HIV-1 tat promotes lysosomal exocytosis in astrocytes and contributes to astrocyte-mediated tat neurotoxicity

Journal of Biological Chemistry

Volumn 291, Issue 43, 2016, Pages 22830-22840

  Fan, Yan ^a   He, Johnny J ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; CELL MEMBRANES; CHEMICAL ACTIVATION; ELECTROPHORESIS; MASS SPECTROMETRY; NEURODEGENERATIVE DISEASES; PROTEINS;

ACIDIC PROTEINS; HYDROLYTIC ENZYME; MEMBRANE-ASSOCIATED PROTEINS; MOLECULAR MECHANISM; TIGHTLY-COUPLED; TWO-DIMENSIONAL GEL ELECTROPHORESIS; UNFOLDED PROTEIN RESPONSE; UP-REGULATION;

DISEASES;

CALCIUM PHOSPHATE; GREEN FLUORESCENT PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MEMBRANE LIPID; TRANSACTIVATOR PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIAL FIBRILLARY ASTROCYTIC PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; AUTOPHAGY; CELL DEATH; CELL MEMBRANE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; EXOCYTOSIS; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HYDROLYSIS; INTRACELLULAR SIGNALING; MASS SPECTROMETRY; MOLECULAR MECHANICS; MOUSE; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PATHOGENESIS; PRECIPITATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUPERNATANT; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; PATHOLOGY; TOXICITY AND INTOXICATION; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; ASTROCYTES; CELL LINE, TUMOR; ENDOPLASMIC RETICULUM STRESS; EXOCYTOSIS; GLIAL FIBRILLARY ACIDIC PROTEIN; HIV-1; HUMANS; MICE; MICE, TRANSGENIC; NEUROTOXICITY SYNDROMES; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; UP-REGULATION;

EID: 84992390018     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.731836     Document Type: Article

References (84)

1. An, S. F., Groves, M., Gray, F., and Scaravilli, F. (1999) Early entry and widespread cellular involvement of HIV-1 DNA in brains of HIV-1 positive asymptomatic individuals. J. Neuropathol. Exp. Neurol. 58, 1156-1162
2. Price, R. W., and Brew, B. J. (1988) The AIDS dementia complex. J. Infect. Dis. 158, 1079-1083
3. Ellis, R. J., Deutsch, R., Heaton, R. K., Marcotte, T. D., McCutchan, J. A., Nelson, J. A., Abramson, I., Thal, L. J., Atkinson, J. H., Wallace, M. R., and Grant, I. (1997) Neurocognitive impairment is an independent risk factor for death in HIV infection. San Diego HIV Neurobehavioral Research Center Group. Arch. Neurol. 54, 416-424
4. Cohen, R. A., and Gongvatana, A. (2009) HIV-associated brain dysfunction in the era of HAART: reasons for hope, but continued concern. Neurology 73, 338-339
5. Ellis, R., Langford, D., and Masliah, E. (2007) HIV and antiretroviral therapy in the brain: neuronal injury and repair. Nat. Rev. Neurosci. 8, 33-44
6. Del Valle, L., and Piña-Oviedo, S. (2006) HIV disorders of the brain: pathology and pathogenesis. Front. Biosci. 11, 718-732
7. Lee, S. C., and Hatch., W. C., Liu, W., Brosnan, C. F., and Dickson, D.W. (1993) Productive infection of human fetal microglia in vitro by HIV-1. Ann. N.Y. Acad. Sci. 693, 314-316
8. Saito, Y., and Sharer., L. R., Epstein, L. G., Michaels, J., Mintz, M., Louder, M., Golding, K., Cvetkovich, T. A., and Blumberg, B. M. (1994) Overexpression of nef as a marker for restricted HIV-1 infection of astrocytes in postmortem pediatric central nervous tissues. Neurology 44, 474-481
9. Ensoli, B., Buonaguro, L., Barillari, G., Fiorelli, V., Gendelman, R., Morgan, R. A., Wingfield, P., and Gallo, R. C. (1993) Release, uptake, and effects of extracellular human immunodeficiency virus type 1 Tat protein on cell growth and viral transactivation. J. Virol. 67, 277-287
10. Hudson, L., Liu, J., Nath, A., Jones, M., Raghavan, R., Narayan, O., Male, D., and Everall, I. (2000) Detection of the human immunodeficiency virus regulatory protein tat in CNS tissues. J. Neurovirol. 6, 145-155
11. Nath, A., Psooy, K., Martin, C., Knudsen, B., and Magnuson., D. S., Haughey, N., and Geiger, J. D. (1996) Identification of a human immunodeficiency virus type 1 Tat epitope that is neuroexcitatory and neurotoxic. J. Virol. 70, 1475-1480
12. Sabatier, J. M., Vives, E., Mabrouk, K., Benjouad, A., Rochat, H., Duval, A., Hue, B., and Bahraoui, E. (1991) Evidence for neurotoxic activity of tat from human immunodeficiency virus type 1. J. Virol. 65, 961-967
13. Benelli, R., Barbero, A., Ferrini, S., Scapini, P., Cassatella, M., Bussolino, F., Tacchetti, C, and Noonan., D. M., and Albini, A. (2000) Human immunodeficiency virus transactivator protein (Tat) stimulates chemotaxis, calcium mobilization, and activation of human polymorphonuclear leukocytes: implications for Tat-mediated pathogenesis. J. Infect. Dis. 182, 1643-1651
14. Lafrenie, R. M., and Wahl., L. M., Epstein, J. S., Hewlett, I. K., Yamada, K. M., and Dhawan, S. (1996) HIV-1-Tat protein promotes chemotaxis and invasive behavior by monocytes. J. Immunol. 157, 974-977
15. Park, I. W., and Wang., J. F., and Groopman, J. E. (2001) HIV-1 Tat promotes monocyte chemoattractant protein-1 secretion followed by transmigration of monocytes. Blood 97, 352-358
16. Jones, M., Olafson, K., Del Bigio, M. R., Peeling, J., and Nath, A. (1998) Intraventricular injection of human immunodeficiency virus type 1 (HIV-1) tat protein causes inflammation, gliosis, apoptosis, and ventricular enlargement. J. Neuropathol. Exp. Neurol. 57, 563-570
17. Conant, K., Garzino-Demo, A., Nath, A., and McArthur., J. C., Halliday, W., Power, C., Gallo, R. C., and Major, E. O. (1998) 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, 3117-3121
18. Magnuson, D. S., and Knudsen., B. E., Geiger, J. D., Brownstone, R. M., and Nath, A. (1995) Human immunodeficiency virus type 1 tat activates non-N-methyl-D-aspartate excitatory amino acid receptors and causes neurotoxicity. Ann. Neurol. 37, 373-380
19. Hui, L., Chen, X., Haughey, N. J., and Geiger, J. D. (2012) Role of endoly-sosomes in HIV-1 Tat-induced neurotoxicity. ASNNeuro 4, 243-252
20. Chauhan, A., Turchan, J., Pocernich, C., Bruce-Keller, A., Roth, S., and Butterfield., D. A., Major, E. O., and Nath, A. (2003) 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, 13512-13519
21. Zhou, B. Y., and He, J. J. (2004) Proliferation inhibition of astrocytes, neurons, and non-glial cells by HIV-1 Tat protein. Neurosci. Lett. 359, 155-158
22. Zhou, B. Y., Liu, Y., Kim, B. O., Xiao, Y., and He, J. J. (2004) Astrocyte activation and dysfunction and neuron death by HIV-1 Tat expression in astrocytes. Mol. Cell Neurosci. 27, 296-305
23. Ranki, A., Nyberg, M., Ovod, V., Haltia, M., Elovaara, I., Raininko, R., Haapasalo, H., and Krohn, K. (1995) Abundant expression of HIVNef and Rev proteins in brain astrocytes in vivo is associated with dementia. AIDS 9, 1001-1008
24. Brack-Werner, R. (1999) Astrocytes: HIV cellular reservoirs and important participants in neuropathogenesis. AIDS 13, 1-22
25. Atwood, W. J., and Tornatore., C. S., Meyers, K., and Major, E. O. (1993) HIV-1 mRNA transcripts from persistently infected human fetal astrocytes. Ann. N.Y. Acad. Sci. 693, 324-325
26. Kolson, D. L., Buchhalter, J., Collman, R., Hellmig, B., and Farrell., C. F., Debouck, C., and Gonzalez-Scarano, F. (1993) HIV-1 Tat alters normal organization of neurons and astrocytes in primary rodent brain cell cultures: RGD sequence dependence. AIDS Res. Hum. Retroviruses 9, 677-685
27. 2+, and the release of MCP-1, RANTES, and IL-6 by astrocytes treated with opiates and HIV-1 Tat. Glia 50, 91-106
28. Williams, R., Yao, H., Dhillon, N. K., and Buch, S. J. (2009) HIV-1 Tat co-operates with IFN-γ and TNF-α to increase CXCL10 in human astrocytes. PLoS One 4, e5709
29. Fan, Y., Zou, W., Green, L. A., Kim, B. O., and He, J. J. (2011) Activation of Egr-1 expression in astrocytes by HIV-1 Tat: new insights into astrocytemediated Tat neurotoxicity. J. Neuroimmune Pharmacol. 6, 121-129
30. Zou, W., Wang, Z., Liu, Y., Fan, Y., and Zhou., B. Y., Yang, X. F., and He, J. J. (2010) Involvement of p300 in constitutive and HIV-1 Tat-activated expression of glial fibrillary acidic protein in astrocytes. Glia 58, 1640-1648
31. Fan, Y., and Timani., K. A., and He, J. J. (2015) STAT3 and its phosphorylation are involved in HIV-1 Tat-induced transactivation of glial fibrillary acidic protein. Curr. HIV Res. 13, 55-63
32. Kim, B. O., Liu, Y., Ruan, Y., Xu, Z. C, Schantz, L., and He, J. J. (2003) Neuropathologies in transgenic mice expressing human immunodeficiency virus type 1 Tat protein under the regulation of the astrocyte-specific glial fibrillary acidic protein promoter and doxycycline. Am. J. Pathol. 162, 1693-1707
33. Fitting, S., Ignatowska-Jankowska, B. M., Bull, C, Skoff, R. P., Lichtman, A. H., Wise, L. E., Fox, M. A., Su, J., Medina, A. E., Krahe, T. E., Knapp, P. E., Guido, W., and Hauser, K. F. (2013) Synaptic dysfunction in the hippocampus accompanies learning and memory deficits in human immunodeficiency virus type-1 Tat transgenic mice. Biol. Psychiatry 73, 443-453
34. Chen, P., Mayne, M., Power, C, and Nath, A. (1997) The Tat protein of HIV-1 induces tumor necrosis factor-α production. Implications for HIV-1-associated neurological diseases. J. Biol. Chem. 272, 22385-22388
35. Turchan-Cholewo, J., Dimayuga, F. O., Gupta, S., Keller, J. N, Knapp, P. E., Hauser, K. F., and Bruce-Keller, A. J. (2009) Morphine and HIV-Tat increase microglial-free radical production and oxidative stress: possible role in cytokine regulation. J. Neurochem. 108, 202-215
36. Boje, K. M., and Arora, P. K. (1992) Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Res. 587, 250-256
37. Shute, A. A., and Cormier., R. J., Moulder, K. L., Benz, A., Isenberg, K. E., Zorumski, C. F., and Mennerick, S. (2005) Astrocytes exert a pro-apoptotic effect on neurons in postnatal hippocampal cultures. Neuroscience 131, 349-358
38. Papagapiou, M. P., and Auer, R. N. (1990) Regional neuroprotective effects of the NMDA receptor antagonist MK-801 (dizocilpine) in hypoglycemic brain damage. J. Cereb. Blood FlowMetab. 10, 270-276
39. 2+-regulated exocytic vesicles in fibroblasts and epithelial cells. J. Cell Biol. 137, 93-104
40. Akopova, I., Tatur, S., Grygorczyk, M., Luchowski, R., Gryczynski, I., Gryczynski, Z., Borejdo, J., and Grygorczyk, R. (2012) Imaging exocytosis of ATP-containing vesicles with TIRF microscopy in lung epithelial A549 cells. Purinergic Signal. 8, 59-70
41. Parks, A., Charest-Morin, X., Boivin-Welch, M., Bouthillier, J., and Marceau, F. (2015) Autophagic flux inhibition and lysosomogenesis ensuing cellular capture and retention of the cationic drug quinacrine in murine models. Peer J 3, e1314
42. Jung, J., Uesugi, N, and Jeong., N. Y., Park, B. S., Konishi, H., and Kiyama, H. (2016) Increase of transcription factor EB (TFEB) and lysosomes in rat DRG neurons and their transportation to the central nerve terminal in dorsal horn after nerve injury. Neuroscience 313, 10-22
43. Bastow, E. R., Last, K., Golub, S., Stow, J. L., Stanley, A. C, and Fosang, A. J. (2012) Evidence for lysosomal exocytosis and release of aggrecan-degrading hydrolases from hypertrophic chondrocytes, in vitro and in vivo. Biol. Open 1, 318-328
44. 2+-dependent lysosomal exocytosis but not cell resealing. EMBO Rep. 5, 883-888
45. Schotte, P., Schauvliege, R., Janssens, S., and Beyaert, R. (2001) The cathepsin B inhibitor z-FA. fmk inhibits cytokine production in macrophages stimulated by lipopolysaccharide. J. Biol. Chem. 276, 21153-21157
46. Lawrence, C. P., Kadioglu, A., Yang, A. L., Coward, W. R., and Chow, S. C. (2006) The cathepsin B inhibitor, z-FA-fmk, inhibits human T cell proliferation in vitro and modulates host response to pneumococcal infection in vivo. J. Immunol. 177, 3827-3836
47. Rodriguez-Franco, E. J., Cantres-Rosario, Y. M., Plaud-Valentin, M., Romeu, R., Rodríguez, Y., Skolasky, R., Meléndez, V., Cadilla, C. L., and Melendez, L. M. (2012) Dysregulation of macrophage-secreted cathepsin B contributes to HIV-1-linked neuronal apoptosis. PLoS One 7, e36571
48. Gan, L., Ye, S., Chu, A., Anton, K., Yi, S., Vincent, V. A., von Schack, D., Chin, D., Murray, J., Lohr, S., Patthy, L., Gonzalez-Zulueta, M., Nikolich, K., and Urfer, R. (2004) Identification of cathepsin B as a mediator of neuronal death induced by Aβ-activated microglial cells using a functional genomics approach. J. Biol. Chem. 279, 5565-5572
49. Sun, L., Wu, Z., Baba, M., Peters, C, Uchiyama, Y., and Nakanishi, H. (2010) Cathepsin B-dependent motor neuron death after nerve injury in the adult mouse. Biochem. Biophys. Res. Commun. 399, 391-395
50. Qi, X., Hosoi, T., Okuma, Y., Kaneko, M., and Nomura, Y. (2004) Sodium 4-phenylbutyrate protects against cerebral ischemic injury. Mol. Pharmacol. 66, 899-908
51. Johnson, T. P., Patel, K., Johnson, K. R., Maric, D., Calabresi, P. A., Hasbun, R., and Nath, A. (2013) Induction of IL-17 and nonclassical T-cell activation by HIV-Tat protein. Proc. Natl. Acad. Sci. U.S.A. 110, 13588-13593
52. Banks, W. A., and Robinson., S. M., and Nath, A. (2005) Permeability of the blood-brain barrier to HIV-1 Tat. Exp. Neurol. 193, 218-227
53. Jin, J., Lam, L., Sadic, E., Fernandez, F., Tan, J., and Giunta, B. (2012) HIV-1 Tat-induced microglial activation and neuronal damage is inhibited via CD45 modulation: a potential new treatment target for HAND. Am. J. Transl. Res. 4, 302-315
54. Fine, S. M., and Angel., R. A., Perry, S. W., Epstein, L. G., Rothstein, J. D., Dewhurst, S., and Gelbard, H. A. (1996) Tumor necrosis factor a inhibits glutamate uptake by primary human astrocytes: implications for pathogenesis of HIV-1 dementia. J. Biol. Chem. 271, 15303-15306
55. Høyer-Hansen, M., and Jäättelä, M. (2007) Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ. 14, 1576-1582
56. Saito, A., Hino, S., Murakami, T., Kondo, S., and Imaizumi, K. (2007) A novel ER stress transducer, OASIS, expressed in astrocytes. Antioxid. Redox Signal. 9, 563-571
57. Harding, H. P., Zhang, Y., and Ron, D. (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274
58. Hammadi, M., Oulidi, A., Gackière, F., Katsogiannou, M., Slomianny, C, Roudbaraki, M., Dewailly, E., Delcourt, P., Lepage, G., Lotteau, S., Ducreux, S., Prevarskaya, N., and Van Coppenolle, F. (2013) Modulation of ER stress and apoptosis by endoplasmic reticulum calcium leak via translocon during unfolded protein response: involvement of GRP78. FASEBJ. 27, 1600-1609
59. Südhof, T. C. (2012) Calcium control of neurotransmitter release. Cold Spring Harbor Perspect. Biol. 4, a011353
60. Buma, P., and Roubos, E. W. (1983) Calcium dynamics, exocytosis, and membrane turnover in the ovulation hormone-releasing caudo-dorsal cells of Lymnaea stagnalis. Cell Tissue Res. 233, 143-159
61. Raraty, M., Ward, J., Erdemli, G., Vaillant, C, and Neoptolemos., J. P., Sutton, R., and Petersen, O. H. (2000) Calcium-dependent enzyme activation and vacuole formation in the apical granular region of pancreatic acinar cells. Proc. Natl. Acad. Sci. U.S.A. 97, 13126-13131
62. Zhang, Z., Chen, G., Zhou, W., Song, A., Xu, T., Luo, Q., Wang, W., and Gu., X. S., and Duan, S. (2007) Regulated ATP release from astrocytes through lysosome exocytosis. Nat Cell Biol. 9, 945-953
63. Ferri, K. F., and Kroemer, G. (2001) Organelle-specific initiation of cell death pathways. Nat Cell Biol. 3, E255-E263
64. Leist, M., and Jäättelä, M. (2001) Triggering of apoptosis by cathepsins. Cell Death Differ. 8, 324-326
65. Haughey, N. J., and Mattson, M. P. (2002) Calcium dysregulation and neuronal apoptosis by the HIV-1 proteins Tat and gp120. J. Acquir. Immune Defic. Syndr. 31, S55-S61
66. Mayne, M., and Holden., C. P., Nath, A., and Geiger, J. D. (2000) Release of calcium from inositol 1,4,5-trisphosphate receptor-regulated stores by HIV-1 Tat regulates TNF-α production in human macrophages. J. Immunol. 164, 6538-6542
67. Leist, M., and Jäättelä, M. (2001) Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev. Mol. Cell Biol. 2, 589-598
68. Los, M., Wesselborg, S., and Schulze-Osthoff, K. (1999) The role of caspases in development, immunity, and apoptotic signal transduction: lessons from knockout mice. Immunity 10, 629-639
69. Houseweart, M. K., and Pennacchio., L. A., Vilaythong, A., Peters, C., Noebels, J. L., and Myers, R. M. (2003) Cathepsin B but not cathepsins L or S contributes to the pathogenesis of Unverricht-Lundborg progressive myoclonus epilepsy (EPM1). J. Neurobiol. 56, 315-327
70. Lieuallen, K., and Pennacchio., L. A., Park, M., Myers, R. M., and Lennon, G. G. (2001) Cystatin B-deficient mice have increased expression of apoptosis and glial activation genes. Hum. Mol. Genet. 10, 1867-1871
71. Rempel, S. A., and Rosenblum., M. L., Mikkelsen, T., Yan, P. S., Ellis, K. D., Golembieski, W. A., Sameni, M., Rozhin, J., Ziegler, G., and Sloane, B. F. (1994) Cathepsin B expression and localization in glioma progression and invasion. Cancer Res. 54, 6027-6031
72. Tsuchiya, K., Kohda, Y., Yoshida, M., Zhao, L., Ueno, T., Yamashita, J., Yoshioka, T., Kominami, E., and Yamashima, T. (1999) Postictal blockade of ischemic hippocampal neuronal death in primates using selective cathepsin inhibitors. Exp. Neurol. 155, 187-194
73. Amritraj, A., Wang, Y., Revett, T. J., Vergote, D., Westaway, D., and Kar, S. (2013) Role of cathepsin D in U18666A-induced neuronal cell death: potential implication in Niemann-Pick type C disease pathogenesis. J. Biol. Chem. 288, 3136-3152
74. Liang, Q., Ouyang, X., Schneider, L., and Zhang, J. (2011) Reduction of mutant huntingtin accumulation and toxicity by lysosomal cathepsins D and B in neurons. Mol. Neurodegener. 6, 37
75. Koike, M., Nakanishi, H., Saftig, P., Ezaki, J., Isahara, K., Ohsawa, Y., Schulz-Schaeffer, W., Watanabe, T., Waguri, S., Kametaka, S., Shibata, M., Yamamoto, K., Kominami, E., Peters, C., von Figura, K., and Uchiyama, Y. (2000) Cathepsin D deficiency induces lysosomal storage with ceroid lipofuscin in mouse CNS neurons. J. Neurosci. 20, 6898-6906
76. Cantres-Rosario, Y., Plaud-Valentín, M., Gerena, Y., Skolasky, R. L., Wojna, V., and Meléndez, L. M. (2013) Cathepsin B and cystatin B in HIVseropositive women are associated with infection and HIV-1-associated neurocognitive disorders. AIDS 27, 347-356
77. Rivera, L. E., Colon, K., Cantres-Rosario, Y. M., Zenon, F. M., and Melendez, L. M. (2014) Macrophage derived cystatin B/cathepsin B in HIV replication and neuropathogenesis. Curr. HIVRes. 12, 111-120
78. McCall, M. A., and Gregg., R. G., Behringer, R. R., Brenner, M., Delaney, C. L., Galbreath, E. J., Zhang, C. L., Pearce, R. A., Chiu, S. Y., and Messing, A. (1996) Targeted deletion in astrocyte intermediate filament (Gfap) alters neuronal physiology. Proc. Natl. Acad. Sci. U.S.A. 93, 6361-6366
79. Zou, W., and Kim., B. O., Zhou, B. Y., Liu, Y., Messing, A., and He, J. J. (2007) Protection against human immunodeficiency virus type 1 Tat neurotoxicity by Ginkgo biloba extract EGb 761 involving glial fibrillary acidic protein. Am. J. Pathol 171, 1923-1935
80. Liu, Z., Zhao, F., and He, J. J. (2014) Hepatitis C virus (HCV) interaction with astrocytes: nonproductive infection and induction of IL-18. J. Neurovirol. 20, 278-293
81. Liu, Y., Li, J., Kim, B. O., Pace, B. S., and He, J. J. (2002) HIV-1 Tat proteinmediated transactivation of the HIV-1 long terminal repeat promoter is potentiated by a novel nuclear Tat-interacting protein of 110 kDa, Tip110. J. Biol. Chem. 277, 23854-23863
82. Klaver, B., and Berkhout, B. (1994) Comparison of 5' and 3' long terminal repeat promoter function in human immunodeficiency virus. J. Virol. 68, 3830-3840
83. Jeeninga, R. E., Hoogenkamp, M., Armand-Ugon, M., de Baar, M., Verhoef, K., and Berkhout, B. (2000) Functional differences between the long terminal repeat transcriptional promoters of human immunodeficiency virus type 1 subtypes A through G. J. Virol. 74, 3740-3751
84. Fan, Y., and He, J. J. (2016) HIV-1 Tat induces unfolded protein response and endoplasmic reticulum stress in astrocytes and causes neurotoxicity through glial fibrillary acidic protein (GFAP) activation and aggregation. J. Biol. Chem. 291, 22819-22829