives as HIV-1 Tat-TAR interaction inhibitors. Bioorg Med Chem Lett 15: 3978-3981.
28. Nekhai S, Jeang KT, (2006) Transcriptional and post-transcriptional regulation of HIV-1 gene expression: role of cellular factors for Tat and Rev. Future Microbiol 1: 417-426.
29. Zeng L, Li J, Muller M, Yan S, Mujtaba S, et al. (2005) Selective small molecules blocking HIV-1 Tat and coactivator PCAF association. J Am Chem Soc 127: 2376-2377.
30. Pan C, Mezei M, Mujtaba S, Muller M, Zeng L, et al. (2007) Structure-guided optimization of small molecules inhibiting human immunodeficiency virus 1 Tat association with the human coactivator p300/CREB binding protein-associated factor. J Med Chem 50: 2285-2288.
31. Stevens M, Balzarini J, Lagoja IM, Noppen B, Francois K, et al. (2007) Inhibition of human immunodeficiency virus type 1 transcription by N-aminoimidazole derivatives. Virology 365: 220-237.
32. Ammosova T, Washington K, Debebe Z, Brady J, Nekhai S, (2005) Dephosphorylation of CDK9 by protein phosphatase 2A and protein phosphatase-1 in Tat-activated HIV-1 transcription. Retrovirology 2: 47.
33. Nguyen VT, Kiss T, Michels AA, Bensaude O, (2001) 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes. Nature 414: 322-325.
34. Yang Z, Zhu Q, Luo K, Zhou Q, (2001) The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature 414: 317-322.
35. Michels AA, Nguyen VT, Fraldi A, Labas V, Edwards M, et al. (2003) MAQ1 and 7SK RNA interact with CDK9/cyclin T complexes in a transcription-dependent manner. Mol Cell Biol 23: 4859-4869.
36. Yik JH, Chen R, Nishimura R, Jennings JL, Link AJ, et al. (2003) Inhibition of P-TEFb (CDK9/Cyclin T) kinase and RNA polymerase II transcription by the coordinated actions of HEXIM1 and 7SK snRNA. Mol Cell 12: 971-982.
37. Jochmann R, Thurau M, Jung S, Hofmann C, Naschberger E, et al. (2009) O-linked N-acetylglucosaminylation of Sp1 inhibits the human immunodeficiency virus type 1 promoter. J Virol 83: 3704-3718.
38. Yedavalli VS, Benkirane M, Jeang KT, (2003) Tat and trans-activation-responsive (TAR) RNA-independent induction of HIV-1 long terminal repeat by human and murine cyclin T1 requires Sp1. J Biol Chem 278: 6404-6410.
39. Chun RF, Semmes OJ, Neuveut C, Jeang KT, (1998) Modulation of Sp1 phosphorylation by human immunodeficiency virus type 1 Tat. J Virol 72: 2615-2629.
40. Zhang Y, Li Y, Shibahara S, Takahashi K, (2008) Synergistic activation of the human adrenomedullin gene promoter by Sp1 and AP-2alpha. Peptides 29: 465-472.
41. Jerebtsova M, Klotchenko SA, Artamonova TO, Ammosova T, Washington K, et al. (2011) Mass spectrometry and biochemical analysis of RNA polymerase II: targeting by protein phosphatase-1. Mol Cell Biochem 347: 79-87.
42. Bollen M, Peti W, Ragusa MJ, Beullens M, (2010) The extended PP1 toolkit: designed to create specificity. Trends Biochem Sci 35: 450-458.
43. McMartin C, Bohacek RS, (1997) QXP: powerful, rapid computer algorithms for structure-based drug design. J Comput Aided Mol Des 11: 333-344.
44. Huang CC, Couch GS, Pettersen EF, Ferrin TE, Howard AE, et al. (1998) The object technology framework: an object-oriented interface to molecular data and its application to collagen. Pac Symp Biocomput pp. 349-361.
45. Ragusa MJ, Dancheck B, Critton DA, Nairn AC, Page R, et al. (2010) Spinophilin directs protein phosphatase 1 specificity by blocking substrate binding sites. Nat Struct Mol Biol 17: 459-464.
46. Ammosova T, Berro R, Jerebtsova M, Jackson A, Charles S, et al. (2006) Phosphorylation of HIV-1 Tat by CDK2 in HIV-1 transcription. Retrovirology 3: 78.
47. Woldehawariat G, Nekhai S, Petryshyn R, (1999) Differential phosphorylation of PKR associates with deregulation of eIF-2alpha phosphorylation and altered growth characteristics in 3T3-F442A fibroblasts. Mol Cell Biochem 198: 7-17.