Methamphetamine abuse, HIV infection, and neurotoxicity

International Journal of Physiology, Pathophysiology and Pharmacology

Volumn 1, Issue 2, 2009, Pages 162-179

  Reiner, Benjamin C ^a   Keblesh, James P ^a   Xiong, Huangui ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

AIDS; HIV 1; Methamphetamine; Neurodegeneration; Neurotoxicity

Indexed keywords

ACETYLCYSTEINE; ALCOHOL; ALPHA TOCOPHEROL; ANTIRETROVIRUS AGENT; ASCORBIC ACID; GLUTAMATE RECEPTOR ANTAGONIST; GLYCOPROTEIN GP 120; MANNITOL; METHAMPHETAMINE; NEF PROTEIN; NITRIC OXIDE SYNTHASE INHIBITOR; PHENYLALANINE; PROTEIN BCL 2; SALICYLIC ACID; SELENIUM; TRANSACTIVATOR PROTEIN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA INHIBITOR; VPR PROTEIN;

APOPTOSIS; BRAIN; BRAIN INFECTION; CELL DEATH; COMORBIDITY; COMPUTER ASSISTED TOMOGRAPHY; DISEASE COURSE; DRUG ABUSE; DRUG DEPENDENCE; DRUG MECHANISM; ENDOPLASMIC RETICULUM; GENE ACTIVATION; GLIA CELL; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MICROGLIA; MITOCHONDRION; NERVE CELL LESION; NERVE DEGENERATION; NEUROIMAGING; NEUROTOXICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OXIDATIVE STRESS; PATHOGENESIS; POSITRON EMISSION TOMOGRAPHY; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; RISK FACTOR; SERODIAGNOSIS; SIGNAL TRANSDUCTION; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SYNAPTIC POTENTIAL;

EID: 77953367759     PISSN: None     EISSN: 19448171     Source Type: Journal    
DOI: None     Document Type: Review

References (219)

1. Purcell DW, Moss S, Remien RH, Woods WJ and Parsons JT. Illicit substance use, sexual risk, and HIV-positive gay and bisexual men: differences by serostatus of casual partners. Aids 2005; 19 Suppl 1: S37-47.
2. Romanelli F and Smith KM. Clinical effects and management of methamphetamine abuse. Pharmacotherapy 2006; 26: 1148-1156.
3. Andrew E. Springer RJP, Ross Shegog, Donna L. White, and Steven H. Kelder. Methamphetamine Use and Sexual Risk Behaviors in U.S. High School Students: Findings from a National Risk Behavior Survey. Prevention Science 2007; 8: 103-113.
4. O'Dea PJ, Murphy B and Balzer C. Traffic and illegal production of drugs in rural America. NIDA Res Monogr 1997; 168: 79-89.
5. Woolverton WL, Cervo L and Johanson CE. Effects of repeated methamphetamine administration on methamphetamine self-administration in rhesus monkeys. Pharmacol Biochem Behav 1984; 21: 737-741.
6. Cadet JL and Krasnova IN. Interactions of HIV and Methamphetamine: Cellular and Molecular Mechanisms of Toxicity Potentiation. Neurotoxicity Research 2007; 12: 181-204.
7. Schepers RJ, Oyler JM, Joseph RE, Jr., Cone EJ, Moolchan ET and Huestis MA. Methamphetamine and amphetamine pharmacokinetics in oral fluid and plasma after controlled oral methamphetamine administration to human volunteers. Clin Chem 2003; 49: 121-132.
8. Glittenberg J and Anderson C. Methamphetamines: use and trafficking in the Tucson-Nogales area. Subst Use Misuse 1999; 34: 1977-1989.
9. Ricaurte GA, Guillery RW, Seiden LS, Schuster CR and Moore RY. Dopamine nerve terminal degeneration produced by high doses of methylamphetamine in the rat brain. Brain Res 1982; 235: 93-103.
10. Davidson C, Gow AJ, Lee TH and Ellinwood EH. Methamphetamine neurotoxicity: necrotic and apoptotic mechanisms and relevance to human abuse and treatment. Brain Res Brain Res Rev 2001; 36: 1-22.
11. Halkitis PN, Parsons JT and Stirratt MJ. A double epidemic: crystal methamphetamine drug use in relation to HIV transmission among gay men. J Homosex 2001; 41: 17-35.
12. Mitchell SJ, Morris SR, Kent CK, Stansell J and Klausner JD. Methamphetamine use and sexual activity among HIV-infected patients in care - San Francisco, 2004. AIDS Patient Care STDS 2006; 20: 502-510.
13. Semple SJ, Patterson TL and Grant I. Motivations associated with methamphetamine use among HIV+ men who have sex with men. J Subst Abuse Treat 2002; 22: 149-156.
14. Thiede H, Valleroy LA, MacKellar DA, Celentano DD, Ford WL, Hagan H, Koblin BA, LaLota M, McFarland W, Shehan DA and Torian LV. Regional patterns and correlates of substance use among young men who have sex with men in 7 US urban areas. Am J Public Health 2003; 93: 1915-1921.
15. Drumright LN, Little SJ, Strathdee SA, Slymen DJ, Araneta MR, Malcarne VL, Daar ES and Gorbach PM. Unprotected anal intercourse and substance use among men who have sex with men with recent HIV infection. J Acquir Immune Defic Syndr 2006; 43: 344-350.
16. Investigation of a new diagnosis of multidrug-resistant, dual-tropic HIV-1 infection - New York City, 2005. MMWR Morb Mortal Wkly Rep 2006; 55: 793-796.
17. Ellis RJ, Childers ME, Cherner M, Lazzaretto D, Letendre S and Grant I. Increased human immunodeficiency virus loads in active methamphetamine users are explained by reduced effectiveness of antiretroviral therapy. J Infect Dis 2003; 188: 1820-1826.
18. Smith DM, Wong JK, Hightower GK, Ignacio CC, Koelsch KK, Petropoulos CJ, Richman DD and Little SJ. HIV drug resistance acquired through superinfection. Aids 2005; 19: 1251-1256.
19. Rondinelli AJ, Ouellet LJ, Strathdee SA, Latka MH, Hudson SM, Hagan H and Garfein RS. Young adult injection drug users in the United States continue to practice HIV risk behaviors. Drug Alcohol Depend 2009;
20. Centers for Disease Control and Prevention. HIV/AIDS Surveillance Report, 2006. Vol. 18. Atlanta: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention; 2008: http://www.cdc.gov/hiv/topics/ surveillance/resources/reports/.
21. McArthur JC, Hoover DR, Bacellar H, Miller EN, Cohen BA, Becker JT, Graham NM, McArthur JH, Selnes OA, Jacobson LP and et al. Dementia in AIDS patients: incidence and risk factors. Multicenter AIDS Cohort Study. Neurology 1993; 43: 2245-2252.
22. Navia BA, Jordan BD and Price RW. The AIDS dementia complex: I. Clinical features. Ann Neurol 1986; 19: 517-524.
23. Power C and Johnson RT. HIV-1 associated dementia: clinical features and pathogenesis. Can J Neurol Sci 1995; 22: 92-100.
24. Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA, Cherner M, Clifford DB, Cinque P, Epstein LG, Goodkin K, Gisslen M, Grant I, Heaton RK, Joseph J, Marder K, Marra CM, McArthur JC, Nunn M, Price RW, Pulliam L, Robertson KR, Sacktor N, Valcour V and Wojna VE. Updated research nosology for HIV-associated neurocognitive disorders. Neurology 2007; 69: 1789-1799.
25. Koutsilieri E, Gotz ME, Sopper S, Sauer U, Demuth M, ter Meulen V and Riederer P. Regulation of glutathione and cell toxicity following exposure to neurotropic substances and human immunodeficiency virus-1 in vitro. J Neurovirol 1997; 3: 342-349.
26. Nath A, Maragos WF, Avison MJ, Schmitt FA and Berger JR. Acceleration of HIV dementia with methamphetamine and cocaine. J Neurovirol 2001; 7: 66-71.
27. Theodore S, Cass WA, Nath A and Maragos WF. Progress in understanding basal ganglia dysfunction as a common target for methamphetamine abuse and HIV-1 neurodegeneration. Curr HIV Res 2007; 5: 301-313.
28. Tse W, Cersosimo MG, Gracies JM, Morgello S, Olanow CW and Koller W. Movement disorders and AIDS: a review. Parkinsonism Relat Disord 2004; 10: 323-334.
29. Daberkow DP, Kesner RP and Keefe KA. Relation between methamphetamine-induced monoamine depletions in the striatum and sequential motor learning. Pharmacol Biochem Behav 2005; 81: 198-204.
30. Gonzalez R, Bechara A and Martin EM. Executive functions among individuals with methamphetamine or alcohol as drugs of choice: preliminary observations. J Clin Exp Neuropsychol 2007; 29: 155-159.
31. Sim T, Simon SL, Domier CP, Richardson K, Rawson RA and Ling W. Cognitive deficits among methamphetamine users with attention deficit hyperactivity disorder symptomatology. J Addict Dis 2002; 21: 75-89.
32. Lipton SA and Gendelman HE. Seminars in medicine of the Beth Israel Hospital, Boston. Dementia associated with the acquired immunodeficiency syndrome. N Engl J Med 1995; 332: 934-940.
33. McArthur JC, Sacktor N and Selnes O. Human immunodeficiency virus-associated dementia. Semin Neurol 1999; 19: 129-150.
34. Heaton RK, Grant I, Butters N, White DA, Kirson D, Atkinson JH, McCutchan JA, Taylor MJ, Kelly MD, Ellis RJ and et al. The HNRC 500-neuropsychology of HIV infection at different disease stages. HIV Neurobehavioral Research Center. J Int Neuropsychol Soc 1995; 1: 231-251.
35. Poutiainen E and Elovaara I. Subjective complaints of cognitive symptoms are related to psychometric findings of memory deficits in patients with HIV-1 infection. J Int Neuropsychol Soc 1996; 2: 219-225.
36. Baldewicz TT, Leserman J, Silva SG, Petitto JM, Golden RN, Perkins DO, Barroso J and Evans DL. Changes in neuropsychological functioning with progression of HIV-1 infection: results of an 8-year longitudinal investigation. AIDS Behav 2004; 8: 345-355.
37. Carey CL, Woods SP, Rippeth JD, Gonzalez R, Heaton RK and Grant I. Additive deleterious effects of methamphetamine dependence and immunosuppression on neuropsychological functioning in HIV infection. AIDS Behav 2006; 10: 185-190.
38. Rippeth JD, Heaton RK, Carey CL, Marcotte TD, Moore DJ, Gonzalez R, Wolfson T and Grant I. Methamphetamine dependence increases risk of neuropsychological impairment in HIV infected persons. J Int Neuropsychol Soc 2004; 10: 1-14.
39. Chang L, Alicata D, Ernst T and Volkow N. Structural and metabolic brain changes in the striatum associated with methamphetamine abuse. Addiction 2007; 102 Suppl 1: 16-32.
40. McCann UD, Wong DF, Yokoi F, Villemagne V, Dannals RF and Ricaurte GA. Reduced striatal dopamine transporter density in abstinent methamphetamine and methcathinone users: evidence from positron emission tomography studies with [11C]WIN-35,428. J Neurosci 1998; 18: 8417-8422.
41. Sekine Y, Iyo M, Ouchi Y, Matsunaga T, Tsukada H, Okada H, Yoshikawa E, Futatsubashi M, Takei N and Mori N. Methamphetamine-related psychiatric symptoms and reduced brain dopamine transporters studied with PET. Am J Psychiatry 2001; 158: 1206-1214.
42. Sekine Y, Minabe Y, Ouchi Y, Takei N, Iyo M, Nakamura K, Suzuki K, Tsukada H, Okada H, Yoshikawa E, Futatsubashi M and Mori N. Association of dopamine transporter loss in the orbitofrontal and dorsolateral prefrontal cortices with methamphetamine-related psychiatric symptoms. Am J Psychiatry 2003; 160: 1699-1701.
43. Volkow ND, Chang L, Wang GJ, Fowler JS, Franceschi D, Sedler M, Gatley SJ, Miller E, Hitzemann R, Ding YS and Logan J. Loss of dopamine transporters in methamphetamine abusers recovers with protracted abstinence. J Neurosci 2001; 21: 9414-9418.
44. Volkow ND, Chang L, Wang GJ, Fowler JS, Franceschi D, Sedler MJ, Gatley SJ, Hitzemann R, Ding YS, Wong C and Logan J. Higher cortical and lower subcortical metabolism in detoxified methamphetamine abusers. Am J Psychiatry 2001; 158: 383-389.
45. Volkow ND, Chang L, Wang GJ, Fowler JS, Ding YS, Sedler M, Logan J, Franceschi D, Gatley J, Hitzemann R, Gifford A, Wong C and Pappas N. Low level of brain dopamine D2 receptors in methamphetamine abusers: association with metabolism in the orbitofrontal cortex. Am J Psychiatry 2001; 158: 2015-2021.
46. Moszczynska A, Fitzmaurice P, Ang L, Kalasinsky KS, Schmunk GA, Peretti FJ, Aiken SS, Wickham DJ and Kish SJ. Why is parkinsonism not a feature of human methamphetamine users? Brain 2004; 127: 363-370.
47. Thompson PM, Hayashi KM, Simon SL, Geaga JA, Hong MS, Sui Y, Lee JY, Toga AW, Ling W and London ED. Structural abnormalities in the brains of human subjects who use methamphetamine. J Neurosci 2004; 24: 6028-6036.
48. Chang L, Cloak C, Patterson K, Grob C, Miller EN and Ernst T. Enlarged striatum in abstinent methamphetamine abusers: a possible compensatory response. Biol Psychiatry 2005; 57: 967-974.
49. Chang L, Ernst T, Speck O and Grob CS. Additive effects of HIV and chronic methamphetamine use on brain metabolite abnormalities. Am J Psychiatry 2005; 162: 361-369.
50. Ernst T, Chang L, Leonido-Yee M and Speck O. Evidence for long-term neurotoxicity associated with methamphetamine abuse: A 1H MRS study. Neurology 2000; 54: 1344-1349.
51. Nordahl TE, Salo R, Natsuaki Y, Galloway GP, Waters C, Moore CD, Kile S and Buonocore MH. Methamphetamine users in sustained abstinence: a proton magnetic resonance spectroscopy study. Arch Gen Psychiatry 2005; 62: 444-452.
52. Nordahl TE, Salo R, Possin K, Gibson DR, Flynn N, Leamon M, Galloway GP, Pfefferbaum A, Spielman DM, Adalsteinsson E and Sullivan EV. Low N-acetyl-aspartate and high choline in the anterior cingulum of recently abstinent methamphetamine-dependent subjects: a preliminary proton MRS study. Magnetic resonance spectroscopy. Psychiatry Res 2002; 116: 43-52.
53. Sekine Y, Minabe Y, Kawai M, Suzuki K, Iyo M, Isoda H, Sakahara H, Ashby CR, Jr., Takei N and Mori N. Metabolite alterations in basal ganglia associated with methamphetamine-related psychiatric symptoms. A proton MRS study. Neuropsychopharmacology 2002; 27: 453-461.
54. Fleckenstein AE, Volz TJ, Riddle EL, Gibb JW and Hanson GR. New insights into the mechanism of action of amphetamines. Annu Rev Pharmacol Toxicol 2007; 47: 681-698.
55. Lyles J and Cadet JL. Methylenedioxymethamphetamine (MDMA, Ecstasy) neurotoxicity: cellular and molecular mechanisms. Brain Res Brain Res Rev 2003; 42: 155-168.
56. O'Callaghan JP and Miller DB. Neurotoxicity profiles of substituted amphetamines in the C57BL/6J mouse. J Pharmacol Exp Ther 1994; 270: 741-751.
57. Yamamoto BK and Zhu W. The effects of methamphetamine on the production of free radicals and oxidative stress. J Pharmacol Exp Ther 1998; 287: 107-114.
58. Giovanni A, Liang LP, Hastings TG and Zigmond MJ. Estimating hydroxyl radical content in rat brain using systemic and intraventricular salicylate: impact of methamphetamine. J Neurochem 1995; 64: 1819-1825.
59. Fridovich I. Fundamental aspects of reactive oxygen species, or what's the matter with oxygen? Ann N Y Acad Sci 1999; 893: 13-18.
60. Gluck MR, Moy LY, Jayatilleke E, Hogan KA, Manzino L and Sonsalla PK. Parallel increases in lipid and protein oxidative markers in several mouse brain regions after methamphetamine treatment. J Neurochem 2001; 79: 152-160.
61. Harold C, Wallace T, Friedman R, Gudelsky G and Yamamoto B. Methamphetamine selectively alters brain glutathione. Eur J Pharmacol 2000; 400: 99-102.
62. Jayanthi S, Ladenheim B and Cadet JL. Methamphetamine-induced changes in antioxidant enzymes and lipid peroxidation in copper/zinc-superoxide dismutase transgenic mice. Ann N Y Acad Sci 1998; 844: 92-102.
63. Potashkin JA and Meredith GE. The role of oxidative stress in the dysregulation of gene expression and protein metabolism in neurodegenerative disease. Antioxid Redox Signal 2006; 8: 144-151.
64. Acikgoz O, Gonenc S, Kayatekin BM, Uysal N, Pekcetin C, Semin I and Gure A. Methamphetamine causes lipid peroxidation and an increase in superoxide dismutase activity in the rat striatum. Brain Res 1998; 813: 200-202.
65. Iwashita A, Mihara K, Yamazaki S, Matsuura S, Ishida J, Yamamoto H, Hattori K, Matsuoka N and Mutoh S. A new poly(ADP-ribose) polymerase inhibitor, FR261529 [2-(4-chlorophenyl)-5-quinoxalinecarboxamide], ameliorates methamphetamine-induced dopaminergic neurotoxicity in mice. J Pharmacol Exp Ther 2004; 310: 1114-1124.
66. De Vito MJ and Wagner GC. Methamphetamine-induced neuronal damage: a possible role for free radicals. Neuropharmacology 1989; 28: 1145-1150.
67. Fukami G, Hashimoto K, Koike K, Okamura N, Shimizu E and Iyo M. Effect of antioxidant Nacetyl-L-cysteine on behavioral changes and neurotoxicity in rats after administration of methamphetamine. Brain Res 2004; 1016: 90-95.
68. Imam SZ and Ali SF. Selenium, an antioxidant, attenuates methamphetamine-induced dopaminergic toxicity and peroxynitrite generation. Brain Res 2000; 855: 186-191.
69. Hirata H, Ladenheim B, Carlson E, Epstein C and Cadet JL. Autoradiographic evidence for methamphetamine-induced striatal dopaminergic loss in mouse brain: attenuation in CuZn-superoxide dismutase transgenic mice. Brain Res 1996; 714: 95-103.
70. Sulzer D, Sonders MS, Poulsen NW and Galli A. Mechanisms of neurotransmitter release by amphetamines: a review. Prog Neurobiol 2005; 75: 406-433.
71. Cervinski MA, Foster JD and Vaughan RA. Psychoactive substrates stimulate dopamine transporter phosphorylation and down-regulation by cocaine-sensitive and protein kinase C-dependent mechanisms. J Biol Chem 2005; 280: 40442-40449.
72. Fumagalli F, Gainetdinov RR, Valenzano KJ and Caron MG. Role of dopamine transporter in methamphetamine-induced neurotoxicity: evidence from mice lacking the transporter. J Neurosci 1998; 18: 4861-4869.
73. Cadet JL and Brannock C. Free radicals and the pathobiology of brain dopamine systems. Neurochem Int 1998; 32: 117-131.
74. Hogan KA, Staal RG and Sonsalla PK. Analysis of VMAT2 binding after methamphetamine or MPTP treatment: disparity between homogenates and vesicle preparations. J Neurochem 2000; 74: 2217-2220.
75. Brown JM, Hanson GR and Fleckenstein AE. Methamphetamine rapidly decreases vesicular dopamine uptake. J Neurochem 2000; 74: 2221-2223.
76. LaVoie MJ and Hastings TG. Peroxynitrite- and nitrite-induced oxidation of dopamine: implications for nitric oxide in dopaminergic cell loss. J Neurochem 1999; 73: 2546-2554.
77. LaVoie MJ and Hastings TG. Dopamine quinone formation and protein modification associated with the striatal neurotoxicity of methamphetamine: evidence against a role for extracellular dopamine. J Neurosci 1999; 19: 1484-1491.
78. Hastings TG, Lewis DA and Zigmond MJ. Role of oxidation in the neurotoxic effects of intrastriatal dopamine injections. Proc Natl Acad Sci U S A 1996; 93: 1956-1961.
79. Zucker M, Weizman A and Rehavi M. Repeated swim stress leads to down-regulation of vesicular monoamine transporter 2 in rat brain nucleus accumbens and striatum. Eur Neuropsychopharmacol 2005; 15: 199-201.
80. Cadet JL, Jayanthi S, McCoy MT, Vawter M and Ladenheim B. Temporal profiling of methamphetamine-induced changes in gene expression in the mouse brain: evidence from cDNA array. Synapse 2001; 41: 40-48.
81. Stumm G, Schlegel J, Schafer T, Wurz C, Mennel HD, Krieg JC and Vedder H. Amphetamines induce apoptosis and regulation of bcl-x splice variants in neocortical neurons. Faseb J 1999; 13: 1065-1072.
82. Cadet JL, Ordonez SV and Ordonez JV. Methamphetamine induces apoptosis in immortalized neural cells: protection by the proto-oncogene, bcl-2. Synapse 1997; 25: 176-184.
83. Jayanthi S, Deng X, Bordelon M, McCoy MT and Cadet JL. Methamphetamine causes differential regulation of pro-death and antideath Bcl-2 genes in the mouse neocortex. Faseb J 2001; 15: 1745-1752.
84. Deng X, Ladenheim B, Tsao LI and Cadet JL. Null mutation of c-fos causes exacerbation of methamphetamine-induced neurotoxicity. J Neurosci 1999; 19: 10107-10115.
85. Jayanthi S, Deng X, Noailles PA, Ladenheim B and Cadet JL. Methamphetamine induces neuronal apoptosis via cross-talks between endoplasmic reticulum and mitochondria-dependent death cascades. Faseb J 2004; 18: 238-251.
86. Ravagnan L, Roumier T and Kroemer G. Mitochondria, the killer organelles and their weapons. J Cell Physiol 2002; 192: 131-137.
87. Deng X and Cadet JL. Methamphetamine-induced apoptosis is attenuated in the striata of copper-zinc superoxide dismutase transgenic mice. Brain Res Mol Brain Res 2000; 83: 121-124.
88. Deng X, Cai NS, McCoy MT, Chen W, Trush MA and Cadet JL. Methamphetamine induces apoptosis in an immortalized rat striatal cell line by activating the mitochondrial cell death pathway. Neuropharmacology 2002; 42: 837-845.
89. Cadet JL, Jayanthi S and Deng X. Methamphetamine-induced neuronal apoptosis involves the activation of multiple death pathways. Review. Neurotox Res 2005; 8: 199-206.
90. Cadet JL, Krasnova IN, Jayanthi S and Lyles J. Neurotoxicity of substituted amphetamines: molecular and cellular mechanisms. Neurotox Res 2007; 11: 183-202.
91. Gorlach A, Klappa P and Kietzmann T. The endoplasmic reticulum: folding, calcium homeostasis, signaling, and redox control. Antioxid Redox Signal 2006; 8: 1391-1418.
92. McCullough KD, Martindale JL, Klotz LO, Aw TY and Holbrook NJ. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 2001; 21: 1249-1259.
93. Ferri KF and Kroemer G. Organelle-specific initiation of cell death pathways. Nat Cell Biol 2001; 3: E255-263.
94. Kroemer G, Galluzzi L and Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007; 87: 99-163.
95. Murachi T, Tanaka K, Hatanaka M and Murakami T. Intracellular Ca2+-dependent protease (calpain) and its high-molecular-weight endogenous inhibitor (calpastatin). Adv Enzyme Regul 1980; 19: 407-424.
96. Nakagawa T and Yuan J. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J Cell Biol 2000; 150: 887-894.
97. Marciniak SJ and Ron D. Endoplasmic reticulum stress signaling in disease. Physiol Rev 2006; 86: 1133-1149.
98. Patil C and Walter P. Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr Opin Cell Biol 2001; 13: 349-355.
99. Cadet JL, Ali S and Epstein C. Involvement of oxygen-based radicals in methamphetamine-induced neurotoxicity: evidence from the use of CuZnSOD transgenic mice. Ann N Y Acad Sci 1994; 738: 388-391.
100. Kreutzberg GW. Microglia: a sensor for pathological events in the CNS. Trends Neurosci 1996; 19: 312-318.
101. Kim YS and Joh TH. Microglia, major player in the brain inflammation: their roles in the pathogenesis of Parkinson's disease. Exp Mol Med 2006; 38: 333-347.
102. Perry VH, Cunningham C and Holmes C. Systemic infections and inflammation affect chronic neurodegeneration. Nat Rev Immunol 2007; 7: 161-167.
103. Garden GA. Microglia in human immunodeficiency virus-associated neurodegeneration. Glia 2002; 40: 240-251.
104. Sekine Y, Ouchi Y, Sugihara G, Takei N, Yoshikawa E, Nakamura K, Iwata Y, Tsuchiya KJ, Suda S, Suzuki K, Kawai M, Takebayashi K, Yamamoto S, Matsuzaki H, Ueki T, Mori N, Gold MS and Cadet JL. Methamphetamine causes microglial activation in the brains of human abusers. J Neurosci 2008; 28: 5756-5761.
105. Thomas DM and Kuhn DM. Attenuated microglial activation mediates tolerance to the neurotoxic effects of methamphetamine. J Neurochem 2005; 92: 790-797.
106. Boje KM and Arora PK. Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Res 1992; 587: 250-256.
107. Ehrlich LC, Hu S, Sheng WS, Sutton RL, Rockswold GL, Peterson PK and Chao CC. Cytokine regulation of human microglial cell IL-8 production. J Immunol 1998; 160: 1944-1948.
108. Gruol DL and Nelson TE. Physiological and pathological roles of interleukin-6 in the central nervous system. Mol Neurobiol 1997; 15: 307-339.
109. McGuire SO, Ling ZD, Lipton JW, Sortwell CE, Collier TJ and Carvey PM. Tumor necrosis factor alpha is toxic to embryonic mesencephalic dopamine neurons. Exp Neurol 2001; 169: 219-230.
110. Ladenheim B, Krasnova IN, Deng X, Oyler JM, Polettini A, Moran TH, Huestis MA and Cadet JL. Methamphetamine-induced neurotoxicity is attenuated in transgenic mice with a null mutation for interleukin-6. Mol Pharmacol 2000; 58: 1247-1256.
111. LaVoie MJ, Card JP and Hastings TG. Microglial activation precedes dopamine terminal pathology in methamphetamine-induced neurotoxicity. Exp Neurol 2004; 187: 47-57.
112. Thomas DM, Dowgiert J, Geddes TJ, Francescutti-Verbeem D, Liu X and Kuhn DM. Microglial activation is a pharmacologically specific marker for the neurotoxic amphetamines. Neurosci Lett 2004; 367: 349-354.
113. Thomas DM, Walker PD, Benjamins JA, Geddes TJ and Kuhn DM. Methamphetamine neurotoxicity in dopamine nerve endings of the striatum is associated with microglial activation. J Pharmacol Exp Ther 2004; 311: 1-7.
114. Aylward EH, Brettschneider PD, McArthur JC, Harris GJ, Schlaepfer TE, Henderer JD, Barta PE, Tien AY and Pearlson GD. Magnetic resonance imaging measurement of gray matter volume reductions in HIV dementia. Am J Psychiatry 1995; 152: 987-994.
115. Archibald SL, Masliah E, Fennema-Notestine C, Marcotte TD, Ellis RJ, McCutchan JA, Heaton RK, Grant I, Mallory M, Miller A and Jernigan TL. Correlation of in vivo neuroimaging abnormalities with postmortem human immunodeficiency virus encephalitis and dendritic loss. Arch Neurol 2004; 61: 369-376.
116. Chang L, Ernst T, Leonido-Yee M and Speck O. Perfusion MRI detects rCBF abnormalities in early stages of HIV-cognitive motor complex. Neurology 2000; 54: 389-396.
117. Ernst T, Itti E, Itti L and Chang L. Changes in cerebral metabolism are detected prior to perfusion changes in early HIV-CMC: A coregistered (1)H MRS and SPECT study. J Magn Reson Imaging 2000; 12: 859-865.
118. Stout JC, Ellis RJ, Jernigan TL, Archibald SL, Abramson I, Wolfson T, McCutchan JA, Wallace MR, Atkinson JH and Grant I. Progressive cerebral volume loss in human immunodeficiency virus infection: a longitudinal volumetric magnetic resonance imaging study. HIV Neurobehavioral Research Center Group. Arch Neurol 1998; 55: 161-168.
119. Bursztyn EM, Lee BC and Bauman J. CT of acquired immunodeficiency syndrome. AJNR Am J Neuroradiol 1984; 5: 711-714.
120. Levy RM, Rosenbloom S and Perrett LV. Neuroradiologic findings in AIDS: a review of 200 cases. AJR Am J Roentgenol 1986; 147: 977-983.
121. Liow JS, Rehm K, Strother SC, Anderson JR, Morch N, Hansen LK, Schaper KA and Rottenberg DA. Comparison of voxel- and volume-of-interest-based analyses in FDG PET scans of HIV positive and healthy individuals. J Nucl Med 2000; 41: 612-621.
122. von Giesen HJ, Antke C, Hefter H, Wenserski F, Seitz RJ and Arendt G. Potential time course of human immunodeficiency virus type 1-associated minor motor deficits: electrophysiologic and positron emission tomography findings. Arch Neurol 2000; 57: 1601-1607.
123. Chang L, Lee PL, Yiannoutsos CT, Ernst T, Marra CM, Richards T, Kolson D, Schifitto G, Jarvik JG, Miller EN, Lenkinski R, Gonzalez G and Navia BA. A multicenter in vivo proton-MRS study of HIV-associated dementia and its relationship to age. Neuroimage 2004; 23: 1336-1347.
124. Ernst T and Chang L. Effect of aging on brain metabolism in antiretroviral-naive HIV patients. Aids 2004; 18 Suppl 1: S61-67.
125. Lee PL, Yiannoutsos CT, Ernst T, Chang L, Marra CM, Jarvik JG, Richards TL, Kwok EW, Kolson DL, Simpson D, Tang CY, Schifitto G, Ketonen LM, Meyerhoff DJ, Lenkinski RE, Gonzalez RG and Navia BA. A multi-center 1H MRS study of the AIDS dementia complex: validation and preliminary analysis. J Magn Reson Imaging 2003; 17: 625-633.
126. Meyerhoff DJ, Weiner MW and Fein G. Deep gray matter structures in HIV infection: a proton MR spectroscopic study. AJNR Am J Neuroradiol 1996; 17: 973-978.
127. Moller HE, Vermathen P, Lentschig MG, Schuierer G, Schwarz S, Wiedermann D, Evers S and Husstedt IW. Metabolic characterization of AIDS dementia complex by spectroscopic imaging. J Magn Reson Imaging 1999; 9: 10-18.
128. Stankoff B, Tourbah A, Suarez S, Turell E, Stievenart JL, Payan C, Coutellier A, Herson S, Baril L, Bricaire F, Calvez V, Cabanis EA, Lacomblez L and Lubetzki C. Clinical and spectroscopic improvement in HIV-associated cognitive impairment. Neurology 2001; 56: 112-115.
129. Suwanwelaa N, Phanuphak P, Phanthumchinda K, Suwanwela NC, Tantivatana J, Ruxrungtham K, Suttipan J, Wangsuphachart S and Hanvanich M. Magnetic resonance spectroscopy of the brain in neurologically asymptomatic HIV-infected patients. Magn Reson Imaging 2000; 18: 859-865.
130. Tarasow E, Wiercinska-Drapalo A, Kubas B, Dzienis W, Orzechowska- Bobkiewicz A, Prokopowicz D and Walecki J. Cerebral MR spectroscopy in neurologically asymptomatic HIV-infected patients. Acta Radiol 2003; 44: 206-212.
131. Chang L, Ernst T, Witt MD, Ames N, Gaiefsky M and Miller E. Relationships among brain metabolites, cognitive function, and viral loads in antiretroviral-naive HIV patients. Neuroimage 2002; 17: 1638-1648.
132. Chang L, Ernst T, Witt MD, Ames N, Walot I, Jovicich J, DeSilva M, Trivedi N, Speck O and Miller EN. Persistent brain abnormalities in antiretroviral-naive HIV patients 3 months after HAART. Antivir Ther 2003; 8: 17-26.
133. Brew BJ, Corbeil J, Pemberton L, Evans L, Saito K, Penny R, Cooper DA and Heyes MP. Quinolinic acid production is related to macrophage tropic isolates of HIV-1. J Neurovirol 1995; 1: 369-374.
134. Gartner S. HIV infection and dementia. Science 2000; 287: 602-604.
135. Giulian D, Vaca K and Noonan CA. Secretion of neurotoxins by mononuclear phagocytes infected with HIV-1. Science 1990; 250: 1593-1596.
136. Giulian D, Wendt E, Vaca K and Noonan CA. The envelope glycoprotein of human immunodeficiency virus type 1 stimulates release of neurotoxins from monocytes. Proc Natl Acad Sci U S A 1993; 90: 2769-2773.
137. Jiang ZG, Piggee C, Heyes MP, Murphy C, Quearry B, Bauer M, Zheng J, Gendelman HE and Markey SP. Glutamate is a mediator of neurotoxicity in secretions of activated HIV-1-infected macrophages. J Neuroimmunol 2001; 117: 97-107.
138. Lipton SA, Sucher NJ, Kaiser PK and Dreyer EB. Synergistic effects of HIV coat protein and NMDA receptor-mediated neurotoxicity. Neuron 1991; 7: 111-118.
139. Viviani B, Corsini E, Binaglia M, Galli CL and Marinovich M. Reactive oxygen species generated by glia are responsible for neuron death induced by human immunodeficiency virus-glycoprotein 120 in vitro. Neuroscience 2001; 107: 51-58.
140. Zhao J, Lopez AL, Erichsen D, Herek S, Cotter RL, Curthoys NP and Zheng J. Mitochondrial glutaminase enhances extracellular glutamate production in HIV-1-infected macrophages: linkage to HIV-1 associated dementia. J Neurochem 2004; 88: 169-180.
141. Zhao ML, Kim MO, Morgello S and Lee SC. Expression of inducible nitric oxide synthase, interleukin-1 and caspase-1 in HIV-1 encephalitis. J Neuroimmunol 2001; 115: 182-19.
142. Letendre SL, Lanier ER and McCutchan JA. Cerebrospinal fluid beta chemokine concentrations in neurocognitively impaired individuals infected with human immunodeficiency virus type 1. J Infect Dis 1999; 180: 310-319.
143. Kaul M and Lipton SA. Chemokines and activated macrophages in HIV gp120-induced neuronal apoptosis. Proc Natl Acad Sci U S A 1999; 96: 8212-8216.
144. Meucci O and Miller RJ. gp120-induced neurotoxicity in hippocampal pyramidal neuron cultures: protective action of TGF-beta1. J Neurosci 1996; 16: 4080-4088.
145. Garden GA, Guo W, Jayadev S, Tun C, Balcaitis S, Choi J, Montine TJ, Moller T and Morrison RS. HIV associated neurodegeneration requires p53 in neurons and microglia. Faseb J 2004; 18: 1141-1143.
146. Milward EA, Fitzsimmons C, Szklarczyk A and Conant K. The matrix metalloproteinases and CNS plasticity: an overview. J Neuroimmunol 2007; 187: 9-19.
147. Gasche Y, Soccal PM, Kanemitsu M and Copin JC. Matrix metalloproteinases and diseases of the central nervous system with a special emphasis on ischemic brain. Front Biosci 2006; 11: 1289-1301.
148. Lo EH, Wang X and Cuzner ML. Extracellular proteolysis in brain injury and inflammation: role for plasminogen activators and matrix metalloproteinases. J Neurosci Res 2002; 69: 1-9.
149. Johnston JB, Zhang K, Silva C, Shalinsky DR, Conant K, Ni W, Corbett D, Yong VW and Power C. HIV-1 Tat neurotoxicity is prevented by matrix metalloproteinase inhibitors. Ann Neurol 2001; 49: 230-241.
150. Webster NL and Crowe SM. Matrix metalloproteinases, their production by monocytes and macrophages and their potential role in HIV-related diseases. J Leukoc Biol 2006; 80: 1052-1066.
151. Zhang K, McQuibban GA, Silva C, Butler GS, Johnston JB, Holden J, Clark-Lewis I, Overall CM and Power C. HIV-induced metalloproteinase processing of the chemokine stromal cell derived factor-1 causes neurodegeneration. Nat Neurosci 2003; 6: 1064-1071.
152. Conant K, McArthur JC, Griffin DE, Sjulson L, Wahl LM and Irani DN. Cerebrospinal fluid levels of MMP-2, 7, and 9 are elevated in association with human immunodeficiency virus dementia. Ann Neurol 1999; 46: 391-398.
153. Chong YH, Seoh JY and Park HK. Increased activity of matrix metalloproteinase-2 in human glial and neuronal cell lines treated with HIV-1 gp41 peptides. J Mol Neurosci 1998; 10: 129-141.
154. Marshall DC, Wyss-Coray T and Abraham CR. Induction of matrix metalloproteinase-2 in human immunodeficiency virus-1 glycoprotein 120 transgenic mouse brains. Neurosci Lett 1998; 254: 97-100.
155. Peruzzi F. The multiple functions of HIV-1 Tat: proliferation versus apoptosis. Front Biosci 2006; 11: 708-717.
156. Tardieu M, Hery C, Peudenier S, Boespflug O and Montagnier L. Human immunodeficiency virus type 1-infected monocytic cells can destroy human neural cells after cell-to-cell adhesion. Ann Neurol 1992; 32: 11-17.
157. Li W, Galey D, Mattson MP and Nath A. Molecular and cellular mechanisms of neuronal cell death in HIV dementia. Neurotox Res 2005; 8: 119-134.
158. Aksenov MY, Hasselrot U, Wu G, Nath A, Anderson C, Mactutus CF and Booze RM. Temporal relationships between HIV-1 Tat-induced neuronal degeneration, OX-42 immunoreactivity, reactive astrocytosis, and protein oxidation in the rat striatum. Brain Res 2003; 987: 1-9.
159. Bansal AK, Mactutus CF, Nath A, Maragos W, Hauser KF and Booze RM. Neurotoxicity of HIV-1 proteins gp120 and Tat in the rat striatum. Brain Res 2000; 879: 42-49.
160. Gavriil ES, Cooney R and Weeks BS. Tat mediates apoptosis in vivo in the rat central nervous system. Biochem Biophys Res Commun 2000; 267: 252-256.
161. Jones M, Olafson K, Del Bigio MR, Peeling J and Nath A. Intraventricular injection of human immunodeficiency virus type 1 (HIV-1) tat protein causes inflammation, gliosis, apoptosis, and ventricular enlargement. J Neuropathol Exp Neurol 1998; 57: 563-570.
162. Bruce-Keller AJ, Chauhan A, Dimayuga FO, Gee J, Keller JN and Nath A. Synaptic transport of human immunodeficiency virus-Tat protein causes neurotoxicity and gliosis in rat brain. J Neurosci 2003; 23: 8417-8422.
163. Bonavia R, Bajetto A, Barbero S, Albini A, Noonan DM and Schettini G. HIV-1 Tat causes apoptotic death and calcium homeostasis alterations in rat neurons. Biochem Biophys Res Commun 2001; 288: 301-308.
164. Kruman, II, Nath A and Mattson MP. HIV-1 protein Tat induces apoptosis of hippocampal neurons by a mechanism involving caspase activation, calcium overload, and oxidative stress. Exp Neurol 1998; 154: 276-288.
165. Bartz SR 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 1999; 73: 1956-1963.
166. Perry SW, Norman JP, Litzburg A, Zhang D, Dewhurst S and Gelbard HA. HIV-1 transactivator of transcription protein induces mitochondrial hyperpolarization and synaptic stress leading to apoptosis. J Immunol 2005; 174: 4333-4344.
167. Agrawal L, Louboutin JP and Strayer DS. Preventing HIV-1 Tat-induced neuronal apoptosis using antioxidant enzymes: mechanistic and therapeutic implications. Virology 2007; 363: 462-472.
168. Westendorp MO, Shatrov VA, Schulze-Osthoff K, Frank R, Kraft M, Los M, Krammer PH, Droge W and Lehmann V. HIV-1 Tat potentiates TNF-induced NF-kappa B activation and cytotoxicity by altering the cellular redox state. Embo J 1995; 14: 546-554.
169. Magnuson DS, Knudsen BE, Geiger JD, Brownstone RM and Nath A. Human immunodeficiency virus type 1 tat activates non-N-methyl-D-aspartate excitatory amino acid receptors and causes neurotoxicity. Ann Neurol 1995; 37: 373-380.
170. New DR, Ma M, Epstein LG, Nath A and Gelbard HA. Human immunodeficiency virus type 1 Tat protein induces death by apoptosis in primary human neuron cultures. J Neurovirol 1997; 3: 168-173.
171. Perez A, Probert AW, Wang KK and Sharmeen L. Evaluation of HIV-1 Tat induced neurotoxicity in rat cortical cell culture. J Neurovirol 2001; 7: 1-10.
172. Caporello E, Nath A, Slevin J, Galey D, Hamilton G, Williams L, Steiner JP and Haughey NJ. The immunophilin ligand GPI1046 protects neurons from the lethal effects of the HIV-1 proteins gp120 and Tat by modulating endoplasmic reticulum calcium load. J Neurochem 2006; 98: 146-155.
173. Willey RL, Bonifacino JS, Potts BJ, Martin MA and Klausner RD. Biosynthesis, cleavage, and degradation of the human immunodeficiency virus 1 envelope glycoprotein gp160. Proc Natl Acad Sci U S A 1988; 85: 9580-9584.
174. Wu P, Price P, Du B, Hatch WC and Terwilliger EF. Direct cytotoxicity of HIV-1 envelope protein gp120 on human NT neurons. Neuroreport 1996; 7: 1045-1049.
175. Bachis A, Major EO and Mocchetti I. Brain-derived neurotrophic factor inhibits human immunodeficiency virus-1/gp120-mediated cerebellar granule cell death by preventing gp120 internalization. J Neurosci 2003; 23: 5715-5722.
176. Brenneman DE, Westbrook GL, Fitzgerald SP, Ennist DL, Elkins KL, Ruff MR and Pert CB. Neuronal cell killing by the envelope protein of HIV and its prevention by vasoactive intestinal peptide. Nature 1988; 335: 639-642.
177. Dreyer EB, Kaiser PK, Offermann JT and Lipton SA. HIV-1 coat protein neurotoxicity prevented by calcium channel antagonists. Science 1990; 248: 364-367.
178. Toggas SM, Masliah E, Rockenstein EM, Rall GF, Abraham CR and Mucke L. Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 1994; 367: 188-193.
179. D'Hooge R, Franck F, Mucke L and De Deyn PP. Age-related behavioural deficits in transgenic mice expressing the HIV-1 coat protein gp120. Eur J Neurosci 1999; 11: 4398-4402.
180. Hill JM, Mervis RF, Avidor R, Moody TW and Brenneman DE. HIV envelope protein-induced neuronal damage and retardation of behavioral development in rat neonates. Brain Res 1993; 603: 222-233.
181. Dawson VL, Dawson TM, Uhl GR and Snyder SH. Human immunodeficiency virus type 1 coat protein neurotoxicity mediated by nitric oxide in primary cortical cultures. Proc Natl Acad Sci U S A 1993; 90: 3256-3259.
182. Garden GA, Budd SL, Tsai E, Hanson L, Kaul M, D'Emilia DM, Friedlander RM, Yuan J, Masliah E and Lipton SA. Caspase cascades in human immunodeficiency virus-associated neurodegeneration. J Neurosci 2002; 22: 4015-4024.
183. Koka P, He K, Camerini D, Tran T, Yashar SS and Merrill JE. The mapping of HIV-1 gp160 epitopes required for interleukin-1 and tumor necrosis factor alpha production in glial cells. J Neuroimmunol 1995; 57: 179-191.
184. Koka P, He K, Zack JA, Kitchen S, Peacock W, Fried I, Tran T, Yashar SS and Merrill JE. Human immunodeficiency virus 1 envelope proteins induce interleukin 1, tumor necrosis factor alpha, and nitric oxide in glial cultures derived from fetal, neonatal, and adult human brain. J Exp Med 1995; 182: 941-951.
185. Merrill JE, Koyanagi Y, Zack J, Thomas L, Martin F and Chen IS. Induction of interleukin-1 and tumor necrosis factor alpha in brain cultures by human immunodeficiency virus type 1. J Virol 1992; 66: 2217-2225.
186. Dickson DW, Lee SC, Mattiace LA, Yen SH and Brosnan C. Microglia and cytokines in neurological disease, with special reference to AIDS and Alzheimer's disease. Glia 1993; 7: 75-83.
187. Kure K, Lyman WD, Weidenheim KM and Dickson DW. Cellular localization of an HIV-1 antigen in subacute AIDS encephalitis using an improved double-labeling immunohistochemical method. Am J Pathol 1990; 136: 1085-1092.
188. Kure K, Weidenheim KM, Lyman WD and Dickson DW. Morphology and distribution of HIV-1 gp41-positive microglia in subacute AIDS encephalitis. Pattern of involvement resembling a multisystem degeneration. Acta Neuropathol 1990; 80: 393-400.
189. Adamson DC, McArthur JC, Dawson TM and Dawson VL. Rate and severity of HIV-associated dementia (HAD): correlations with Gp41 and iNOS. Mol Med 1999; 5: 98-109.
190. Bukrinsky M and Adzhubei A. Viral protein R of HIV-1. Rev Med Virol 1999; 9: 39-49.
191. Piller SC, Jans P, Gage PW and Jans DA. Extracellular HIV-1 virus protein R causes a large inward current and cell death in cultured hippocampal neurons: implications for AIDS pathology. Proc Natl Acad Sci U S A 1998; 95: 4595-4600.
192. Sabbah EN and Roques BP. Critical implication of the (70-96) domain of human immunodeficiency virus type 1 Vpr protein in apoptosis of primary rat cortical and striatal neurons. J Neurovirol 2005; 11: 489-502.
193. Jones GJ, Barsby NL, Cohen EA, Holden J, Harris K, Dickie P, Jhamandas J and Power C. HIV-1 Vpr causes neuronal apoptosis and in vivo neurodegeneration. J Neurosci 2007; 27: 3703-3711.
194. Jacotot E, Ferri KF, El Hamel C, Brenner C, Druillennec S, Hoebeke J, Rustin P, Metivier D, Lenoir C, Geuskens M, Vieira HL, Loeffler M, Belzacq AS, Briand JP, Zamzami N, Edelman L, Xie ZH, Reed JC, Roques BP and Kroemer G. Control of mitochondrial membrane permeabilization by adenine nucleotide translocator interacting with HIV-1 viral protein rR and Bcl-2. J Exp Med 2001; 193: 509-519.
195. Jacotot E, Ravagnan L, Loeffler M, Ferri KF, Vieira HL, Zamzami N, Costantini P, Druillennec S, Hoebeke J, Briand JP, Irinopoulou T, Daugas E, Susin SA, Cointe D, Xie ZH, Reed JC, Roques BP and Kroemer G. The HIV-1 viral protein R induces apoptosis via a direct effect on the mitochondrial permeability transition pore. J Exp Med 2000; 191: 33-46.
196. Sabbah EN, Druillennec S, Morellet N, Bouaziz S, Kroemer G and Roques BP. Interaction between the HIV-1 protein Vpr and the adenine nucleotide translocator. Chem Biol Drug Des 2006; 67: 145-154.
197. Patel CA, Mukhtar M and Pomerantz RJ. Human immunodeficiency virus type 1 Vpr induces apoptosis in human neuronal cells. J Virol 2000; 74: 9717-9726.
198. Stewart SA, Poon B, Song JY and Chen IS. Human immunodeficiency virus type 1 vpr induces apoptosis through caspase activation. J Virol 2000; 74: 3105-3111.
199. Shostak LD, Ludlow J, Fisk J, Pursell S, Rimel BJ, Nguyen D, Rosenblatt JD and Planelles V. Roles of p53 and caspases in the induction of cell cycle arrest and apoptosis by HIV-1 vpr. Exp Cell Res 1999; 251: 156-165.
200. Tungaturthi PK, Sawaya BE, Singh SP, Tomkowicz B, Ayyavoo V, Khalili K, Collman RG, Amini S and Srinivasan A. Role of HIV-1 Vpr in AIDS pathogenesis: relevance and implications of intravirion, intracellular and free Vpr. Biomed Pharmacother 2003; 57: 20-24.
201. Das SR and Jameel S. Biology of the HIV Nef protein. Indian J Med Res 2005; 121: 315-332.
202. Koedel U, Kohleisen B, Sporer B, Lahrtz F, Ovod V, Fontana A, Erfle V and Pfister HW. HIV type 1 Nef protein is a viral factor for leukocyte recruitment into the central nervous system. J Immunol 1999; 163: 1237-1245.
203. Bencheikh M, Bentsman G, Sarkissian N, Canki M and Volsky DJ. Replication of different clones of human immunodeficiency virus type 1 in primary fetal human astrocytes: enhancement of viral gene expression by Nef. J Neurovirol 1999; 5: 115-124.
204. Harris M. HIV: a new role for Nef in the spread of HIV. Curr Biol 1999; 9: R459-461.
205. Kestler HW, 3rd, Ringler DJ, Mori K, Panicali DL, Sehgal PK, Daniel MD and Desrosiers RC. Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 1991; 65: 651-662.
206. Acheampong E, Mukhtar M, Parveen Z, Ngoubilly N, Ahmad N, Patel C and Pomerantz RJ. Ethanol strongly potentiates apoptosis induced by HIV-1 proteins in primary human brain microvascular endothelial cells. Virology 2002; 304: 222-234.
207. He J, deCastro CM, Vandenbark GR, Busciglio J and Gabuzda D. Astrocyte apoptosis induced by HIV-1 transactivation of the c-kit protooncogene. Proc Natl Acad Sci U S A 1997; 94: 3954-3959.
208. Trillo-Pazos G, McFarlane-Abdulla E, Campbell IC, Pilkington GJ and Everall IP. Recombinant nef HIV-IIIB protein is toxic to human neurons in culture. Brain Res 2000; 864: 315-326.
209. Mordelet E, Kissa K, Cressant A, Gray F, Ozden S, Vidal C, Charneau P and Granon S. Histopathological and cognitive defects induced by Nef in the brain. Faseb J 2004; 18: 1851-1861.
210. Taylor MJ, Alhassoon OM, Schweinsburg BC, Videen JS and Grant I. MR spectroscopy in HIV and stimulant dependence HNRC Group. HIV Neurobehavioral Research Center. J Int Neuropsychol Soc 2000; 6: 83-85.
211. Maragos WF, Young KL, Turchan JT, Guseva M, Pauly JR, Nath A and Cass WA. Human immunodeficiency virus-1 Tat protein and methamphetamine interact synergistically to impair striatal dopaminergic function. J Neurochem 2002; 83: 955-963.
212. Czub S, Koutsilieri E, Sopper S, Czub M, Stahl-Hennig C, Muller JG, Pedersen V, Gsell W, Heeney JL, Gerlach M, Gosztonyi G, Riederer P and ter Meulen V. Enhancement of central nervous system pathology in early simian immunodeficiency virus infection by dopaminergic drugs. Acta Neuropathol 2001; 101: 85-91.
213. Flora G, Lee YW, Nath A, Hennig B, Maragos W and Toborek M. Methamphetamine potentiates HIV-1 Tat protein-mediated activation of redox-sensitive pathways in discrete regions of the brain. Exp Neurol 2003; 179: 60-70.
214. Theodore S, Cass WA and Maragos WF. Involvement of cytokines in human immunodeficiency virus-1 protein Tat and methamphetamine interactions in the striatum. Exp Neurol 2006; 199: 490-498.
215. 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 2004; 10: 327-337.
216. Cass WA, Harned ME, Peters LE, Nath A and Maragos WF. HIV-1 protein Tat potentiation of methamphetamine-induced decreases in evoked overflow of dopamine in the striatum of the rat. Brain Res 2003; 984: 133-142.
217. Theodore S, Cass WA, Nath A, Steiner J, Young K and Maragos WF. Inhibition of tumor necrosis factor-alpha signaling prevents human immunodeficiency virus-1 protein Tat and methamphetamine interaction. Neurobiol Dis 2006; 23: 663-668.
218. 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 2004; 10: 21-28.
219. Hauser KF, El-Hage N, Stiene-Martin A, Maragos WF, Nath A, Persidsky Y, Volsky DJ and Knapp PE. HIV-1 neuropathogenesis: glial mechanisms revealed through substance abuse. J Neurochem 2007; 100: 567-586.