Abstract
Human immunodeficiency virus type 1 (HIV-1) infection has been associated with an increase in the binding of the transcription factor NF-kappa B to its consensus sequence in the viral promoter. Using cultures of primary human fetal astrocytes, we show that exogenous HIV-1 Tat protein, which has been demonstrated to be released from infected cells, is associated with an increase in the binding of this transcription factor to an HIV-1 long terminal repeat kappa B sequence. This effect occurs rapidly and is independent of new protein synthesis. We also demonstrate that extracellular Tat protein is associated with an increase in protein kinase C activity. If Tat functions similarly in other cell types, such findings could relate to some of this protein's previously described physiological effects. These effects include Tat's ability to upregulate the synthesis of specific cytokines and to act as a growth factor.
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- Adachi A., Gendelman H. E., Koenig S., Folks T., Willey R., Rabson A., Martin M. A. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J Virol. 1986 Aug;59(2):284–291. doi: 10.1128/jvi.59.2.284-291.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Alcamí J., Laín de Lera T., Folgueira L., Pedraza M. A., Jacqué J. M., Bachelerie F., Noriega A. R., Hay R. T., Harrich D., Gaynor R. B. Absolute dependence on kappa B responsive elements for initiation and Tat-mediated amplification of HIV transcription in blood CD4 T lymphocytes. EMBO J. 1995 Apr 3;14(7):1552–1560. doi: 10.1002/j.1460-2075.1995.tb07141.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Aloisi F., Borsellino G., Samoggia P., Testa U., Chelucci C., Russo G., Peschle C., Levi G. Astrocyte cultures from human embryonic brain: characterization and modulation of surface molecules by inflammatory cytokines. J Neurosci Res. 1992 Aug;32(4):494–506. doi: 10.1002/jnr.490320405. [DOI] [PubMed] [Google Scholar]
- Andrews N. C., Faller D. V. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 1991 May 11;19(9):2499–2499. doi: 10.1093/nar/19.9.2499. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Arima N., Molitor J. A., Smith M. R., Kim J. H., Daitoku Y., Greene W. C. Human T-cell leukemia virus type I Tax induces expression of the Rel-related family of kappa B enhancer-binding proteins: evidence for a pretranslational component of regulation. J Virol. 1991 Dec;65(12):6892–6899. doi: 10.1128/jvi.65.12.6892-6899.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Arya S. K., Guo C., Josephs S. F., Wong-Staal F. Trans-activator gene of human T-lymphotropic virus type III (HTLV-III). Science. 1985 Jul 5;229(4708):69–73. doi: 10.1126/science.2990040. [DOI] [PubMed] [Google Scholar]
- Atwood W. J., Tornatore C. S., Traub R., Conant K., Drew P. D., Major E. O. Stimulation of HIV type 1 gene expression and induction of NF-kappa B (p50/p65)-binding activity in tumor necrosis factor alpha-treated human fetal glial cells. AIDS Res Hum Retroviruses. 1994 Oct;10(10):1207–1211. doi: 10.1089/aid.1994.10.1207. [DOI] [PubMed] [Google Scholar]
- Bagasra O., Khalili K., Seshamma T., Taylor J. P., Pomerantz R. J. TAR-independent replication of human immunodeficiency virus type 1 in glial cells. J Virol. 1992 Dec;66(12):7522–7528. doi: 10.1128/jvi.66.12.7522-7528.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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 Sep 1;90(17):7941–7945. doi: 10.1073/pnas.90.17.7941. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beckmann R., Lindschau C., Haller H., Hucho F., Buchner K. Differential nuclear localization of protein kinase C isoforms in neuroblastoma x glioma hybrid cells. Eur J Biochem. 1994 Jun 1;222(2):335–343. doi: 10.1111/j.1432-1033.1994.tb18872.x. [DOI] [PubMed] [Google Scholar]
- Benos D. J., Hahn B. H., Bubien J. K., Ghosh S. K., Mashburn N. A., Chaikin M. A., Shaw G. M., Benveniste E. N. Envelope glycoprotein gp120 of human immunodeficiency virus type 1 alters ion transport in astrocytes: implications for AIDS dementia complex. Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):494–498. doi: 10.1073/pnas.91.2.494. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bessho R., Matsubara K., Kubota M., Kuwakado K., Hirota H., Wakazono Y., Lin Y. W., Okuda A., Kawai M., Nishikomori R. Pyrrolidine dithiocarbamate, a potent inhibitor of nuclear factor kappa B (NF-kappa B) activation, prevents apoptosis in human promyelocytic leukemia HL-60 cells and thymocytes. Biochem Pharmacol. 1994 Nov 16;48(10):1883–1889. doi: 10.1016/0006-2952(94)90586-x. [DOI] [PubMed] [Google Scholar]
- Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
- Brake D. A., Debouck C., Biesecker G. Identification of an Arg-Gly-Asp (RGD) cell adhesion site in human immunodeficiency virus type 1 transactivation protein, tat. J Cell Biol. 1990 Sep;111(3):1275–1281. doi: 10.1083/jcb.111.3.1275. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown K., Gerstberger S., Carlson L., Franzoso G., Siebenlist U. Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation. Science. 1995 Mar 10;267(5203):1485–1488. doi: 10.1126/science.7878466. [DOI] [PubMed] [Google Scholar]
- Brown K., Park S., Kanno T., Franzoso G., Siebenlist U. Mutual regulation of the transcriptional activator NF-kappa B and its inhibitor, I kappa B-alpha. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2532–2536. doi: 10.1073/pnas.90.6.2532. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buonaguro L., Barillari G., Chang H. K., Bohan C. A., Kao V., Morgan R., Gallo R. C., Ensoli B. Effects of the human immunodeficiency virus type 1 Tat protein on the expression of inflammatory cytokines. J Virol. 1992 Dec;66(12):7159–7167. doi: 10.1128/jvi.66.12.7159-7167.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen S. J., Klann E., Gower M. C., Powell C. M., Sessoms J. S., Sweatt J. D. Studies with synthetic peptide substrates derived from the neuronal protein neurogranin reveal structural determinants of potency and selectivity for protein kinase C. Biochemistry. 1993 Feb 2;32(4):1032–1039. doi: 10.1021/bi00055a006. [DOI] [PubMed] [Google Scholar]
- Clark E. A., Brugge J. S. Integrins and signal transduction pathways: the road taken. Science. 1995 Apr 14;268(5208):233–239. doi: 10.1126/science.7716514. [DOI] [PubMed] [Google Scholar]
- Cohen D. I., Tani Y., Tian H., Boone E., Samelson L. E., Lane H. C. Participation of tyrosine phosphorylation in the cytopathic effect of human immunodeficiency virus-1. Science. 1992 Apr 24;256(5056):542–545. doi: 10.1126/science.1570514. [DOI] [PubMed] [Google Scholar]
- Conant K., Atwood W. J., Traub R., Tornatore C., Major E. O. An increase in p50/p65 NF-kB binding to the HIV-1 LTR is not sufficient to increase viral expression in the primary human astrocyte. Virology. 1994 Dec;205(2):586–590. doi: 10.1006/viro.1994.1685. [DOI] [PubMed] [Google Scholar]
- Dayton A. I., Sodroski J. G., Rosen C. A., Goh W. C., Haseltine W. A. The trans-activator gene of the human T cell lymphotropic virus type III is required for replication. Cell. 1986 Mar 28;44(6):941–947. doi: 10.1016/0092-8674(86)90017-6. [DOI] [PubMed] [Google Scholar]
- Diaz-Meco M. T., Berra E., Municio M. M., Sanz L., Lozano J., Dominguez I., Diaz-Golpe V., Lain de Lera M. T., Alcamí J., Payá C. V. A dominant negative protein kinase C zeta subspecies blocks NF-kappa B activation. Mol Cell Biol. 1993 Aug;13(8):4770–4775. doi: 10.1128/mcb.13.8.4770. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Diaz-Meco M. T., Dominguez I., Sanz L., Dent P., Lozano J., Municio M. M., Berra E., Hay R. T., Sturgill T. W., Moscat J. zeta PKC induces phosphorylation and inactivation of I kappa B-alpha in vitro. EMBO J. 1994 Jun 15;13(12):2842–2848. doi: 10.1002/j.1460-2075.1994.tb06578.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dressler K. A., Mathias S., Kolesnick R. N. Tumor necrosis factor-alpha activates the sphingomyelin signal transduction pathway in a cell-free system. Science. 1992 Mar 27;255(5052):1715–1718. doi: 10.1126/science.1313189. [DOI] [PubMed] [Google Scholar]
- Elder G. A., Major E. O. Early appearance of type II astrocytes in developing human fetal brain. Brain Res. 1988 Jul 1;470(1):146–150. doi: 10.1016/0165-3806(88)90211-8. [DOI] [PubMed] [Google Scholar]
- Ensoli B., Barillari G., Salahuddin S. Z., Gallo R. C., Wong-Staal F. Tat protein of HIV-1 stimulates growth of cells derived from Kaposi's sarcoma lesions of AIDS patients. Nature. 1990 May 3;345(6270):84–86. doi: 10.1038/345084a0. [DOI] [PubMed] [Google Scholar]
- 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 Jan;67(1):277–287. doi: 10.1128/jvi.67.1.277-287.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ensoli B., Gendelman R., Markham P., Fiorelli V., Colombini S., Raffeld M., Cafaro A., Chang H. K., Brady J. N., Gallo R. C. Synergy between basic fibroblast growth factor and HIV-1 Tat protein in induction of Kaposi's sarcoma. Nature. 1994 Oct 20;371(6499):674–680. doi: 10.1038/371674a0. [DOI] [PubMed] [Google Scholar]
- Finco T. S., Beg A. A., Baldwin A. S., Jr Inducible phosphorylation of I kappa B alpha is not sufficient for its dissociation from NF-kappa B and is inhibited by protease inhibitors. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11884–11888. doi: 10.1073/pnas.91.25.11884. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Flores S. C., Marecki J. C., Harper K. P., Bose S. K., Nelson S. K., McCord J. M. Tat protein of human immunodeficiency virus type 1 represses expression of manganese superoxide dismutase in HeLa cells. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7632–7636. doi: 10.1073/pnas.90.16.7632. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Frankel A. D. Activation of HIV transcription by Tat. Curr Opin Genet Dev. 1992 Apr;2(2):293–298. doi: 10.1016/s0959-437x(05)80287-4. [DOI] [PubMed] [Google Scholar]
- Gonzalez A., Klann E., Sessoms J. S., Chen S. J. Use of the synthetic peptide neurogranin(28-43) as a selective protein kinase C substrate in assays of tissue homogenates. Anal Biochem. 1993 Dec;215(2):184–189. doi: 10.1006/abio.1993.1574. [DOI] [PubMed] [Google Scholar]
- Goodnight J. A., Mischak H., Kolch W., Mushinski J. F. Immunocytochemical localization of eight protein kinase C isozymes overexpressed in NIH 3T3 fibroblasts. Isoform-specific association with microfilaments, Golgi, endoplasmic reticulum, and nuclear and cell membranes. J Biol Chem. 1995 Apr 28;270(17):9991–10001. doi: 10.1074/jbc.270.17.9991. [DOI] [PubMed] [Google Scholar]
- Grabarek J., Ware J. A. Protein kinase C activation without membrane contact in platelets stimulated by bryostatin. J Biol Chem. 1993 Mar 15;268(8):5543–5549. [PubMed] [Google Scholar]
- Grilli M., Chiu J. J., Lenardo M. J. NF-kappa B and Rel: participants in a multiform transcriptional regulatory system. Int Rev Cytol. 1993;143:1–62. doi: 10.1016/s0074-7696(08)61873-2. [DOI] [PubMed] [Google Scholar]
- Guy G. R., Bunce C. M., Gordon J., Michell R. H., Brown G. A combination of calcium ionophore and 12-O-tetradecanoyl-phorbol-13-acetate (TPA) stimulates the growth of purified resting B cells. Scand J Immunol. 1985 Nov;22(5):591–596. doi: 10.1111/j.1365-3083.1985.tb01919.x. [DOI] [PubMed] [Google Scholar]
- Héry C., Sébire G., Peudenier S., Tardieu M. Adhesion to human neurons and astrocytes of monocytes: the role of interaction of CR3 and ICAM-1 and modulation by cytokines. J Neuroimmunol. 1995 Mar;57(1-2):101–109. doi: 10.1016/0165-5728(94)00168-n. [DOI] [PubMed] [Google Scholar]
- Jaken S., Leach K., Klauck T. Association of type 3 protein kinase C with focal contacts in rat embryo fibroblasts. J Cell Biol. 1989 Aug;109(2):697–704. doi: 10.1083/jcb.109.2.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kanno T., Franzoso G., Siebenlist U. Human T-cell leukemia virus type I Tax-protein-mediated activation of NF-kappa B from p100 (NF-kappa B2)-inhibited cytoplasmic reservoirs. Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12634–12638. doi: 10.1073/pnas.91.26.12634. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knox K. A., Finney M., Milner A. E., Gregory C. D., Wakelam M. J., Michell R. H., Gordon J. Second-messenger pathways involved in the regulation of survival in germinal-centre B cells and in Burkitt lymphoma lines. Int J Cancer. 1992 Dec 2;52(6):959–966. doi: 10.1002/ijc.2910520622. [DOI] [PubMed] [Google Scholar]
- Koong A. C., Chen E. Y., Mivechi N. F., Denko N. C., Stambrook P., Giaccia A. J. Hypoxic activation of nuclear factor-kappa B is mediated by a Ras and Raf signaling pathway and does not involve MAP kinase (ERK1 or ERK2). Cancer Res. 1994 Oct 15;54(20):5273–5279. [PubMed] [Google Scholar]
- Li C. J., Friedman D. J., Wang C., Metelev V., Pardee A. B. Induction of apoptosis in uninfected lymphocytes by HIV-1 Tat protein. Science. 1995 Apr 21;268(5209):429–431. doi: 10.1126/science.7716549. [DOI] [PubMed] [Google Scholar]
- Lindholm P. F., Reid R. L., Brady J. N. Extracellular Tax1 protein stimulates tumor necrosis factor-beta and immunoglobulin kappa light chain expression in lymphoid cells. J Virol. 1992 Mar;66(3):1294–1302. doi: 10.1128/jvi.66.3.1294-1302.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu J., Perkins N. D., Schmid R. M., Nabel G. J. Specific NF-kappa B subunits act in concert with Tat to stimulate human immunodeficiency virus type 1 transcription. J Virol. 1992 Jun;66(6):3883–3887. doi: 10.1128/jvi.66.6.3883-3887.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lotz M., Clark-Lewis I., Ganu V. HIV-1 transactivator protein Tat induces proliferation and TGF beta expression in human articular chondrocytes. J Cell Biol. 1994 Feb;124(3):365–371. doi: 10.1083/jcb.124.3.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Machleidt T., Wiegmann K., Henkel T., Schütze S., Baeuerle P., Krönke M. Sphingomyelinase activates proteolytic I kappa B-alpha degradation in a cell-free system. J Biol Chem. 1994 May 13;269(19):13760–13765. [PubMed] [Google Scholar]
- 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 Mar;37(3):373–380. doi: 10.1002/ana.410370314. [DOI] [PubMed] [Google Scholar]
- Mann D. A., Frankel A. D. Endocytosis and targeting of exogenous HIV-1 Tat protein. EMBO J. 1991 Jul;10(7):1733–1739. doi: 10.1002/j.1460-2075.1991.tb07697.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McConkey D. J., Hartzell P., Amador-Pérez J. F., Orrenius S., Jondal M. Calcium-dependent killing of immature thymocytes by stimulation via the CD3/T cell receptor complex. J Immunol. 1989 Sep 15;143(6):1801–1806. [PubMed] [Google Scholar]
- McConkey D. J., Hartzell P., Jondal M., Orrenius S. Inhibition of DNA fragmentation in thymocytes and isolated thymocyte nuclei by agents that stimulate protein kinase C. J Biol Chem. 1989 Aug 15;264(23):13399–13402. [PubMed] [Google Scholar]
- Meichle A., Schütze S., Hensel G., Brunsing D., Krönke M. Protein kinase C-independent activation of nuclear factor kappa B by tumor necrosis factor. J Biol Chem. 1990 May 15;265(14):8339–8343. [PubMed] [Google Scholar]
- Milani D., Zauli G., Neri L. M., Marchisio M., Previati M., Capitani S. Influence of the human immunodeficiency virus type 1 Tat protein on the proliferation and differentiation of PC12 rat pheochromocytoma cells. J Gen Virol. 1993 Dec;74(Pt 12):2587–2594. doi: 10.1099/0022-1317-74-12-2587. [DOI] [PubMed] [Google Scholar]
- 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 Mar;70(3):1475–1480. doi: 10.1128/jvi.70.3.1475-1480.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nishizuka Y. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science. 1992 Oct 23;258(5082):607–614. doi: 10.1126/science.1411571. [DOI] [PubMed] [Google Scholar]
- Ojeda F., Folch H., Guarda M. I., Jastorff B., Diehl H. A. Induction of apoptosis in thymocytes: new evidence for an interaction of PKC and PKA pathways. Biol Chem Hoppe Seyler. 1995 Jun;376(6):389–393. [PubMed] [Google Scholar]
- Rautonen J., Rautonen N., Martin N. L., Wara D. W. HIV type 1 Tat protein induces immunoglobulin and interleukin 6 synthesis by uninfected peripheral blood mononuclear cells. AIDS Res Hum Retroviruses. 1994 Jul;10(7):781–785. doi: 10.1089/aid.1994.10.781. [DOI] [PubMed] [Google Scholar]
- Roulston A., Beauparlant P., Rice N., Hiscott J. Chronic human immunodeficiency virus type 1 infection stimulates distinct NF-kappa B/rel DNA binding activities in myelomonoblastic cells. J Virol. 1993 Sep;67(9):5235–5246. doi: 10.1128/jvi.67.9.5235-5246.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roulston A., D'Addario M., Boulerice F., Caplan S., Wainberg M. A., Hiscott J. Induction of monocytic differentiation and NF-kappa B-like activities by human immunodeficiency virus 1 infection of myelomonoblastic cells. J Exp Med. 1992 Mar 1;175(3):751–763. doi: 10.1084/jem.175.3.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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 Feb;65(2):961–967. doi: 10.1128/jvi.65.2.961-967.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Samuels E. R., Scott J. E. Distribution and characteristics of Ca+2-phosphatidylserine-dependent protein kinase C in subcellular fractions and lamellar bodies of adult rabbit lung. Life Sci. 1994;55(14):1129–1137. doi: 10.1016/0024-3205(94)00241-x. [DOI] [PubMed] [Google Scholar]
- Scala G., Ruocco M. R., Ambrosino C., Mallardo M., Giordano V., Baldassarre F., Dragonetti E., Quinto I., Venuta S. The expression of the interleukin 6 gene is induced by the human immunodeficiency virus 1 TAT protein. J Exp Med. 1994 Mar 1;179(3):961–971. doi: 10.1084/jem.179.3.961. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schlaepfer D. D., Hanks S. K., Hunter T., van der Geer P. Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature. 1994 Dec 22;372(6508):786–791. doi: 10.1038/372786a0. [DOI] [PubMed] [Google Scholar]
- Schreck R., Baeuerle P. A. Assessing oxygen radicals as mediators in activation of inducible eukaryotic transcription factor NF-kappa B. Methods Enzymol. 1994;234:151–163. doi: 10.1016/0076-6879(94)34085-4. [DOI] [PubMed] [Google Scholar]
- Schreck R., Meier B., Männel D. N., Dröge W., Baeuerle P. A. Dithiocarbamates as potent inhibitors of nuclear factor kappa B activation in intact cells. J Exp Med. 1992 May 1;175(5):1181–1194. doi: 10.1084/jem.175.5.1181. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schütze S., Potthoff K., Machleidt T., Berkovic D., Wiegmann K., Krönke M. TNF activates NF-kappa B by phosphatidylcholine-specific phospholipase C-induced "acidic" sphingomyelin breakdown. Cell. 1992 Nov 27;71(5):765–776. doi: 10.1016/0092-8674(92)90553-o. [DOI] [PubMed] [Google Scholar]
- Sen R., Baltimore D. Inducibility of kappa immunoglobulin enhancer-binding protein Nf-kappa B by a posttranslational mechanism. Cell. 1986 Dec 26;47(6):921–928. doi: 10.1016/0092-8674(86)90807-x. [DOI] [PubMed] [Google Scholar]
- Siebenlist U., Franzoso G., Brown K. Structure, regulation and function of NF-kappa B. Annu Rev Cell Biol. 1994;10:405–455. doi: 10.1146/annurev.cb.10.110194.002201. [DOI] [PubMed] [Google Scholar]
- Sodroski J., Goh W. C., Rosen C., Dayton A., Terwilliger E., Haseltine W. A second post-transcriptional trans-activator gene required for HTLV-III replication. Nature. 1986 May 22;321(6068):412–417. doi: 10.1038/321412a0. [DOI] [PubMed] [Google Scholar]
- Tornatore C., Nath A., Amemiya K., Major E. O. Persistent human immunodeficiency virus type 1 infection in human fetal glial cells reactivated by T-cell factor(s) or by the cytokines tumor necrosis factor alpha and interleukin-1 beta. J Virol. 1991 Nov;65(11):6094–6100. doi: 10.1128/jvi.65.11.6094-6100.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Toullec D., Pianetti P., Coste H., Bellevergue P., Grand-Perret T., Ajakane M., Baudet V., Boissin P., Boursier E., Loriolle F. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J Biol Chem. 1991 Aug 25;266(24):15771–15781. [PubMed] [Google Scholar]
- Tranque P. A., Calle R., Naftolin F., Robbins R. Involvement of protein kinase-C in the mitogenic effect of insulin-like growth factor-I on rat astrocytes. Endocrinology. 1992 Oct;131(4):1948–1954. doi: 10.1210/endo.131.4.1396338. [DOI] [PubMed] [Google Scholar]
- Vogel B. E., Lee S. J., Hildebrand A., Craig W., Pierschbacher M. D., Wong-Staal F., Ruoslahti E. A novel integrin specificity exemplified by binding of the alpha v beta 5 integrin to the basic domain of the HIV Tat protein and vitronectin. J Cell Biol. 1993 Apr;121(2):461–468. doi: 10.1083/jcb.121.2.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vogel J., Hinrichs S. H., Napolitano L. A., Ngo L., Jay G. Liver cancer in transgenic mice carrying the human immunodeficiency virus tat gene. Cancer Res. 1991 Dec 15;51(24):6686–6690. [PubMed] [Google Scholar]
- Vogel J., Hinrichs S. H., Reynolds R. K., Luciw P. A., Jay G. The HIV tat gene induces dermal lesions resembling Kaposi's sarcoma in transgenic mice. Nature. 1988 Oct 13;335(6191):606–611. doi: 10.1038/335606a0. [DOI] [PubMed] [Google Scholar]
- Whisler R. L., Goyette M. A., Grants I. S., Newhouse Y. G. Sublethal levels of oxidant stress stimulate multiple serine/threonine kinases and suppress protein phosphatases in Jurkat T cells. Arch Biochem Biophys. 1995 May 10;319(1):23–35. doi: 10.1006/abbi.1995.1263. [DOI] [PubMed] [Google Scholar]
- Yong V. W. Proliferation of human and mouse astrocytes in vitro: signalling through the protein kinase C pathway. J Neurol Sci. 1992 Aug;111(1):92–103. doi: 10.1016/0022-510x(92)90117-4. [DOI] [PubMed] [Google Scholar]
- Zauli G., Gibellini D., Milani D., Mazzoni M., Borgatti P., La Placa M., Capitani S. Human immunodeficiency virus type 1 Tat protein protects lymphoid, epithelial, and neuronal cell lines from death by apoptosis. Cancer Res. 1993 Oct 1;53(19):4481–4485. [PubMed] [Google Scholar]