HIV tat and neurotoxicity

Microbes and Infection

Volumn 8, Issue 5, 2006, Pages 1347-1357

  King, J E ^a   Eugenin, E A ^a   Buckner, C M ^a   Berman, J W ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Apoptosis; CCL2; Glutamate; Inflammation; NeuroAIDS

Indexed keywords

GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; TRANSACTIVATOR PROTEIN; VIRUS PROTEIN;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ASTROCYTE; BLOOD BRAIN BARRIER; CENTRAL NERVOUS SYSTEM DISEASE; DEMENTIA; ENCEPHALITIS; GENETIC TRANSCRIPTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFLAMMATION; MICROGLIA; NERVE CELL LESION; NEUROPATHOLOGY; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; SHORT SURVEY; SUBSTANCE ABUSE; VIRUS GENE; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

AIDS DEMENTIA COMPLEX; APOPTOSIS; BRAIN; CHEMOKINE CCL2; ENCEPHALITIS, VIRAL; GENE PRODUCTS, TAT; HIV INFECTIONS; HUMANS; NEURONS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 33744920797     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2005.11.014     Document Type: Short Survey

References (112)

1. Albright A.V., Soldan S.S., and Gonzalez-Scarano F. Pathogenesis of human immunodeficiency virus-induced neurological disease. J. Neurovirol. 9 2 (2003) 222-227
2. McArthur J.C., Brew B.J., and Nath A. Neurological complications of HIV infection. Lancet Neurol. 4 9 (2005) 543-555
3. McArthur J.C. HIV dementia: an evolving disease. J. Neuroimmunol. 157 1-2 (2004) 3-10
4. Nath A., and Geiger J.D. Neurobiological aspects of human immunodeficiency virus infection: neurotoxic mechanisms. Prog. Neurobiol. 54 1 (1998) 19-33
5. Kaul M., Garden G.A., and Lipton S.A. Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410 6831 (2001) 988-994
6. Schweighardt B., and Atwood W.J. HIV type 1 infection of human astrocytes is restricted by inefficient viral entry. AIDS Res. Hum. Retroviruses. 17 12 (2001) 1133-1142
7. Ong C.L., Thorpe J.C., Gorry P.R., et al. Low TRBP levels support an innate human immunodeficiency virus type 1 resistance in astrocytes by enhancing the PKR antiviral response. J. Virol. 79 20 (2005) 12763-12772
8. Hudson L., Liu J., Nath A., Jones M., Raghavan R., Narayan O., Male D., and Everall I. Detection of the human immunodeficiency virus regulatory protein tat in CNS tissues. J. Neurovirol. 6 2 (2000) 145-155
9. Wiley C.A., Baldwin M., and Achim C.L. Expression of HIV regulatory and structural mRNA in the central nervous system. AIDS 10 8 (1996) 843-847
10. Banks W.A., Robinson S.M., and Nath A. Permeability of the blood-brain barrier to HIV-1 tat. Exp. Neurol. 193 1 (2005) 218-227
11. Bonavia R., Bajetto A., Barbero S., Albini A., Noonan D.M., and Schettini G. HIV-1 tat causes apoptotic death and calcium homeostasis alterations in rat neurons. Biochem. Biophys. Res. Commun. 288 2 (2001) 301-308
12. Eugenin E.A., D'Aversa T.G., Lopez L., Calderon T.M., and Berman J.W. MCP-1 (CCL2) protects human neurons and astrocytes from NMDA or HIV-tat-induced apoptosis. J. Neurochem. 85 5 (2003) 1299-1311
13. Haughey N.J., Nath A., Mattson M.P., Slevin J.T., and Geiger J.D. HIV-1 tat through phosphorylation of NMDA receptors potentiates glutamate excitotoxicity. J. Neurochem. 78 3 (2001) 457-467
14. Kruman I.I., Nath A., and 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. 154 2 (1998) 276-288
15. Nath A., Haughey N.J., Jones M., Anderson C., Bell J.E., and Geiger J.D. Synergistic neurotoxicity by human immunodeficiency virus proteins tat and gp120: protection by memantine. Ann. Neurol. 47 2 (2000) 186-194
16. Perez A., Probert A.W., Wang K.K., and Sharmeen L. Evaluation of HIV-1 tat induced neurotoxicity in rat cortical cell culture. J. Neurovirol. 7 1 (2001) 1-10
17. Bruce-Keller A.J., Chauhan A., Dimayuga F.O., Gee J., Keller J.N., and Nath A. Synaptic transport of human immunodeficiency virus-tat protein causes neurotoxicity and gliosis in rat brain. J. Neurosci. 23 23 (2003) 8417-8422
18. Kumar A., Dhawan S., Mukhopadhyay A., and Aggarwal B.B. Human immunodeficiency virus-1-tat induces matrix metalloproteinase-9 in monocytes through protein tyrosine phosphatase-mediated activation of nuclear transcription factor NF-kB. FEBS Lett. 462 1-2 (1999) 140-144
19. McManus C.M., Weidenheim K., Woodman S.E., Nunez J., Hesselgesser J., Nath A., and Berman J.W. Chemokine and chemokine-receptor expression in human glial elements: induction by the HIV protein, tat, and chemokine autoregulation. Am. J. Pathol. 156 4 (2000) 1441-1453
20. Rappaport J., Joseph J., Croul S., Alexander G., Del Valle L., Amini S., and Khalili K. Molecular pathway involved in HIV-1-induced CNS pathology: role of viral regulatory protein, tat. J. Leukoc. Biol. 65 4 (1999) 458-465
21. Haughey N.J., Holden C.P., Nath A., and Geiger J.D. Involvement of inositol 1,4,5-trisphosphate-regulated stores of intracellular calcium in calcium dysregulation and neuron cell death caused by HIV-1 protein tat. Journal of Neurochem. 73 4 (1999) 1363-1374
22. Bartz S.R., and Emerman M. Human immunodeficiency virus type 1 tat induces apoptosis and increases sensitivity to apoptotic signals by up-regulating FLICE/Caspase-8. J. Virol. 73 3 (1999) 1956-1963
23. Albini A., Soldi R., Giunciuglio D., et al. The angiogenesis induced by HIV-1 tat protein is mediated by the Flk-1/KDR receptor on vascular endothelial cells. Nat. Med. 2 12 (1996) 1371-1375
24. Ghezzi S., Noonan D.M., Aluigi M.G., et al. Inhibition of CXCR4-dependent HIV-1 infection by extracellular HIV-1 tat. Biochem. Biophys. Res. Commun. 270 3 (2000) 992-996
25. Liu Y., Jones M., Hingtgen C.M., et al. 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. 6 12 (2000) 1380-1387
26. Rebeck G.W., Reiter J.S., Strickland D.K., and Hyman B.T. Apolipoprotein E in sporadic Alzheimer's disease: allelic variation and receptor interactions. Neuron 11 4 (1993) 575-580
27. Herz J., and Strickland D.K. LRP: a multifunctional scavenger and signaling receptor. J. Clin. Invest. 108 6 (2001) 779-784
28. Narita M., Bu G., Holtzman D.M., and Schwartz A.L. The low-density lipoprotein receptor-related protein, a multifunctional apolipoprotein E receptor, modulates hippocampal neurite development. J. Neurochem. 68 2 (1997) 587-595
29. Zerbinatti C.V., and Bu G. LRP and Alzheimer's disease. Rev. Neurosci. 16 2 (2005) 123-135
30. Vives E., Brodin P., and Lebleu B. A truncated HIV-1 tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem. 272 25 (1997) 16010-16017
31. Wadia J.S., Stan R.V., and Dowdy S.F. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat. Med. 10 3 (2004) 310-315
32. Magnuson D.S., Knudsen B.E., Geiger J.D., Brownstone R.M., and Nath A. Human immunodeficiency virus type 1 tat activates non-N-methyl-d-aspartate excitatory amino acid receptors and causes neurotoxicity. Ann. Neurol. 37 3 (1995) 373-380
33. Cheng J., Nath A., Knudsen B., Hochman S., Geiger J.D., Ma M., and Magnuson D.S. Neuronal excitatory properties of human immunodeficiency virus type 1 tat protein. Neuroscience 82 1 (1998) 97-106
34. Chandra T., Maier W., Konig H.G., et al. Molecular interactions of the type 1 human immunodeficiency virus transregulatory protein tat with N-methyl-d-aspartate receptor subunits. Neuroscience 134 1 (2005) 145-153
35. Frankel A.D., Bredt D.S., and Pabo C.O. tat protein from human immunodeficiency virus forms a metal-linked dimer. Science 240 4848 (1998) 70-73
36. Frankel A.D., Chen L., Cotter R.J., and Pabo C.O. Dimerization of the tat protein from human immunodeficiency virus: a cysteine-rich peptide mimics the normal metal-linked dimer interface. Proc. Natl. Acad. Sci. U.S.A. 85 17 (1988) 6297-6300
37. Kim E., and Sheng M. PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5 10 (2004) 771-781
38. Heidinger V., Manzerra P., Wang X.Q., Strasser U., Yu S.-P., Choi D.W., and Behrens M.M. Metabotropic glutamate receptor 1-induced upregulation of NMDA receptor current: mediation through the Pyk2/Src-family kinase pathway in cortical neurons. J. Neurosci. 22 13 (2002) 5452-5461
39. Guo J., Meng F., Fu X., Song B., Yan X., and Zhang G. N-methyl-d-aspartate receptor and L-type voltage-gated Ca2+ channel activation mediate proline-rich tyrosine kinase 2 phosphorylation during cerebral ischemia in rats. Neurosci. Lett. 355 3 (2004) 177-180
40. Prendergast M.A., Rogers D.T., Mulholland P.J., Littleton J.M., Wilkins L.H.J., Self R.L., and Nath A. Neurotoxic effects of the human immunodeficiency virus type-1 transcription factor tat require function of a polyamine sensitive-site on the N-methyl-d-aspartate receptor. Brain Res. 954 2 (2002) 300-307
41. Song L., Nath A., Geiger J.D., Moore A., and Hochman S. Human immunodeficiency virus type 1 tat protein directly activates neuronal N-methyl-d-aspartate receptors at an allosteric zinc-sensitive site. J. Neurovirol. 9 3 (2003) 399-403
42. Paoletti P., Perin-Dureau F., Fayyazuddin A., Le Goff A., Callebaut I., and Neyton J. Molecular organization of a zinc binding n-terminal modulatory domain in a NMDA receptor subunit. Neuron 28 3 (2000) 911-925
43. Li S.-T., Matsushita M., Moriwakiet al. A. HIV-1 inhibits long-term potentiation and attenuates spatial learning. Ann. Neurol. 55 3 (2004) 362-371
44. Clark III J.P., Sampair C.S., Kofuji P., Nath A., and Ding J.M. HIV protein, transactivator of transcription, alters circadian rhythms through the light entrainment pathway. Am J Physiol Regul Integr Comp Physiol. 289 3 (2005) R656-R662
45. Bacskai B.J., Xia M.Q., Strickland D.K., Rebeck G.W., and Hyman B.T. The endocytic receptor protein LRP also mediates neuronal calcium signaling via N-methyl-d-aspartate receptors. Proc. Natl. Acad. Sci. U.S.A. 97 21 (2000) 11551-11556
46. Haughey N.J., and Mattson M.P. Calcium dysregulation and neuronal apoptosis by the HIV-1 proteins tat and gp120. J. Acquir. Immune Defic. Syndr. 31 Suppl 2 (2002) S55-S61
47. Guix F.X., Uribesalgo I., Coma M., and Munoz F.J. The physiology and pathophysiology of nitric oxide in the brain. Prog. Neurobiol. 76 2 (2005) 126-152
48. Cao J., Viholainen J.I., Dart C., Warwick H.K., Leyland M.L., and Courtney M.J. The PSD95-nNOS interface: a target for inhibition of excitotoxic p38 stress-activated protein kinase activation and cell death. J. Cell Biol. 168 1 (2005) 117-126
49. Singh I.N., El-Hage N., Campbell M.E., Lutz S.E., Knapp P.E., Nath A., and Hauser K.F. Differential involvement of p38 and JNK MAP kinases in HIV-1 tat and gp120-induced apoptosis and neurite degeneration in striatal neurons. Neuroscience 135 3 (2005) 781-790
50. Singh I.N., Goody R.J., Dean C., Ahmad N.M., Lutz S.E., Knapp P.E., Nath A., and Hauser K.F. Apoptotic death of striatal neurons induced by human immunodeficiency virus-1 tat and gp120: differential involvement of caspase-3 and endonuclease G. J. Neurovirol. 10 3 (2004) 141-151
51. Campbell G.R., Pasquier E., Watkins J., et al. The Glutamine-rich region of the HIV-1 tat protein is involved in T-cell apoptosis. J. Biol. Chem. 279 46 (2004) 48197-48204
52. Chen D., Wang M., Zhou S., and Zhou Q. HIV-1 tat targets microtubules to induce apoptosis, a process promoted by the pro-apoptotic Bcl-2 relative Bim. EMBO J. 21 24 (2002) 6801-6810
53. Epie N., Ammosova T., Sapir T., Voloshin Y., Lane W., Turner W., Reiner O., and Nekhai S. HIV-1 tat interacts with LIS1 protein. Retrovirology 2 1 (2005) 6
54. Conant K., Garzino-Demo A., Nath A., McArthur J.C., Halliday W., Power C., Gallo R.C., and 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. 95 6 (1998) 3117-3121
55. Cinque P., Vago L., Mengozzi M., et al. Elevated cerebrospinal fluid levels of monocyte chemotactic protein-1 correlate with HIV-1 encephalitis and local viral replication. AIDS 12 11 (1998) 1327-1332
56. Mankowski J.L., Queen S.E., Clements J.E., and Zink M.C. Cerebrospinal fluid markers that predict SIV CNS disease. J. Neuroimmunol. 157 1-2 (2004) 66-70
57. Zink M.C., Coleman G.D., Mankowski J.L., Adams R.J., Tarwater P.M., Fox K, and Clements J.E. Increased macrophage chemoattractant protein-1 in cerebrospinal fluid precedes and predicts simian immunodeficiency virus encephalitis. J. Infect. Dis. 184 8 (2001) 1015-1021
58. Zink M.C., Uhrlaub J., DeWitt J., et al. Neuroprotective and anti-human immunodeficiency virus activity of minocycline. JAMA 293 16 (2005) 2003-2011
59. Lim S.P., and Garzino-Demo A. The human immunodeficiency virus type 1 tat protein up-regulates the promoter activity of the beta-chemokine monocyte chemoattractant protein 1 in the human astrocytoma cell line U-87 MG: role of SP-1, AP-1, and NF-kappa B consensus sites. J. Virol. 74 4 (2000) 1632-1640
60. Sheng W.S., Hu S., Lokensgard J.R., and Peterson P.K. U50,488 inhibits HIV-1 tat-induced monocyte chemoattractant protein-1 (CCL2) production by human astrocytes. Biochem. Pharmacol. 65 1 (2003) 9-14
61. Abraham S., Sawaya B.E., Safak M., Batuman O., Khalili K., and Amini S. Regulation of MCP-1 gene transcription by Smads and HIV-1 tat in human glial cells. Virology 309 2 (2003) 132-146
62. Abraham S., Sweet T., Sawaya B.E., Rappaport J., Khalili K., and Amini S. Cooperative interaction of C/EBP beta and tat modulates MCP-1 gene transcription in astrocytes. J. Neuroimmunol. 160 1-2 (2005) 219-227
63. LeClair K.P., Blanar M.A., and Sharp P.A. The p50 subunit of NF-{kappa}B associates with the NF-IL6 transcription factor. Proc. Natl. Acad. Sci. U.S.A. 89 17 (1992) 8145-8149
64. Stein B., Cogswell P.C., and Baldwin A.S.J. Functional and physical associations between NF-kappa B and C/EBP family members: a Rel domain-bZIP interaction. Mol. Cell Biol. 13 7 (1993) 3964-3974
65. Fine S.M., Angel R.A., Perry S.W., Epstein L.G., Rothstein J.D., Dewhurst S., and Gelbard H.A. Tumor necrosis factor alpha inhibits glutamate uptake by primary human astrocytes. Implications for pathogenesis of HIV-1 dementia. J. Biol. Chem. 271 26 (1996) 15303-15306
66. Zhou B.Y., Liu Y., Kim B., Xiao Y., and He J.J. Astrocyte activation and dysfunction and neuron death by HIV-1 tat expression in astrocytes. Mol. Cell. Neurosci. 27 3 (2004) 296-305
67. Wang Z., Pekarskaya O., Bencheikh M., Chao W., Gelbard H.A., Ghorpade A., Rothstein J.D., and Volsky D.J. Reduced expression of glutamate transporter EAAT2 and impaired glutamate transport in human primary astrocytes exposed to HIV-1 or gp120. Virology 312 1 (2003) 60-73
68. Liu X., Jana M., Dasgupta S., Koka S., He J., Wood C., and Pahan K. Human immunodeficiency virus type 1 (HIV-1) Tat induces nitric-oxide synthase in human astroglia. J. Biol. Chem. 277 42 (2002) 39312-39319
69. Amini S., Mameli G., Del Valle L., et al. p73 Interacts with human immunodeficiency virus type 1 tat in astrocytic cells and prevents its acetylation on lysine 28. Mol. Cell Biol. 25 18 (2005) 8126-8138
70. Saunders M., Eldeen M.B., Valle L.D., et al. p73 modulates HIV-1 tat transcriptional and apoptotic activities in human astrocytes. Apoptosis (2005)
71. Chauhan A., Turchan J., Pocernich C., Bruce-Keller A., Roth S., Butterfield D.A., Major E.O., and Nath A. Intracellular human immunodeficiency virus tat expression in astrocytes promotes astrocyte survival but induces potent neurotoxicity at distant sites via axonal transport. J. Biol. Chem. 278 15 (2003) 13512-13519
72. Sevigny J.J., Albert S.M., McDermott M.P., et al. Evaluation of HIV RNA and markers of immune activation as predictors of HIV-associated dementia. Neurology 63 11 (2004) 2084-2090
73. D'Aversa T.G., Eugenin E.A., and Berman J.W. NeuroAIDS: contributions of the human immunodeficiency virus-1 proteins tat and gp120 as well as CD40 to microglial activation. J. Neurosci. Res. 81 3 (2005) 436-446
74. Minghetti L., Visentin S., Patrizio M., Franchini L., Ajmone-Cat M.A., and Levi G. Multiple actions of the human immunodeficiency virus type-1 tat protein on microglial cell functions. Neurochem. Res. 29 5 (2004) 965-978
75. D'Aversa T.G., Yu K.O., and Berman J.W. Expression of chemokines by human fetal microglia after treatment with the human immunodeficiency virus type 1 protein tat. J. Neurovirol. 10 2 (2004) 86-97
76. Lokensgard J.R., Hu S., Hegg C.C., Thayer S.A., Gekker G., and Peterson P.K. Diazepam inhibits HIV-1 tat-induced migration of human microglia. J. Neurovirol. 7 5 (2001) 481-486
77. Eugenin E.A., Dyer G., Calderon T.M., and Berman J.W. HIV-1 tat protein induces a migratory phenotype in human fetal microglia by a CCL2 (MCP-1)-dependent mechanism: possible role in NeuroAIDS. Glia 49 4 (2005) 501-510
78. Goldstein G.W. Endothelial cell-astrocyte interactions. A cellular model of the blood-brain barrier. Ann. N.Y. Acad. Sci. 529 (1988) 31-39
79. Toborek M., Lee Y.W., Flora G., Pu H., Andras I.E., Wylegala E., Hennig B., and Nath A. Mechanisms of the blood-brain barrier disruption in HIV-1 infection. Cell. Mol. Neurobiol. 25 1 (2005) 181-199
80. Eugenin E.A., and Berman J.W. Chemokine-dependent mechanisms of leukocyte trafficking across a model of the blood-brain barrier. Methods 29 4 (2003) 351-361
81. Dallasta L.M., Pisarov L.A., Esplen J.E., Werley J.V., Moses A.V., Nelson J.A., and Achim C.L. Blood-brain barrier tight junction disruption in human immunodeficiency virus-1 encephalitis. Am. J. Pathol. 155 6 (1999) 1915-1927
82. András I.E., Pu H., Deli M.A., Nath A., Hennig B., and Toborek M. HIV-1 tat protein alters tight junction protein expression and distribution in cultured brain endothelial cells. J. Neurosci. Res. 74 2 (2003) 255-265
83. Toborek M., Lee Y.W., Pu H., et al. HIV-tat protein induces oxidative and inflammatory pathways in brain endothelium. J. Neurochem. 84 1 (2003) 169-179
84. Hawkins B.T., and Davis T.P. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol. Rev. 57 2 (2005) 173-185
85. Aurrand-Lions M., Johnson-Leger C., and Imhof B.A. The last molecular fortress in leukocyte trans-endothelial migration. Nat. Immunol. 3 2 (2002) 116-118
86. Muller W.A., and Randolph G.J. Migration of leukocytes across endothelium and beyond: molecules involved in the transmigration and fate of monocytes. J. Leukoc. Biol. 66 5 (1999) 698-704
87. Adamson D.C., Dawson T.M., Zink M.C., Clements J.E., and Dawson V.L. Neurovirulent simian immunodeficiency virus infection induces neuronal, endothelial, and glial apoptosis. Mol. Med. 2 4 (1996) 417-428
88. Shi B., De Girolami U., He J., Wang S., Lorenzo A., Busciglio J., and Gabuzda D. Apoptosis induced by HIV-1 infection of the central nervous system. J. Clin. Invest. 98 9 (1996) 1979-1990
89. Khan N.A., Di Cello F., Nath A., and Kim K.S. Human immunodeficiency virus type 1 tat-mediated cytotoxicity of human brain microvascular endothelial cells. J. Neurovirol. 9 6 (2003) 584-593
90. Kim T.-A., Avraham H.K., Koh Y-H, Jiang S., Park I.-W., and Avraham S. HIV-1 tat-mediated apoptosis in human brain microvascular endothelial cells. J. Immunol. 170 5 (2003) 2629-2637
91. Bergonzini V., Delbue S., Wang J.Y., Reiss K., Prisco M., Amini S., Khalili K., and Peruzzi F. HIV-tat promotes cellular proliferation and inhibits NGF-induced differentiation through mechanisms involving Id1 regulation. Oncogene 23 46 (2004) 7701-7711
92. Wong K., Sharma A., Awasthi S., et al. HIV-1 tat interactions with p300 and PCAF transcriptional coactivators inhibit histone acetylation and neurotrophin signaling through CREB. J. Biol. Chem. 280 10 (2005) 9390-9399
93. Peruzzi F., Gordon J., Darbinian N., and Amini S. Tat-induced deregulation of neuronal differentiation and survival by nerve growth factor pathway. J. Neurovirol. 8 Suppl. 2 (2002) 91-96
94. Bres V., Tagami H., Peloponese J.-M., et al. Differential acetylation of Tat coordinates its interaction with the co-activators cyclin T1 and PCAF. EMBO J. 21 24 (2002) 6811-6819
95. Dorr A., Kiermer V., Pedal A., et al. Transcriptional synergy between tat and PCAF is dependent on the binding of acetylated tat to the PCAF bromodomain. EMBO J. 21 11 (2002) 2715-2723
96. Kaehlcke K., Dorr A., Hetzer-Egger C., et al. Acetylation of tat defines a cyclinT1-independent step in HIV transactivation. Mol. Cell 12 1 (2003) 167-176
97. Kiernan R.E., Vanhulle C., Schiltz L., et al. HIV-1 tat transcriptional activity is regulated by acetylation. EMBO J. 18 21 (1999) 6106-6118
98. Mujtaba S., He Y., Zeng L., Farooq A., Carlson J.E., Ott M., Verdin E., and Zhou M.M. Structural basis of lysine-acetylated HIV-1 tat recognition by PCAF bromodomain. Mol. Cell 9 3 (2002) 575-586
99. Ott M., Schnolzer M., Garnica J., Fischle W., Emiliani S., Rackwitz H.R., and Verdin E. Acetylation of the HIV-1 tat protein by p300 is important for its transcriptional activity. Curr. Biol. 9 24 (1999) 1489-1492
100. Ramirez S.H., Sanchez J.F., Dimitri C.A., Gelbard H.A., Dewhurst S., and Maggirwar S.B. Neurotrophins prevent HIV tat-induced neuronal apoptosis via a nuclear factor-κB (NFκB)-dependent mechanism. J. Neurochem. 78 4 (2001) 874-889
101. Nath A., Maragos W.F., Avison M.J., Schmitt F.A., and Berger J.R. Acceleration of HIV dementia with methamphetamine and cocaine. J. Neurovirol. 7 1 (2001) 66-71
102. Nair M.P., Schwartz S.A., Mahajan S.D., Tsiao C., Chawda R.P., Whitney R., Don Sykes B.B., and Hewitt R. Drug abuse and neuropathogenesis of HIV infection: role of DC-SIGN and IDO. J. Neuroimmunol. 157 1-2 (2004) 56-60
103. Conant K., St Hillaire C., Anderson C., Galey D., Wang J., and Nath A. Human immunodeficiency virus type 1 tat and methamphetamine affect the release and activation of matrix-degrading proteinases. J. Neurovirol. 10 1 (2004) 21-28
104. Nath A., Hauser K.F., Wojna V., Booze R.M., Maragos W., Prendergast M., Cass W., and Turchan J.T. Molecular basis for interactions of HIV and drugs of abuse. J. Acquir. Immune. Defic. Syndr. 31 Suppl. 2 (2002) S62-S69
105. El-Hage N., Gurwell J.A., Singh I.N., Knapp P.E., Nath A., and Hauser K.F. Synergistic increases in intracellular Ca2+, and the release of MCP-1, RANTES, and IL-6 by astrocytes treated with opiates and HIV-1 tat. Glia 50 2 (2005) 91-106
106. El-Hage N., Wu G., Wang J., Ambati J., Knapp P.E., Reed J.L., Bruce-Keller A.J., and Hauser K.F. HIV-1 tat and opiate-induced changes in astrocytes promote chemotaxis of microglia through the expression of MCP-1 and alternative chemokines. Glia 53 2 (2006) 132-146
107. Khurdayan V.K., Buch S., El-Hage N., et al. Preferential vulnerability of astroglia and glial precursors to combined opioid and HIV-1 tat exposure in vitro. Eur. J. Neurosci. 19 12 (2004) 3171-3182
108. Gurwell J.A., Nath A., Sun Q., Zhang J., Martin K.M., Chen Y., and Hauser K.F. Synergistic neurotoxicity of opioids and human immunodeficiency virus-1 tat protein in striatal neurons in vitro. Neuroscience 102 3 (2001) 555-563
109. Langford D., Grigorian A., Hurford R., Adame A., Crews L., and Masliah E. The role of mitochondrial alterations in the combined toxic effects of human immunodeficiency virus tat protein and methamphetamine on calbindin positive-neurons. J. Neurovirol. 10 6 (2004) 327-337
110. Maragos W.F., Young K.L., Turchan J.T., Guseva M., Pauly J.R., Nath A., and Cass W.A. Human immunodeficiency virus-1 tat protein and methamphetamine interact synergistically to impair striatal dopaminergic function. J. Neurochem. 83 4 (2002) 955-963
111. Turchan J., Anderson C., Hauser K., et al. Estrogen protects against the synergistic toxicity by HIV proteins, methamphetamine and cocaine. BMC Neurosci. 2 1 (2001) 3
112. Eugenin E.A., Osiecki K., Lopez L., Calderon T.M., and Berman J.W. CCL2/monocyte chemoattractant protein-1 mediates enhanced transmigration of human immunodeficiency virus (HIV)-infected leukocytes across the blood brain barrier: a potential mechanism of HIV-CNS invasion and NeuroAIDS. J. Neurosci. 26 4 (2006) 1098-1106