Neuronal toxicity in HIV CNS disease

Future Virology

Volumn 7, Issue 7, 2012, Pages 687-698

  Kovalevich, Jane ^a   Langford, Dianne ^a  

^a TEMPLE UNIVERSITY   (United States)

Author keywords

blood brain barrier; cART; CNS; excitotoxicity; HIV associated neurocognitive disorders; inflammation; neurons; synaptodendritic

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CALBINDIN; CHEMOKINE RECEPTOR CXCR4; FIBROBLAST GROWTH FACTOR RECEPTOR; GLYCOPROTEIN GP 120; INTERLEUKIN 1BETA; INTERLEUKIN 6; METHAMPHETAMINE; MORPHINE; NERVE GROWTH FACTOR; PARVALBUMIN; PLATELET DERIVED GROWTH FACTOR; TRANSACTIVATOR PROTEIN; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; VIRUS DNA;

GLIA CELL; HIV ASSOCIATED DEMENTIA; HOST CELL; HUMAN; IMMUNOHISTOCHEMISTRY; NERVE CELL; NEUROTOXICITY; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SUBSTANCE ABUSE; VIRUS CELL INTERACTION; VIRUS REPLICATION;

EID: 84864486828     PISSN: 17460794     EISSN: 17460808     Source Type: Journal    
DOI: 10.2217/fvl.12.57     Document Type: Review

References (128)

1. Stevenson M. HIV-1 pathogenesis. Nat. Med. 9(7), 853-860 (2003).
2. Gorry PR, Ancuta P. Coreceptors and HIV-1 pathogenesis. Curr. HIV/AIDS Rep. 8(1), 45-53 (2011).
3. Fauci AS. Host factors and the pathogenesis of HIV-induced disease. Nature 384(6609), 529-534 (1996).
4. Lavi E, Kolson DL, Ulrich AM, Fu L, Gonzalez-Scarano F. Chemokine receptors in the human brain and their relationship to HIV infection. J. Neurovirol. 4(3), 301-311 (1998).
5. Strazza M, Pirrone V, Wigdahl B, Nonnemacher MR. Breaking down the barrier: The effects of HIV-1 on the blood-brain barrier. Brain Res. 1399, 96-115 (2011).
6. Resnick L, Berger JR, Shapshak P, Tourtellotte WW. Early penetration of the blood-brain-barrier by HIV. Neurology 38(1), 9-14 (1988).
7. Wiley CA, Schrier RD, Nelson JA, Lampert PW, Oldstone MB. Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients. Proc. Natl Acad. Sci. USA 83(18), 7089-7093 (1986).
8. Funke I, Hahn A, Rieber EP, Weiss E, Riethmuller G. The cellular receptor (CD4) of the human immunodeficiency virus is expressed on neurons and glial cells in human brain. J. Exp. Med. 165(4), 1230-1235 (1987).
9. Lavi E, Strizki JM, Ulrich AM et al. CXCR-4 (Fusin), a co-receptor for the type 1 human immunodeficiency virus (HIV-1), is expressed in the human brain in a variety of cell types, including microglia and neurons. Am. J. Pathol. 151(4), 1035-1042 (1997).
10. Peudenier S, Hery C, Ng KH, Tardieu M. HIV receptors within the brain: A study of CD4 and MHC-II on human neurons, astrocytes and microglial cells. Res. Virol. 142(2-3), 145-149 (1991).
11. Bagasra O, Lavi E, Bobroski L et al. Cellular reservoirs of HIV-1 in the central nervous system of infected individuals: Identification by the combination of in situ polymerase chain reaction and immunohistochemistry. AIDS (London, England) 10(6), 573-585 (1996).
12. Nuovo Gj, Gallery F, Macconnell P, Braun A. In situ detection of polymerase chain reaction-amplified HIV-1 nucleic acids and tumor necrosis factor-alpha RNA in the central nervous system. Am. J. Pathol. 144(4), 659-666 (1994).
13. Torres-Munoz J, Stockton P, Tacoronte N, Roberts B, Maronpot RR, Petito CK. Detection of HIV-1 gene sequences in hippocampal neurons isolated from postmortem AIDS brains by laser capture microdissection. J. Neuropathol. Exp. Neurol. 60(9), 885-892 (2001).
14. Trillo-Pazos G, Diamanturos A, Rislove L et al. Detection of HIV-1 DNA in microglia/ macrophages, astrocytes and neurons isolated from brain tissue with HIV-1 encephalitis by laser capture microdissection. Brain Pathol. (Zurich, Switzerland) 13(2), 144-154 (2003).
15. Torres-Munoz JE, Nunez M, Petito CK. Successful application of hyperbranched multidisplacement genomic amplification to detect HIV-1 sequences in single neurons removed from autopsy brain sections by laser capture microdissection. J. Mol. Diagn. 10(4), 317-324 (2008).
16. Mukhtar M, Acheampong E, Khan MA, Bouhamdan M, Pomerantz RJ. Down-modulation of the CXCR4 co-receptor by intracellular expression of a single chain variable fragment (SFv) inhibits HIV-1 entry into primary human brain microvascular endothelial cells and post-mitotic neurons. Brain Res. Mol. Brain Res. 135(1-2), 48-57 (2005).
17. Alvarez-Losada S, Canto-Nogues C, Munoz-Fernandez MA. A new possible mechanism of human immunodeficiency virus type 1 infection of neural cells. Neurobiol. Dis. 11(3), 469-478 (2002).
18. Kure K, Llena JF, Lyman WD et al. Human immunodeficiency virus-1 infection of the nervous system: An autopsy study of 268 adult, pediatric, and fetal brains. Hum. Pathol. 22(7), 700-710 (1991).
19. Lyman WD, Kress Y, Kure K, Rashbaum WK, Rubinstein A, Soeiro R. Detection of HIV in fetal central nervous system tissue. AIDS (London, England) 4(9), 917-920 (1990).
20. Canto-Nogues C, Sanchez-Ramon S, Alvarez S, Lacruz C, Munoz-Fernandez MA. HIV-1 infection of neurons might account for progressive HIV-1-associated encephalopathy in children. J. Mol. Neurosci. 27(1), 79-89 (2005).
21. Vallat AV, De Girolami U, He J et al. Localization of HIV-1 co-receptors CCR5 and CXCR4 in the brain of children with AIDS. Am. J. Pathol. 152(1), 167-178 (1998).
22. Sharer LR, Saito Y, Da Cunha A et al. In situ amplification and detection of HIV-1 DNA in fixed pediatric AIDS brain tissue. Hum. Pathol. 27(6), 614-617 (1996).
23. Sharer LR, Saito Y, Epstein LG, Blumberg BM. Detection of HIV-1 DNA in pediatric AIDS brain tissue by two-step ISPCR. Adv. Neuroimmunol. 4(3), 283-285 (1994).
24. Schwartz L, Civitello L, Dunn-Pirio A et al. Evidence of human immunodeficiency virus type 1 infection of nestin-positive neural progenitors in archival pediatric brain tissue. J. Neurovirol. 13(3), 274-283 (2007).
25. Ensoli F, Cafaro A, Fiorelli V, Vannelli B, Ensoli B, Thiele CJ. HIV-1 infection of primary human neuroblasts. Virology 210(1), 221-225 (1995).
26. Lawrence DM, Durham LC, Schwartz L, Seth P, Maric D, Major EO. Human immunodeficiency virus type 1 infection of human brain-derived progenitor cells. J. Virol. 78(14), 7319-7328 (2004).
27. Bell JE. The neuropathology of adult HIV infection. Rev. Neurol. 154(12), 816-829 (1998).
28. Kaul M, Lipton SA. Mechanisms of neuronal injury and death in HIV-1 associated dementia. Curr. HIV Res. 4(3), 307-318 (2006).
29. Nath A. Human immunodeficiency virus (HIV) proteins in neuropathogenesis of HIV dementia. J. Infect. Dis. 186, s193-s198 (2002).
30. Ellis R, Langford D, Masliah E. HIV and antiretroviral therapy in the brain: Neuronal injury and repair. Nat. Rev. 8(1), 33-44 (2007).
31. Barnes DM. Solo actions of AIDS virus coat. Science 237(4818), 971-973 (1987).
32. Louboutin JP, Agrawal L, Reyes BA, Van Bockstaele EJ, Strayer DS. Gene delivery of antioxidant enzymes inhibits HIV-1 gp120-induced expression of caspases. Neuroscience doi:10.1016/j. neuroscience.2012.03.061 (2012) (Epub ahead of print).
33. Zhang Y, Shi Y, Qiao L et al. Sigma-1 receptor agonists provide neuroprotection against gp120 via a change in bcl-2 expression in mouse neuronal cultures. Brain Res. 1431, 13-22 (2012).
34. Sabatier JM, Vives E, Mabrouk K et al. Evidence for neurotoxic activity of tat from human immunodeficiency virus type 1. J. Virol. 65(2), 961-967 (1991).
35. Li W, Li G, Steiner J, Nath A. Role of Tat protein in HIV neuropathogenesis. Neurotoxicity Res. 16(3), 205-220 (2009).
36. Magnuson DS, Knudsen BE, Geiger JD, Brownstone RM, 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), 373-380 (1995).
37. Norman JP, Perry SW, Reynolds HM et al. HIV-1 Tat activates neuronal ryanodine receptors with rapid induction of the unfolded protein response and mitochondrial hyperpolarization. PLoS One 3(11), e3731 (2008).
38. Hui L, Chen X, Bhatt D et al. Ketone bodies protection against HIV-1 Tat-induced neurotoxicity. J. Neurochem. doi:10.1111/j.1471-4159.2012.07764 (2012) (Epub ahead of print).
39. Chang JR, Mukerjee R, Bagashev A et al. HIV-1 Tat protein promotes neuronal dysfunction through disruption of microRNAs. J. Biol. Chem. 286(47), 41125-41134 (2011).
40. Maragos WF, Tillman P, Jones M et al. Neuronal injury in hippocampus with human immunodeficiency virus transactivating protein, Tat. Neuroscience 117(1), 43-53 (2003).
41. Alirezaei M, Watry DD, Flynn CF et al. Human immunodeficiency virus-1/surface glycoprotein 120 induces apoptosis through RNA-activated protein kinase signaling in neurons. J. Neurosci. 27(41), 11047-11055 (2007).
42. Li W, Galey D, Mattson MP, Nath A. Molecular and cellular mechanisms of neuronal cell death in HIV dementia. Neurotoxicity Res. 8(1-2), 119-134 (2005).
43. Lu SM, Tremblay ME, King IL et al. HIV-1 Tat-induced microgliosis and synaptic damage via interactions between peripheral and central myeloid cells. PLoS One 6(9), e23915 (2011).
44. Singh KK, Nathamu S, Adame A et al. Expression of mannose binding lectin in HIV-1-infected brain: Implications for HIV-related neuronal damage and neuroAIDS. Neurobehav. HIV Med. 3, 41-52 (2011).
45. Mothobi NZ, Brew BJ. Neurocognitive dysfunction in the highly active antiretroviral therapy era. Curr. Opin. Infect. Dis. 25(1), 4-9 (2012).
46. Langford D, Marquie-Beck J, De Almeida S et al. Relationship of antiretroviral treatment to postmortem brain tissue viral load in human immunodeficiency virus-infected patients. J. Neurovirol. 12(2), 100-107 (2006).
47. Letendre S. Central nervous system complications in HIV disease: hiv-associated neurocognitive disorder. Top. Antiviral Med. 19(4), 137-142 (2011).
48. Everall IP, Hansen LA, Masliah E. The shifting patterns of HIV encephalitis neuropathology. Neurotoxicity Res. 8(1-2), 51-61 (2005).
49. Petito CK, Roberts B. Evidence of apoptotic cell death in HIV encephalitis. Am. J. Pathol. 146(5), 1121-1130 (1995).
50. Masliah E, Ge N, Achim CL, Wiley CA. Cytokine receptor alterations during HIV infection in the human central nervous system. Brain Res. 663(1), 1-6 (1994).
51. Masliah E, Ge N, Achim CL, Hansen LA, Wiley CA. Selective neuronal vulnerability in HIV encephalitis. J. Neuropathol. Exp. Neurol. 51(6), 585-593 (1992).
52. Crews L, Patrick C, Achim CL, Everall IP, Masliah E. Molecular pathology of neuro-AIDS (CNS-HIV). Int. J. Mol. Sci. 10(3), 1045-1063 (2009).
53. Ahmed F, Tessarollo L, Thiele C, Mocchetti I. Brain-derived neurotrophic factor modulates expression of chemokine receptors in the brain. Brain Res. 1227, 1-11 (2008).
54. Sanders VJ, Everall IP, Johnson RW, Masliah E. Fibroblast growth factor modulates HIV coreceptor CXCR4 expression by neural cells. HNRC Group. J. Neurosci. Res. 59(5), 671-679 (2000).
55. Masliah E, Ge N, Mucke L. Pathogenesis of HIV-1 associated neurodegeneration. Crit. Rev. Neurobiol. 10(1), 57-67 (1996).
56. Masliah E, Ge N, Achim CL, Deteresa R, Wiley CA. Patterns of neurodegeneration in HIV encephalitis. J. NeuroAIDS 1(1), 161-173 (1996).
57. Mucke L, Masliah E, Campbell IL. Transgenic models to assess the neuropathogenic potential of HIV-1 proteins and cytokines. Curr. Top. Microbiol. Immunol. 202, 187-205 (1995).
58. Zauli G, Secchiero P, Rodella L et al. HIV-1 Tat-mediated inhibition of the tyrosine hydroxylase gene expression in dopaminergic neuronal cells. J. Biol. Chem. 275(6), 4159-4165 (2000).
59. Nath A, Anderson C, Jones M et al. Neurotoxicity and dysfunction of dopaminergic systems associated with AIDS dementia. J. Psychopharmacol. (Oxford, England) 14(3), 222-227 (2000).
60. Lopez OL, Smith G, Meltzer CC, Becker JT. Dopamine systems in human immunodeficiency virus-associated dementia. Neuropsych. Neuropsychol. Behav. Neurol. 12(3), 184-192 (1999).
61. Ramirez SH, Sanchez JF, Dimitri CA, Gelbard HA, Dewhurst S, Maggirwar SB. Neurotrophins prevent HIV Tat-induced neuronal apoptosis via a nuclear factor-kappaB (NF-kappaB)-dependent mechanism. J. Neurochem. 78(4), 874-889 (2001).
62. Fox L, Alford M, Achim C, Mallory M, Masliah E. Neurodegeneration of somatostatin-immunoreactive neurons in HIV encephalitis. J. Neuropathol. Exp. Neurol. 56(4), 360-368 (1997).
63. Toggas SM, Masliah E, Rockenstein EM, Rall GF, Abraham CR, Mucke L. Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 367(6459), 188-193 (1994).
64. Campbell IL, Abraham CR, Masliah E et al. Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. Proc. Natl Acad. Sci. USA 90(21), 10061-10065 (1993).
65. Campbell IL, Stalder AK, Chiang CS et al. Transgenic models to assess the pathogenic actions of cytokines in the central nervous system. Mol. Psychiatr. 2(2), 125-129 (1997).
66. Budka H, Costanzi G, Cristina S et al. Brain pathology induced by infection with the human immunodeficiency virus (HIV). A histological, immunocytochemical, and electron microscopical study of 100 autopsy cases. Acta Neuropathologica 75(2), 185-198 (1987).
67. Everall IP, Luthert PJ, Lantos PL. Neuronal loss in the frontal cortex in HIV infection. Lancet 337(8750), 1119-1121 (1991).
68. Wiley CA, Masliah E, Morey M et al. Neocortical damage during HIV infection. Ann. Neurol. 29(6), 651-657 (1991).
69. Langford TD, Everall. IP, Maslaih E. Neuronal injury, white matter disease and neurotrophic factors. In: THE Neurology of AIDS, 3rd Edition. Gendelman HE, Everall IP, Grant I et al. (Eds). Oxford University Press, UK, 619-632 (2012).
70. Gray F, Adle-Biassette H, Chretien F, Lorin De La Grandmaison G, Force G, Keohane C. Neuropathology and neurodegeneration in human immunodeficiency virus infection. Pathogenesis of HIV-induced lesions of the brain, correlations with HIV-associated disorders and modifications according to treatments. Clin. Neuropathol. 20(4), 146-155 (2001).
71. Gray F, Haug H, Chimelli L et al. Prominent cortical atrophy with neuronal loss as correlate of human immunodeficiency virus encephalopathy. Acta Neuropathologica 82(3), 229-233 (1991).
72. Everall IP, Heaton RK, Marcotte TD et al. Cortical synaptic density is reduced in mild to moderate human immunodeficiency virus neurocognitive disorder. HNRC Group. HIV Neurobehavioral Research Center. Brain Pathol. (Zurich, Switzerland) 9(2), 209-217 (1999).
73. Masliah E, Heaton RK, Marcotte TD et al. Dendritic injury is a pathological substrate for human immunodeficiency virus-related cognitive disorders. HNRC Group. The HIV Neurobehavioral Research Center. Ann. Neurol. 42(6), 963-972 (1997).
74. Everall IP, Gray F, Masliah E. Neuronal injury and apoptosis. In: NEUROLOGY of AIDS. Gendelman H, Lipton S, Epstein L, Swindells S (Eds). Chapman and Hall, NY, USA, 261-274 (1988).
75. Wiley CA, Achim CL, Hammond R et al. Damage and repair of DNA in HIV encephalitis. J. Neuropathol. Exp. Neurol. 59(11), 955-965 (2000).
76. Adle-Biassette H, Chretien F, Wingertsmann L et al. Neuronal apoptosis does not correlate with dementia in HIV infection but is related to microglial activation and axonal damage. Neuropathol. Appl. Neurobiol. 25(2), 123-133 (1999).
77. Noorbakhsh F, Ramachandran R, Barsby N et al. MicroRNA profiling reveals new aspects of HIV neurodegeneration: Caspase-6 regulates astrocyte survival. FASEB J. 24(6), 1799-1812 (2010).
78. Encinas M, Iglesias M, Liu Y et al. Sequential treatment of SH-SY5Y cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factor-dependent, human neuron-like cells. J. Neurochem. 75(3), 991-1003 (2000).
79. Asensio VC, Campbell IL. Chemokines and viral diseases of the central nervous system. Adv. Virus Res. 56, 127-173 (2001).
80. Langford D, Masliah E. Role of trophic factors on neuroimmunity in neurodegenerative infectious diseases. J. Neurovirol. 8(6), 625-638 (2002).
81. Spehar T, Strand M. Molecular mimicry between HIV-1 gp41 and an astrocyte isoform of alpha-actinin. J. Neurovirol. 1(5-6), 381-390 (1995).
82. Scheidegger P, Weiglhofer W, Suarez S et al. Signalling properties of an HIV-encoded angiogenic peptide mimicking vascular endothelial growth factor activity. Biochem. J. 353(Pt 3), 569-578 (2001).
83. Nyagol J, De Falco G, Lazzi S et al. HIV-1 Tat mimetic of VEGF correlates with increased microvessels density in AIDS-related diffuse large B-cell and Burkitt lymphomas. J. Hematopathol. 1(1), 3-10 (2008).
84. Murphy PM. Viral exploitation and subversion of the immune system through chemokine mimicry. Nat. Immunol. 2(2), 116-122 (2001).
85. Alcami A, Koszinowski UH. Viral mechanisms of immune evasion. Mol. Med. Today 6(9), 365-372 (2000).
86. Lalani AS, Mcfadden G. Evasion and exploitation of chemokines by viruses. Cytokine Growth Factor Rev. 10(3-4), 219-233 (1999).
87. Barnea A, Roberts J, Ho RH. Evidence for a synergistic effect of the HIV-1 envelope protein gp120 and brain-derived neurotrophic factor (BDNF) leading to enhanced expression of somatostatin neurons in aggregate cultures derived from the human fetal cortex. Brain Res. 815(2), 349-357 (1999).
88. Corasaniti MT, Bagetta G, Rotiroti D, Nistico G. The HIV envelope protein gp120 in the nervous system: Interactions with nitric oxide, interleukin-1beta and nerve growth factor signalling, with pathological implications in vivo and in vitro. Biochem. Pharmacol. 56(2), 153-156 (1998).
89. Bagetta G, Corasaniti MT, Aloe L et al. Intracerebral injection of human immunodeficiency virus type 1 coat protein gp120 differentially affects the expression of nerve growth factor and nitric oxide synthase in the hippocampus of rat. Proc. Natl Acad. Sci. USA 93(2), 928-933 (1996).
90. Peruzzi F, Gordon J, Darbinian N, Amini S. Tat-induced deregulation of neuronal differentiation and survival by nerve growth factor pathway. J. Neurovirol. 8(Suppl. 2), 91-96 (2002).
91. Boven LA, Middel J, Portegies P, Verhoef J, Jansen GH, Nottet HS. Overexpression of nerve growth factor and basic fibroblast growth factor in AIDS dementia complex. J. Neuroimmunol. 97(1-2), 154-162 (1999).
92. Albrecht D, Garcia L, Cartier L et al. Trophic factors in cerebrospinal fluid and spinal cord of patients with tropical spastic paraparesis, HIV, and Creutzfeldt-Jakob disease. AIDS Res. Hum. Retroviruses 22(3), 248-254 (2006).
93. Saarelainen T, Vaittinen S, Castren E. trkB-receptor activation contributes to the kainate-induced increase in BDNF mRNA synthesis. Cell. Mol. Neurobiol. 21(4), 429-435 (2001).
94. Zhu X, Yao H, Peng F, Callen S, Buch S. PDGF-mediated protection of SH-SY5Y cells against Tat toxin involves regulation of extracellular glutamate and intracellular calcium. Toxicol. Appl. Pharmacol. 240(2), 286-291 (2009).
95. Peng F, Dhillon NK, Yao H, Zhu X, Williams R, Buch S. Mechanisms of platelet-derived growth factor-mediated neuroprotection - implications in HIV dementia. Eur. J. Neurosci. 28(7), 1255-1264 (2008).
96. Peng F, Dhillon N, Callen S et al. Platelet-derived growth factor protects neurons against gp120-mediated toxicity. J. Neurovirol. 14(1), 62-72 (2008).
97. Yao H, Peng F, Fan Y, Zhu X, Hu G, Buch SJ. TRPC channel-mediated neuroprotection by PDGF involves Pyk2/ERK/CREB pathway. Cell Death Differ. 16(12), 1681-1693 (2009).
98. Sacktor N, Nakasujja N, Skolasky RL et al. HIV subtype D is associated with dementia, compared with subtype A, in immunosuppressed individuals at risk of cognitive impairment in Kampala, Uganda. Clin. Infect. Dis. 49(5), 780-786 (2009).
99. Satishchandra P, Nalini A, Gourie-Devi M et al. Profile of neurologic disorders associated with HIV/AIDS from Bangalore, south India (1989-1996). Indian J. Med. Res. 111, 14-23 (2000).
100. Shankar SK, Mahadevan A, Satishchandra P et al. Neuropathology of HIV/AIDS with an overview of the Indian scene. Indian J. Med. Res. 121(4), 468-488 (2005).
101. Yepthomi T, Paul R, Vallabhaneni S et al. Neurocognitive consequences of HIV in southern India: A preliminary study of clade C virus. J. Int. Neuropsychol. Soc. 12(3), 424-430 (2006).
102. Clifford DB, Mitike MT, Mekonnen Y et al. Neurological evaluation of untreated human immunodeficiency virus infected adults in Ethiopia. J. Neurovirol. 13(1), 67-72 (2007).
103. Gupta JD, Satishchandra P, Gopukumar K et al. Neuropsychological deficits in human immunodeficiency virus type 1 clade C-seropositive adults from south India. J. Neurovirol. 13(3), 195-202 (2007).
104. Riedel D, Ghate M, Nene M et al. Screening for human immunodeficiency virus (HIV) dementia in an HIV clade C-infected population in India. J. Neurovirol. 12(1), 34-38 (2006).
105. Mishra M, Vetrivel S, Siddappa NB, Ranga U, Seth P. Clade-specific differences in neurotoxicity of human immunodeficiency virus-1 B and C Tat of human neurons: Significance of dicysteine C30C31 motif. Ann. Neurol. 63(3), 366-376 (2008).
106. Campbell GR, Watkins JD, Loret EP, Spector SA. Differential induction of rat neuronal excitotoxic cell death by human immunodeficiency virus type 1 clade B and C tat proteins. AIDS Res. Hum. Retroviruses 27(6), 647-654 (2011).
107. Nath A, Hauser KF, Wojna V et al. Molecular basis for interactions of HIV and drugs of abuse. J. Acquired Immune Deficiency Syndr. 31(Suppl. 2), S62-S69 (2002).
108. Ferris MJ, Mactutus CF, Booze RM. Neurotoxic profiles of HIV, psychostimulant drugs of abuse, and their concerted effect on the brain: Current status of dopamine system vulnerability in NeuroAIDS. Neurosci. Biobehav. Rev. 32(5), 883-909 (2008).
109. Langford D, Adame A, Grigorian A et al. Patterns of selective neuronal damage in methamphetamine-user AIDS patients. J. Acquir. Immune Defic. Syndr. 34(5), 467-474 (2003).
110. Chana G, Everall IP, Crews L et al. Cognitive deficits and degeneration of interneurons in HIV+ methamphetamine users. Neurology 67(8), 1486-1489 (2006).
111. Turchan J, Anderson C, Hauser KF et al. Estrogen protects against the synergistic toxicity by HIV proteins, methamphetamine and cocaine. BMC Neurosci. 2, 3 (2001).
112. Cass WA, Harned ME, Peters LE, Nath A, Maragos WF. HIV-1 protein Tat potentiation of methamphetamine-induced decreases in evoked overflow of dopamine in the striatum of the rat. Brain Res. 984(1-2), 133-142 (2003).
113. Maragos WF, Young KL, Turchan JT et al. Human immunodeficiency virus-1 Tat protein and methamphetamine interact synergistically to impair striatal dopaminergic function. J. Neurochem. 83(4), 955-963 (2002).
114. Conant K, St Hillaire C, Anderson C, Galey D, Wang J, Nath A. Human immunodeficiency virus type 1 Tat and methamphetamine affect the release and activation of matrix-degrading proteinases. J. Neurovirol. 10(1), 21-28 (2004).
115. Langford D, Grigorian A, Hurford R, Adame A, Crews L, 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), 327-337 (2004).
116. Theodore S, Cass WA, Nath A, Steiner J, Young K, Maragos WF. Inhibition of tumor necrosis factor-alpha signaling prevents human immunodeficiency virus-1 protein Tat and methamphetamine interaction. Neurobiol. Dis. 23(3), 663-668 (2006).
117. Qi L, Gang L, Hang KW et al. Programmed neuronal cell death induced by HIV-1 tat and methamphetamine. Microsc. Res. Tech. 74(12), 1139-1144 (2011).
118. Bandaru VV, Patel N, Ewaleifoh O, Haughey NJ. A failure to normalize biochemical and metabolic insults during morphine withdrawal disrupts synaptic repair in mice transgenic for HIV-gp120. J. Neuroimmune Pharmacol. 6(4), 640-649 (2011).
119. Fitting S, Xu R, Bull C et al. Interactive comorbidity between opioid drug abuse and HIV-1 Tat: Chronic exposure augments spine loss and sublethal dendritic pathology in striatal neurons. Am. J. Pathol. 177(3), 1397-1410 (2010).
120. Bruce-Keller AJ, Turchan-Cholewo J, Smart EJ et al. Morphine causes rapid increases in glial activation and neuronal injury in the striatum of inducible HIV-1 Tat transgenic mice. Glia 56(13), 1414-1427 (2008).
121. Hu S, Sheng WS, Lokensgard JR, Peterson PK. Morphine potentiates HIV-1 gp120-induced neuronal apoptosis. J. Infect. Dis. 191(6), 886-889 (2005).
122. Suzuki M, El-Hage N, Zou S et al. Fractalkine/ CX3CL1 protects striatal neurons from synergistic morphine and HIV-1 Tat-induced dendritic losses and death. Mol. Neurodegen. 6, 78 (2011).
123. Hauser KF, El-Hage N, Buch S et al. Impact of opiate-HIV-1 interactions on neurotoxic signaling. J. Neuroimmune Pharmacol. 1(1), 98-105 (2006).
124. Zou S, Fitting S, Hahn YK et al. Morphine potentiates neurodegenerative effects of HIV-1 Tat through actions at mu-opioid receptor-expressing glia. Brain 134(Pt 12), 3616-3631 (2011).
125. Avdoshina V, Biggio F, Palchik G, Campbell LA, Mocchetti I. Morphine induces the release of CCL5 from astrocytes: Potential neuroprotective mechanism against the HIV protein gp120. Glia 58(13), 1630-1639 (2010).
126. Podhaizer EM, Zou S, Fitting S et al. Morphine and gp120 toxic interactions in striatal neurons are dependent on HIV-1 strain. J. Neuroimmune Pharmacol. doi:10.1007/s11481-011-9326-z (2011) (Epub ahead of print).
127. Tan IL, McArthur JC. HIV-associated neurological disorders: A guide to pharmacotherapy. CNS Drugs 26(2), 123-134 (2012).
128. Gelman BB, Nguyen TP. Synaptic proteins linked to HIV-1 infection and immunoproteasome induction: Proteomic analysis of human synaptosomes. J. Neuroimmune Pharmacol. 5, 92-102 (2010).