Inhibition of Tat-mediated HIV-1 replication and neurotoxicity by novel GSK3-beta inhibitors

Virology

Volumn 415, Issue 1, 2011, Pages 56-68

  Kehn Hall, Kylene ^a   Guendel, Irene ^a   Carpio, Lawrence ^a   Skaltsounis, Leandros ^b   Meijer, Laurent ^b   Al Harthi, Lena ^c   Steiner, Joseph P ^d   Nath, Avindra ^d   Kutsch, Olaf ^e   Kashanchi, Fatah ^a  

^a GEORGE MASON UNIVERSITY   (United States)

^b STATION BIOLOGIQUE   (France)

^c RUSH MEDICAL COLLEGE   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e University of Alabama at Birmingham   (United States)

Author keywords

GSK 3; HAND; HIV 1; Indirubin; Neuroprotection; Tat; Therapeutic target; Transcriptional inhibition

Indexed keywords

2 [[[2 (5 BROMO 2 OXO 1,2 DIHYDRO 2H INDOL 3 YLIDENE)HYDRAZINO]OXO ACETYL]AMINO]BENZOIC ACID; 6 BROMO 5 METHYL 1H INDOLE 2,3 DIONE 3 [(6 BROMO 5 METHYL 2 OXO 1,2 DIHYDRO 3H INDOL 3 YLIDENE)HYDRAZONE]; 6 BROMOINDIRUBIN 3' OXIME; DACTINOMYCIN; EPIRUBICIN; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; GLYCOGEN SYNTHASE KINASE 3BETA; GLYCOGEN SYNTHASE KINASE 3BETA INHIBITOR; QUININE DERIVATIVE; QUININE ETHYLCARBONATE; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; ARTICLE; ASTROCYTE; CELL DEATH; CELL LINE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ASSAY; ENZYME INHIBITION; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IC 50; IN VITRO STUDY; INHIBITION KINETICS; MACROPHAGE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; TISSUE CULTURE; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

ANIMALS; ANTI-HIV AGENTS; ASTROCYTES; CELL DEATH; CELL LINE; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; GLYCOGEN SYNTHASE KINASE 3; HIGH-THROUGHPUT SCREENING ASSAYS; HIV-1; HUMANS; INDOLES; MACROPHAGES; NEUROPROTECTIVE AGENTS; NEUROTOXINS; OXIMES; POLYMERASE CHAIN REACTION; RATS; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TRANSCRIPTION, GENETIC; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; RATTUS;

EID: 79956223920     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.03.025     Document Type: Article

References (97)

1. Aboul-ela F., Karn J., Varani G. The structure of the human immunodeficiency virus type-1 TAR RNA reveals principles of RNA recognition by Tat protein. J. Mol. Biol. 1995, 253:313-332.
2. Agbottah E., de La Fuente C., Nekhai S., Barnett A., Gianella-Borradori A., Pumfery A., Kashanchi F. Antiviral activity of CYC202 in HIV-1-infected cells. J. Biol. Chem. 2005, 280:3029-3042.
3. Aksenov M.Y., Hasselrot U., Wu G., Nath A., Anderson C., Mactutus C.F., Booze R.M. Temporal relationships between HIV-1 Tat-induced neuronal degeneration, OX-42 immunoreactivity, reactive astrocytosis, and protein oxidation in the rat striatum. Brain Res. 2003, 987:1-9.
4. Ali A., Hoeflich K.P., Woodgett J.R. Glycogen synthase kinase-3: properties, functions, and regulation. Chem. Rev. 2001, 101:2527-2540.
5. Amit S., Hatzubai A., Birman Y., Andersen J.S., Ben-Shushan E., Mann M., Ben-Neriah Y., Alkalay I. Axin-mediated CKI phosphorylation of beta-catenin at Ser 45: a molecular switch for the Wnt pathway. Genes Dev. 2002, 16:1066-1076.
6. Baba M., Okamoto M., Makino M., Kimura Y., Ikeuchi T., Sakaguchi T., Okamoto T. Potent and selective inhibition of human immunodeficiency virus type 1 transcription by piperazinyloxoquinoline derivatives. Antimicrob. Agents Chemother. 1997, 41:1250-1255.
7. Baba M., Okamoto M., Kawamura M., Makino M., Higashida T., Takashi T., Kimura Y., Ikeuchi T., Tetsuka T., Okamoto T. Inhibition of human immunodeficiency virus type 1 replication and cytokine production by fluoroquinoline derivatives. Mol. Pharmacol. 1998, 53:1097-1103.
8. Bailly C., Colson P., Houssier C., Hamy F. The binding mode of drugs to the TAR RNA of HIV-1 studied by electric linear dichroism. Nucleic Acids Res. 1996, 24:1460-1464.
9. Bansal A.K., Mactutus C.F., Nath A., Maragos W., Hauser K.F., Booze R.M. Neurotoxicity of HIV-1 proteins gp120 and Tat in the rat striatum. Brain Res. 2000, 879:42-49.
10. Barillari G., Gendelman R., Gallo R.C., Ensoli B. The Tat protein of human immunodeficiency virus type 1, a growth factor for AIDS Kaposi sarcoma and cytokine-activated vascular cells, induces adhesion of the same cell types by using integrin receptors recognizing the RGD amino acid sequence. Proc. Natl Acad. Sci. U. S. A. 1993, 90:7941-7945.
11. Berridge M.J., Downes C.P., Hanley M.R. Neural and developmental actions of lithium: a unifying hypothesis. Cell 1989, 59:411-419.
12. Bonavia R., Bajetto A., Barbero S., Albini A., Noonan D.M., Schettini G. HIV-1 Tat causes apoptotic death and calcium homeostasis alterations in rat neurons. Biochem. Biophys. Res. Commun. 2001, 288:301-308.
13. Bournat J.C., Brown A.M., Soler A.P. Wnt-1 dependent activation of the survival factor NF-kappaB in PC12 cells. J. Neurosci. Res. 2000, 61:21-32.
14. Boykins R.A., Mahieux R., Shankavaram U.T., Gho Y.S., Lee S.F., Hewlett I.K., Wahl L.M., Kleinman H.K., Brady J.N., Yamada K.M., Dhawan S. Cutting edge: a short polypeptide domain of HIV-1-Tat protein mediates pathogenesis. J. Immunol. 1999, 163:15-20.
15. Brodsky A.S., Williamson J.R. Solution structure of the HIV-2 TAR-argininamide complex. J. Mol. Biol. 1997, 267:624-639.
16. Brodsky A.S., Erlacher H.A., Williamson J.R. NMR evidence for a base triple in the HIV-2 TAR C-G.C+ mutant-argininamide complex. Nucleic Acids Res. 1998, 26:1991-1995.
17. Buss H., Dorrie A., Schmitz M.L., Frank R., Livingstone M., Resch K., Kracht M. Phosphorylation of serine 468 by GSK-3beta negatively regulates basal p65 NF-kappaB activity. J. Biol. Chem. 2004, 279:49571-49574.
18. Carroll-Anzinger D., Kumar A., Adarichev V., Kashanchi F., Al-Harthi L. Human immunodeficiency virus-restricted replication in astrocytes and the ability of gamma interferon to modulate this restriction are regulated by a downstream effector of the Wnt signaling pathway. J. Virol. 2007, 81:5864-5871.
19. Cerpa W., Toledo E.M., Varela-Nallar L., Inestrosa N.C. The role of Wnt signaling in neuroprotection. Drug News Perspect. 2009, 22:579-591.
20. Coghlan M.P., Culbert A.A., Cross D.A., Corcoran S.L., Yates J.W., Pearce N.J., Rausch O.L., Murphy G.J., Carter P.S., Roxbee Cox L., Mills D., Brown M.J., Haigh D., Ward R.W., Smith D.G., Murray K.J., Reith A.D., Holder J.C. Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen metabolism and gene transcription. Chem. Biol. 2000, 7:793-803.
21. Conant K., Garzino-Demo A., Nath A., McArthur J.C., Halliday W., Power C., Gallo R.C., Major E.O. Induction of monocyte chemoattractant protein-1 in HIV-1 Tat-stimulated astrocytes and elevation in AIDS dementia. Proc. Natl Acad. Sci. U. S. A. 1998, 95:3117-3121.
22. Cross D.A., Culbert A.A., Chalmers K.A., Facci L., Skaper S.D., Reith A.D. Selective small-molecule inhibitors of glycogen synthase kinase-3 activity protect primary neurones from death. J. Neurochem. 2001, 77:94-102.
23. Dassonneville L., Hamy F., Colson P., Houssier C., Bailly C. Binding of Hoechst 33258 to the TAR RNA of HIV-1. Recognition of a pyrimidine bulge-dependent structure. Nucleic Acids Res. 1997, 25:4487-4492.
24. Davies S.P., Reddy H., Caivano M., Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 2000, 351:95-105.
25. Dou H., Birusingh K., Faraci J., Gorantla S., Poluektova L.Y., Maggirwar S.B., Dewhurst S., Gelbard H.A., Gendelman H.E. Neuroprotective activities of sodium valproate in a murine model of human immunodeficiency virus-1 encephalitis. J. Neurosci. 2003, 23:9162-9170.
26. Dou H., Ellison B., Bradley J., Kasiyanov A., Poluektova L.Y., Xiong H., Maggirwar S., Dewhurst S., Gelbard H.A., Gendelman H.E. Neuroprotective mechanisms of lithium in murine human immunodeficiency virus-1 encephalitis. J. Neurosci. 2005, 25:8375-8385.
27. Edwards T.E., Sigurdsson S.T. Electron paramagnetic resonance dynamic signatures of TAR RNA-small molecule complexes provide insight into RNA structure and recognition. Biochemistry 2002, 41:14843-14847.
28. Ensoli B., Buonaguro L., Barillari G., Fiorelli V., Gendelman R., Morgan R.A., Wingfield P., Gallo R.C. Release, uptake, and effects of extracellular human immunodeficiency virus type 1 Tat protein on cell growth and viral transactivation. J. Virol. 1993, 67:277-287.
29. Etienne-Manneville S., Hall A. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 2001, 106:489-498.
30. Everall I.P., Bell C., Mallory M., Langford D., Adame A., Rockestein E., Masliah E. Lithium ameliorates HIV-gp120-mediated neurotoxicity. Mol. Cell. Neurosci. 2002, 21:493-501.
31. Faber C., Sticht H., Schweimer K., Rosch P. Structural rearrangements of HIV-1 Tat-responsive RNA upon binding of neomycin B. J. Biol. Chem. 2000, 275:20660-20666.
32. Farooqui R., Zhu S., Fenteany G. Glycogen synthase kinase-3 acts upstream of ADP-ribosylation factor 6 and Rac1 to regulate epithelial cell migration. Exp. Cell Res. 2006, 312:1514-1525.
33. Frame S., Cohen P. GSK3 takes centre stage more than 20years after its discovery. Biochem. J. 2001, 359:1-16.
34. Fujinaga K., Cujec T.P., Peng J., Garriga J., Price D.H., Grana X., Peterlin B.M. The ability of positive transcription elongation factor B to transactivate human immunodeficiency virus transcription depends on a functional kinase domain, cyclin T1, and Tat. J. Virol. 1998, 72:7154-7159.
35. Fukao T., Koyasu S. PI3K and negative regulation of TLR signaling. Trends Immunol. 2003, 24:358-363.
36. Galons H., Oumata N., Meijer L. Cyclin-dependent kinase inhibitors: a survey of recent patent literature. Expert Opin. Ther. Pat. 2010, 20:377-404.
37. Guendel I., Agbottah E.T., Kehn-Hall K., Kashanchi F. Inhibition of human immunodeficiency virus type-1 by cdk inhibitors. AIDS Res. Ther. 2010, 7:7.
38. Hamy F., Brondani V., Florsheimer A., Stark W., Blommers M.J., Klimkait T. A new class of HIV-1 Tat antagonist acting through Tat-TAR inhibition. Biochemistry 1998, 37:5086-5095.
39. Haubrich R.H., Flexner C., Lederman M.M., Hirsch M., Pettinelli C.P., Ginsberg R., Lietman P., Hamzeh F.M., Spector S.A., Richman D.D. A randomized trial of the activity and safety of Ro 24-7429 (Tat antagonist) versus nucleoside for human immunodeficiency virus infection. The AIDS Clinical Trials Group 213 Team. J. Infect. Dis. 1995, 172:1246-1252.
40. Haughey N.J., Mattson M.P. Calcium dysregulation and neuronal apoptosis by the HIV-1 proteins Tat and gp120. J. Acquir. Immune Defic. Syndr. 2002, 31(Suppl 2):S55-S61.
41. Haughey N.J., Nath A., Mattson M.P., Slevin J.T., Geiger J.D. HIV-1 Tat through phosphorylation of NMDA receptors potentiates glutamate excitotoxicity. J. Neurochem. 2001, 78:457-467.
42. Herrmann C.H., Rice A.P. 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.
43. Hetman M., Cavanaugh J.E., Kimelman D., Xia Z. Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal. J. Neurosci. 2000, 20:2567-2574.
44. Ho C.Y., Wong C.H., Li H.Y. Perturbation of the chromosomal binding of RCC1, Mad2 and survivin causes spindle assembly defects and mitotic catastrophe. J. Cell. Biochem. 2008, 105:835-846.
45. Hoeflich K.P., Luo J., Rubie E.A., Tsao M.S., Jin O., Woodgett J.R. Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature 2000, 406:86-90.
46. Hsu M.C., Dhingra U., Earley J.V., Holly M., Keith D., Nalin C.M., Richou A.R., Schutt A.D., Tam S.Y., Potash M.J., et al. Inhibition of type 1 human immunodeficiency virus replication by a tat antagonist to which the virus remains sensitive after prolonged exposure in vitro. Proc. Natl Acad. Sci. U. S. A. 1993, 90:6395-6399.
47. Jones M., Olafson K., Del Bigio M.R., Peeling J., Nath A. Intraventricular injection of human immunodeficiency virus type 1 (HIV-1) tat protein causes inflammation, gliosis, apoptosis, and ventricular enlargement. J. Neuropathol. Exp. Neurol. 1998, 57:563-570.
48. Jones J., Whitford W., Wagner F., Kutsch O. Optimization of HIV-1 infectivity assays. BioTechniques 2007, 43:589-594.
49. Jope R.S., Yuskaitis C.J., Beurel E. Glycogen synthase kinase-3 (GSK3): inflammation, diseases, and therapeutics. Neurochem. Res. 2007, 32:577-595.
50. Kang H.J., Park H.J. Novel molecular mechanism for actinomycin d activity as an oncogenic promoter g-quadruplex binder. Biochemistry 2009, 48:7392-7398.
51. Kashanchi F., Kehn-Hall K. Cyclin dependent kinases as attractive targets to prevent transcription from viral genomes. Curr. Pharm. Des. 2009, 15:2520-2532.
52. Kempf M.C., Jones J., Heil M.L., Kutsch O. A high-throughput drug screening system for HIV-1 transcription inhibitors. J. Biomol. Screen. 2006, 11:807-815.
53. Koivisto L., Hakkinen L., Matsumoto K., McCulloch C.A., Yamada K.M., Larjava H. Glycogen synthase kinase-3 regulates cytoskeleton and translocation of Rac1 in long cellular extensions of human keratinocytes. Exp. Cell Res. 2004, 293:68-80.
54. Krum J.M., Rosenstein J.M. VEGF mRNA and its receptor flt-1 are expressed in reactive astrocytes following neural grafting and tumor cell implantation in the adult CNS. Exp. Neurol. 1998, 154:57-65.
55. Kruman I.I., Nath A., Mattson M.P. HIV-1 protein Tat induces apoptosis of hippocampal neurons by a mechanism involving caspase activation, calcium overload, and oxidative stress. Exp. Neurol. 1998, 154:276-288.
56. Kumar A., Zloza A., Moon R.T., Watts J., Tenorio A.R., Al-Harthi L. Active beta-catenin signaling is an inhibitory pathway for human immunodeficiency virus replication in peripheral blood mononuclear cells. J. Virol. 2008, 82:2813-2820.
57. Laspia M.F., Rice A.P., Mathews M.B. HIV-1 Tat protein increases transcriptional initiation and stabilizes elongation. Cell 1989, 59:283-292.
58. Liu Y., Jones M., Hingtgen C.M., Bu G., Laribee N., Tanzi R.E., Moir R.D., Nath A., He J.J. Uptake of HIV-1 tat protein mediated by low-density lipoprotein receptor-related protein disrupts the neuronal metabolic balance of the receptor ligands. Nat. Med. 2000, 6:1380-1387.
59. Maggirwar S.B., Tong N., Ramirez S., Gelbard H.A., Dewhurst S. HIV-1 Tat-mediated activation of glycogen synthase kinase-3beta contributes to Tat-mediated neurotoxicity. J. Neurochem. 1999, 73:578-586.
60. Magnuson D.S., Knudsen B.E., Geiger J.D., Brownstone R.M., Nath A. Human immunodeficiency virus type 1 tat activates non-N-methyl-d-aspartate excitatory amino acid receptors and causes neurotoxicity. Ann. Neurol. 1995, 37:373-380.
61. Malim M.H., Cullen B.R. HIV-1 structural gene expression requires the binding of multiple Rev monomers to the viral RRE: implications for HIV-1 latency. Cell 1991, 65:241-248.
62. Malumbres M., Pevarello P., Barbacid M., Bischoff J.R. CDK inhibitors in cancer therapy: what is next?. Trends Pharmacol. Sci. 2008, 29:16-21.
63. Maragos W.F., Tillman P., Jones M., Bruce-Keller A.J., Roth S., Bell J.E., Nath A. Neuronal injury in hippocampus with human immunodeficiency virus transactivating protein, Tat. Neuroscience 2003, 117:43-53.
64. Martin M., Rehani K., Jope R.S., Michalek S.M. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 2005, 6:777-784.
65. Meijer L., Skaltsounis A.L., Magiatis P., Polychronopoulos P., Knockaert M., Leost M., Ryan X.P., Vonica C.A., Brivanlou A., Dajani R., Crovace C., Tarricone C., Musacchio A., Roe S.M., Pearl L., Greengard P. GSK-3-selective inhibitors derived from Tyrian purple indirubins. Chem. Biol. 2003, 10:1255-1266.
66. Meijer L., Flajolet M., Greengard P. Pharmacological inhibitors of glycogen synthase kinase 3. Trends Pharmacol. Sci. 2004, 25:471-480.
67. Mestre B., Arzumanov A., Singh M., Boulme F., Litvak S., Gait M.J. Oligonucleotide inhibition of the interaction of HIV-1 Tat protein with the trans-activation responsive region (TAR) of HIV RNA. Biochim. Biophys. Acta 1999, 1445:86-98.
68. Nabel G., Baltimore D. An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature 1987, 326:711-713.
69. Nath A., Psooy K., Martin C., Knudsen B., Magnuson D.S., Haughey N., Geiger J.D. Identification of a human immunodeficiency virus type 1 Tat epitope that is neuroexcitatory and neurotoxic. J. Virol. 1996, 70:1475-1480.
70. Nath A., Conant K., Chen P., Scott C., Major E.O. Transient exposure to HIV-1 Tat protein results in cytokine production in macrophages and astrocytes. A hit and run phenomenon. J. Biol. Chem. 1999, 274:17098-17102.
71. Nguyen T.B., Lucero G.R., Chana G., Hult B.J., Tatro E.T., Masliah E., Grant I., Achim C.L., Everall I.P., Grp H.N.R. Glycogen synthase kinase-3 beta (GSK-3 beta) inhibitors AR-A014418 and B6B3O prevent human immunodeficiency virus-mediated neurotoxicity in primary human neurons. J. Neurovirol. 2009, 15:434-438.
72. Nifosi R., Reyes C.M., Kollman P.A. Molecular dynamics studies of the HIV-1 TAR and its complex with argininamide. Nucleic Acids Res. 2000, 28:4944-4955.
73. Noonan D., Albini A. From the outside in: extracellular activities of HIV Tat. Adv. Pharmacol. 2000, 48:229-250.
74. Owen R., Gordon-Weeks P.R. Inhibition of glycogen synthase kinase 3beta in sensory neurons in culture alters filopodia dynamics and microtubule distribution in growth cones. Mol. Cell. Neurosci. 2003, 23:626-637.
75. Peng J., Zhu Y., Milton J.T., Price D.H. Identification of multiple cyclin subunits of human P-TEFb. Genes Dev. 1998, 12:755-762.
76. Philippon V., Vellutini C., Gambarelli D., Harkiss G., Arbuthnott G., Metzger D., Roubin R., Filippi P. The basic domain of the lentiviral Tat protein is responsible for damages in mouse brain: involvement of cytokines. Virology 1994, 205:519-529.
77. Plyte S.E., Hughes K., Nikolakaki E., Pulverer B.J., Woodgett J.R. Glycogen synthase kinase-3: functions in oncogenesis and development. Biochim. Biophys. Acta 1992, 1114:147-162.
78. Polychronopoulos P., Magiatis P., Skaltsounis A.L., Myrianthopoulos V., Mikros E., Tarricone A., Musacchio A., Roe S.M., Pearl L., Leost M., Greengard P., Meijer L. Structural basis for the synthesis of indirubins as potent and selective inhibitors of glycogen synthase kinase-3 and cyclin-dependent kinases. J. Med. Chem. 2004, 47:935-946.
79. Rao R., Hao C.M., Breyer M.D. Hypertonic stress activates glycogen synthase kinase 3beta-mediated apoptosis of renal medullary interstitial cells, suppressing an NFkappaB-driven cyclooxygenase-2-dependent survival pathway. J. Biol. Chem. 2004, 279:3949-3955.
80. Rice A.P., Mathews M.B. Transcriptional but not translational regulation of HIV-1 by the tat gene product. Nature 1988, 332:551-553.
81. Rohr O., Marban C., Aunis D., Schaeffer E. Regulation of HIV-1 gene transcription: from lymphocytes to microglial cells. J. Leukoc. Biol. 2003, 74:736-749.
82. Rossi A., Mukerjee R., Ferrante P., Khalili K., Amini S., Sawaya B.E. Human immunodeficiency virus type 1 Tat prevents dephosphorylation of Sp1 by TCF-4 in astrocytes. J. Gen. Virol. 2006, 87:1613-1623.
83. Rubinfeld B., Albert I., Porfiri E., Fiol C., Munemitsu S., Polakis P. Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science 1996, 272:1023-1026.
84. Rusnati M., Presta M. HIV-1 Tat protein and endothelium: from protein/cell interaction to AIDS-associated pathologies. Angiogenesis 2002, 5:141-151.
85. Sabatier J.M., Vives E., Mabrouk K., Benjouad A., Rochat H., Duval A., Hue B., Bahraoui E. Evidence for neurotoxic activity of tat from human immunodeficiency virus type 1. J. Virol. 1991, 65:961-967.
86. Sanchez J.F., Sniderhan L.F., Williamson A.L., Fan S., Chakraborty-Sett S., Maggirwar S.B. Glycogen synthase kinase 3beta-mediated apoptosis of primary cortical astrocytes involves inhibition of nuclear factor kappaB signaling. Mol. Cell. Biol. 2003, 23:4649-4662.
87. Sobhian B., Laguette N., Yatim A., Nakamura M., Levy Y., Kiernan R., Benkirane M. HIV-1 Tat assembles a multifunctional transcription elongation complex and stably associates with the 7SK snRNP. Mol. Cell 2010, 38:439-451.
88. Sui Z., Sniderhan L.F., Fan S., Kazmierczak K., Reisinger E., Kovacs A.D., Potash M.J., Dewhurst S., Gelbard H.A., Maggirwar S.B. Human immunodeficiency virus-encoded Tat activates glycogen synthase kinase-3beta to antagonize nuclear factor-kappaB survival pathway in neurons. Eur. J. Neurosci. 2006, 23:2623-2634.
89. Swindle C.S., Kim H.G., Klug C.A. Mutation of CpGs in the murine stem cell virus retroviral vector long terminal repeat represses silencing in embryonic stem cells. J. Biol. Chem. 2004, 279:34-41.
90. Tardieu M., Hery C., Peudenier S., Boespflug O., Montagnier L. Human immunodeficiency virus type 1-infected monocytic cells can destroy human neural cells after cell-to-cell adhesion. Ann. Neurol. 1992, 32:11-17.
91. Van Duyne R., Cardenas J., Easley R., Wu W., Kehn-Hall K., Klase Z., Mendez S., Zeng C., Chen H., Saifuddin M., Kashanchi F. Effect of transcription peptide inhibitors on HIV-1 replication. Virology 2008, 376:308-322.
92. van Weeren P.C., de Bruyn K.M., de Vries-Smits A.M., van Lint J., Burgering B.M. Essential role for protein kinase B (PKB) in insulin-induced glycogen synthase kinase 3 inactivation. Characterization of dominant-negative mutant of PKB. J. Biol. Chem. 1998, 273:13150-13156.
93. Verhoef K., Marzio G., Hillen W., Bujard H., Berkhout B. Strict control of human immunodeficiency virus type 1 replication by a genetic switch: Tet for Tat. J. Virol. 2001, 75:979-987.
94. Weeks B.S., Lieberman D.M., Johnson B., Roque E., Green M., Loewenstein P., Oldfield E.H., Kleinman H.K. Neurotoxicity of the human immunodeficiency virus type 1 tat transactivator to PC12 cells requires the Tat amino acid 49-58 basic domain. J. Neurosci. Res. 1995, 42:34-40.
95. Wei P., Garber M.E., Fang S.M., Fischer W.H., Jones K.A. A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell 1998, 92:451-462.
96. Weiss J.M., Nath A., Major E.O., Berman J.W. HIV-1 Tat induces monocyte chemoattractant protein-1-mediated monocyte transmigration across a model of the human blood-brain barrier and up-regulates CCR5 expression on human monocytes. J. Immunol. 1999, 163:2953-2959.
97. Wortman B., Darbinian N., Sawaya B.E., Khalili K., Amini S. Evidence for regulation of long terminal repeat transcription by Wnt transcription factor TCF-4 in human astrocytic cells. J. Virol. 2002, 76:11159-11165.