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Methamphetamine and lentivirus interactions: Reciprocal enhancement of central nervous system disease

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Abstract

Use of methamphetamine is increasingly a significant factor for the spread of human immunodeficiency virus type 1, for in certain populations, there is a convergence of methamphetamine abuse with human immunodeficiency virus type 1 infection. Methamphetamine and human immunodeficiency virus type 1 are both individually neuropathogenic, and the neuropathology caused by these two agents occurs in overlapping brain regions. However, the biological interaction of methamphetamine with lentiviruses remains unknown. Here, we investigate the effects of simultaneous exposure of these two agents on disease progression using the feline immunodeficiency virus model. The study models the bingeing methamphetamine user with sequential and repeatedepisodes of use, which were interrupted by periods of abstinence. Methamphetamine exposure significantly accelerated and enhanced the severity of the feline immunodeficiency virus model-induced central nervous system functional pathology, as measured in delays in brainstem auditory evoked potentials. Reciprocally, feline immunodeficiency virus enhanced the severity of the methamphetamine-induced effects on brain monoamine neurotransmitter and dopamine transporter levels. The results of this study indicate that a dual potentiation occurred. That is, methamphetamine enhanced feline immunodeficiency virus model—induced central nervous system disease and feline immunodeficiency virus model enhanced the toxic effects of methamphetamine, heralding a significant concern for those individuals that are exposed to both agents.

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References

  • Abbruzzese G, Rizzo F, Dall’Agata D, Morandi N, Favale E (1990). Generalized dystonia with bilateral striatal computed-tomographic lucencies in a patient with human immunodeficiency virus infection. Eur Neurol 30: 271–273.

    Article  CAS  PubMed  Google Scholar 

  • Albers DS, Sonsalla PK (1995). Methamphetamine-induced hyperthermia and dopaminergic neurotoxicity in mice: pharmacological profile of protective and nonprotective agents. J Pharmacol Exp Ther 275: 1104–1114.

    CAS  PubMed  Google Scholar 

  • Angrist B (1994). Amphetamine psychosis: clinical variation of the syndrome. San Diego: Academic Press.

    Google Scholar 

  • Barr MC, Billaud JN, Selway DR, Huitron-Resendiz S, Osborn KG, Henriksen SJ, Phillips TR (2000a). Effects of multiple acute morphine exposures on feline immunodeficiency virus disease progression. J Infect Dis 182: 725–732.

    Article  CAS  PubMed  Google Scholar 

  • Barr MC, Huitron-Resendiz S, Sanchez-Alavez M, Henriksen SJ, Phillips TR (2003). Escalating morphine exposures followed by withdrawal in feline immunodeficiency virus-infected cats. Drug Alcohol Depend 72: 141–149.

    Article  CAS  PubMed  Google Scholar 

  • Barr MC, Huitron-Resendiz S, Selway DR, Henriksen SJ, Phillips TR (2000b). Exogenous glucocorticoids alter parameters of early feline immunodeficiency virus infection. J Infect Dis 181: 576–586.

    Article  CAS  PubMed  Google Scholar 

  • Bell JE, Brettle RP, Chiswick A, Simmonds P (1998). HIV encephalitis, proviral load and dementia in drug users and homosexuals with AIDS. Effect of neocortical involvement. Brain 121 (Pt 11): 2043–2052.

    Article  PubMed  Google Scholar 

  • Berger JR, Nath A (1997). HIV dementia and the basal ganglia. Intervirology 40: 122–131.

    Article  CAS  PubMed  Google Scholar 

  • Bouwman FH, Skolasky RL, Hes D, Selnes OA, Glass JD, Nance-Sproson TE, Royal W, Dal Pan GJ, McArthur JC (1998). Variable progression of HIV-associated dementia. Neurology 50: 1814–1820.

    CAS  PubMed  Google Scholar 

  • Broening HW, Pu C, Vorhees CV (1997). Methamphetamine selectively damages dopaminergic innervation to the nucleus accumbens core while sparing the shell. Synapse 27: 153–160.

    Article  CAS  PubMed  Google Scholar 

  • Callahan B, Yuan J, Stover G, Hatzidimitriou G, Ricaurte G (1998). Effects of 2-deoxy-D-glucose on methamphetamine-induced dopamine and serotonin neurotoxicity. J Neurochem 70: 190–197.

    Article  CAS  PubMed  Google Scholar 

  • Cappon GD, Morford LL, Vorhees CV (1997). Ontogeny of methamphetamine-induced neurotoxicity and associated hyperthermic response. Brain Res Dev Brain Res 103: 155–162.

    Article  CAS  PubMed  Google Scholar 

  • Cass WA, Harned ME, Peters LE, Nath A, Maragos WF (2003). HIV-1 protein Tat potentiation of methamphetamine-induced decreases in evoked overflow of dopamine in the striatum of the rat. Brain Res 984: 133–142.

    Article  CAS  PubMed  Google Scholar 

  • Cass WA, Manning MW (1999). Recovery of presynaptic dopaminergic functioning in rats treated with neurotoxic doses of methamphetamine. J Neurosci 19: 7653–7660.

    CAS  PubMed  Google Scholar 

  • Castello E, Baroni N, Pallestrini E (1998). Neurotological auditory brain stem response findings in human immunodeficiency virus-positive patients without neurologic manifestations. Ann Otol Rhinol Laryngol 107: 1054–1060.

    CAS  PubMed  Google Scholar 

  • Cazzullo CL, Gala C, Ducati A, Landi A, Donati R, Russo R, Rossini M, Nicolosi A (1990). Multimodality evoked potentials in HIV infected subjects: a longitudinal study. Ital J Neurol Sci 11: 481–485.

    Article  CAS  PubMed  Google Scholar 

  • Chang L, Ernst T, Speck O, Grob CS (2005). Additive effects of HIV and chronic methamphetamine use on brain metabolite abnormalities. Am J Psychiatry 162: 361–369.

    Article  PubMed  Google Scholar 

  • Christensen LA, Morehouse CR, Powell TW, Alchediak T, Silio M (1998). Antiviral therapy in a child with pediatric human immunodeficiency virus (HIV): case study of audiologic findings. J Am Acad Audiol 9: 292–298.

    CAS  PubMed  Google Scholar 

  • Commins DL, Vosmer G, Virus RM, Woolverton WL, Schuster CR, Seiden LS (1987). Biochemical and histological evidence that methylenedioxymethylamphetamine (MDMA) is toxic to neurons in the rat brain. J Pharmacol Exp Ther 241: 338–345.

    CAS  PubMed  Google Scholar 

  • Corsi KF, Booth RE (2008). HIV sex risk behaviors among heterosexual methamphetamine users: literature review from 2000 to present. Curr Drug Abuse Rev 1: 292–296.

    Article  PubMed  Google Scholar 

  • Crews L, Patrick C, Achim CL, Everall IP, Masliah E (2009). Molecular pathology of Neuro-AIDS (CNS-HIV). Int J Mol Sci 10: 1045–1063.

    Article  CAS  PubMed  Google Scholar 

  • Ellinwood EH, Jr., Escalante O (1970). Behavior and histopathological findings during chronic methedrine intoxication. Biol Psychiatry 2: 27–39.

    CAS  PubMed  Google Scholar 

  • Everall I, Luthert P, Lantos P (1993). A review of neuronal damage in human immunodeficiency virus infection: its assessment, possible mechanism and relationship to dementia. J Neuropathol Exp Neurol 52: 561–566.

    Article  CAS  PubMed  Google Scholar 

  • Ferris MJ, Mactutus CF, Booze RM (2008). 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: 883–909.

    Article  CAS  PubMed  Google Scholar 

  • Fox HS, Weed MR, Huitron-Resendiz S, Baig J, Horn TF, Dailey PJ, Bischofberger N, Henriksen SJ (2000). Antiviral treatment normalizes neurophysiological but not movement abnormalities in simian immunodeficiency virus-infected monkeys. J Clin Invest 106: 37–45.

    Article  CAS  PubMed  Google Scholar 

  • Gavrilin MA, Mathes LE, Podell M (2002). Methamphetamine enhances cell-associated feline immunodeficiency virus replication in astrocytes. J NeuroVirol 8: 240–249.

    Article  CAS  PubMed  Google Scholar 

  • Gruol DL, Yu N, Parsons KL, Billaud JN, Elder JH, Phillips TR (1998). Neurotoxic effects of feline immunodeficiency virus, FIV-PPR. J NeuroVirol 4: 415–425.

    Article  CAS  PubMed  Google Scholar 

  • Hanson JE, Birdsall E, Seferian KS, Crosby MA, Keefe KA, Gibb JW, Hanson GR, Fleckenstein AE (2009). Methamphetamine-induced dopaminergic deficits and refractoriness to subsequent treatment. Eur J Pharmacol 607: 68–73.

    Article  CAS  PubMed  Google Scholar 

  • Hausler R, Vibert D, Koralnik IJ, Hirschel B (1991). Neurootological manifestations in different stages of HIV infection. Acta Otolaryngol Suppl 481: 515–521.

    Article  CAS  PubMed  Google Scholar 

  • Henriksen SJ, Prospero-Garcia O, Phillips TR, Fox HS, Bloom FE, Elder JH (1995). Feline immunodeficiency virus as a model for study of lentivirus infection of the central nervous system. In: Current topics in microbiology and immunology: HIV and dementia. Oldstone MBA, Vitkovic L (eds). Springer, Berlin, Germany. pp 167–186.

    Google Scholar 

  • Jaffe J (1990). Drug addiction and drug abuse. In: The pharmacological basis of therapeutics, 8th ed. Alfred G Gilman, Alan S Nies, Theodore W Rall, Palmer Tayler (eds). New York: McGraw-Hill, pp 522–573.

    Google Scholar 

  • Kipke MD, O’Connor S, Palmer R, MacKenzie RG (1995). Street youth in Los Angeles. Profile of a group at high risk for human immunodeficiency virus infection. Arch Pediatr Adolesc Med 149: 513–519.

    CAS  PubMed  Google Scholar 

  • Klein D, Leutenegger CM, Bahula C, Gold P, Hofmann-Lehmann R, Salmons B, Lutz H, Gunzburg WH (2001). Influence of preassay and sequence variations on viral load determination by a multiplex real-time reverse transcriptase-polymerase chain reaction for feline immunodeficiency virus. J Acquir Immune Defic Syndr 26: 8–20.

    CAS  PubMed  Google Scholar 

  • Kogan FJ, Nichols WK, Gibb JW (1976). Influence of methamphetamine on nigral and striatal tyrosine hydroxylase activity and on striatal dopamine levels. Eur J Pharmacol 36: 363–371.

    Article  CAS  PubMed  Google Scholar 

  • Langford D, Adame A, Grigorian A, Grant I, McCutchan JA, Ellis RJ, Marcotte TD, Masliah E (2003). Patterns of selective neuronal damage in methamphetamine-user AIDS patients. J Acquir Immune Defic Syndr 34: 467–474.

    Article  CAS  PubMed  Google Scholar 

  • Liang H, Wang X, Chen H, Song L, Ye L, Wang SH, Wang YJ, Zhou L, Ho WZ (2008). Methamphetamine enhances HIV infection of macrophages. Am J Pathol 172: 1617–1624.

    Article  CAS  PubMed  Google Scholar 

  • Maragos WF, Young KL, Turchan JT, Guseva M, Pauly JR, Nath A, Cass WA (2002). Human immunodeficiency virus-1 Tat protein and methamphetamine interact synergistically to impair striatal dopaminergic function. J Neurochem 83: 955–963.

    Article  CAS  PubMed  Google Scholar 

  • Masliah E, Ge N, Achim CL, Hansen LA, Wiley CA (1992). Selective neuronal vulnerability in HIV encephalitis. J Neuropathol Exp Neurol 51: 585–593.

    Article  CAS  PubMed  Google Scholar 

  • Masliah E, Heaton RK, Marcotte TD, Ellis RJ, Wiley CA, Mallory M, Achim CL, McCutchan JA, Nelson JA, Atkinson JH, Grant I, Group H (1997). Dendritic injury is a pathological substrate for human immunodeficiency virus-related cognitive disorders. Ann Neurol 42: 963–972.

    Article  CAS  PubMed  Google Scholar 

  • Meeker RB, Thiede BA, Hall C, English R, Tompkins M (1997). Cortical cell loss in asymptomatic cats experimentally infected with feline immunodeficiency virus. AIDS Res Hum Retroviruses 13: 1131–1140.

    Article  CAS  PubMed  Google Scholar 

  • Molitor F, Truax SR, Ruiz JD, Sun RK (1998). Association of methamphetamine use during sex with risky sexual behaviors and HIV infection among non-injection drug users. West J Med 168: 93–97.

    CAS  PubMed  Google Scholar 

  • Molliver ME, Berger UV, Mamounas LA, Molliver DC, O’Hearn E, Wilson MA (1990). Neurotoxicity of MDMA and related compounds: anatomic studies. Ann N Y Acad Sci 600: 649–661; discussion 661–644.

    Article  CAS  PubMed  Google Scholar 

  • Moore DJ, Masliah E, Rippeth JD, Gonzalez R, Carey CL, Cherner M, Ellis RJ, Achim CL, Marcotte TD, Heaton RK, Grant I (2006). Cortical and subcortical neurodegeneration is associated with HIV neurocognitive impairment. AIDS 20: 879–887.

    Article  PubMed  Google Scholar 

  • Nath A, Hauser KF, Wojna V, Booze RM, Maragos W, Prendergast M, Cass W, Turchan JT (2002). Molecular basis for interactions of HIV and drugs of abuse. J Acquir Immune Defic Syndr 31 (Suppl 2): S62-S69.

    CAS  PubMed  Google Scholar 

  • Nath A, Maragos WF, Avison MJ, Schmitt FA, Berger JR (2001). Acceleration of HIV dementia with methamphetamine and cocaine. J NeuroVirol 7: 66–71.

    Article  CAS  PubMed  Google Scholar 

  • Ollo C, Johnson R, Jr., Grafman J (1991). Signs of cognitive change in HIV disease: an event-related brain potential study. Neurology 41: 209–215.

    CAS  PubMed  Google Scholar 

  • Pardo J, Marcos A, Bhathal H, Castro M, Varea de Seijas E (1998). Chorea as a form of presentation of human immunodeficiency virus-associated dementia complex. Neurology 50: 568–569.

    CAS  PubMed  Google Scholar 

  • Phillips TR, Billaud JN, Henriksen SJ (2000). Methamphetamine and HIV-1: potential interactions and the use of the FIV/cat model. J Psychopharmacol 14: 244–250.

    Article  CAS  PubMed  Google Scholar 

  • Phillips TR, Prospero-Garcia O, Puaoi DL, Lerner DL, Fox HS, Olmsted RA, Bloom FE, Henriksen SJ, Elder JH (1994). Neurological abnormalities associated with feline immunodeficiency virus infection. J Gen Virol 75: 979–987.

    Article  CAS  PubMed  Google Scholar 

  • Phillips TR, Prospero-Garcia O, Wheeler DW, Wagaman PC, Lerner DL, Fox HS, Whalen LR, Bloom FE, Elder JH, Henriksen SJ (1996). Neurologic dysfunctions caused by a molecular clone of feline immunodeficiency virus, FIV-PPR. J NeuroVirol 2: 388–396.

    Article  CAS  PubMed  Google Scholar 

  • Power C, Kong PA, Crawford TO, Wesselingh S, Glass JD, McArthur JC, Trapp BD (1993). Cerebral white matter changes in acquired immunodeficiency syndrome dementia: alterations of the blood-brain barrier. Ann Neurol 34: 339–350.

    Article  CAS  PubMed  Google Scholar 

  • Prospero-Garcia O, Gold LH, Fox HS, Polis I, Koob GF, Bloom FE, Henriksen SJ (1996). Microglia-passaged simian immunodeficiency virus induces neurophysiological abnormalities in monkeys. Proc Natl Acad Sci U S A 93: 14158–14163.

    Article  CAS  PubMed  Google Scholar 

  • Prospero-Garcia O, Herold N, Phillips T, Elder J, Bloom FE, Henriksen SJ (1994a). Sleep patterns are disturbed in cats infected with feline immunodeficiency virus. Proc Natl Acad Sci U S A. 91: 12947–12951.

    Article  CAS  PubMed  Google Scholar 

  • Prospero-Garcia O, Herold N, Waters A, Phillips T, Elder J, Henriksen SJ (1994b). Intraventricular administration of a FIV-envelope protein induces sleep architecture changes in rats. Brain Res 659: 254–258.

    Article  CAS  PubMed  Google Scholar 

  • Prospero-Garcia O, Huitron-Resendiz S, Casalman SC, Sanchez-Alavez M, Diaz-Ruiz O, Navarro L, Lerner DL, Phillips TR, Elder JH, Henriksen SJ (1999). Feline immunodeficiency virus envelope protein (FIVgp120) causes electrophysiological alterations in rats. Brain Res 836: 203–209.

    Article  CAS  PubMed  Google Scholar 

  • Raymond LA, Wallace D, Berman NE, Marcario J, Foresman L, Joag SV, Raghavan R, Narayan O, Cheney PD (1998). Auditory brainstem responses in a Rhesus Macaque model of neuro-AIDS. J NeuroVirol 4: 512–520.

    Article  CAS  PubMed  Google Scholar 

  • Reyes MG, Faraldi F, Senseng CS, Flowers C, Fariello R (1991). Nigral degeneration in acquired immune deficiency syndrome (AIDS). Acta Neuropathol (Berl) 82: 39–44.

    Article  CAS  Google Scholar 

  • Reyes-Contreras L, Silva-Rojas A, Ysunza-Rivera A, Jimenez-Ruiz G, Berruecos-Villalobos P, Romo-Gutierrez G (2002). Brainstem auditory evoked response in HIV-infected patients with and without AIDS. Arch Med Res 33: 25–28.

    Article  PubMed  Google Scholar 

  • Ricaurte GA, Guillery RW, Seiden LS, Schuster CR, Moore RY (1982). Dopamine nerve terminal degeneration produced by high doses of methylamphetamine in the rat brain. Brain Res 235: 93–103.

    Article  CAS  PubMed  Google Scholar 

  • Ricaurte GA, McCann UD (1992). Neurotoxic amphetamine analogues: effects in monkeys and implications for humans. Ann N Y Acad Sci 648: 371–382.

    Article  CAS  PubMed  Google Scholar 

  • Rotheram-Borus MJ, Cajetan Luna G, Marotta T, Kelly H (1994). Going nowhere fast: Methamphetamine use and HIV infection. NIDA Res Monogr 143: 155–182.

    CAS  PubMed  Google Scholar 

  • Sahakian BJ, Elliott R, Low N, Mehta M, Clark RT, Pozniak AL (1995). Neuropsychological deficits in tests of executive function in asymptomatic and symptomatic HIV-1 seropositive men. Psychol Med 25: 1233–1246.

    Article  CAS  PubMed  Google Scholar 

  • Sardar AM, Czudek C, Reynolds GP (1996). Dopamine deficits in the brain: the neurochemical basis of parkinsonian symptoms in AIDS. Neuroreport 7: 910–912.

    Article  CAS  PubMed  Google Scholar 

  • Semple SJ, Strathdee SA, Zians J, Patterson TL (2009). Sexual risk behavior associated with co-administration of methamphetamine and other drugs in a sample of HIV-positive men who have sex with men. Am J Addict 18: 65–72.

    Article  PubMed  Google Scholar 

  • Smith T, Jakobsen J, Gaub J, Helweg-Larsen S, Trojaborg W (1988). Clinical and electrophysiological studies of human immunodeficiency virus-seropositive men without AIDS. Ann Neurol 23: 295–297.

    Article  CAS  PubMed  Google Scholar 

  • Taffe MA, Davis SA, Yuan J, Schroeder R, Hatzidimitriou G, Parsons LH, Ricaurte GA, Gold LH (2002). Cognitive performance of MDMA-treated rhesus monkeys: sensitivity to serotonergic challenge. Neuropsychopharmacology 27: 993–1005.

    Article  CAS  PubMed  Google Scholar 

  • Theodore S, Stolberg S, Cass WA, Maragos WF (2006). Human immunodeficiency virus-1 protein tat and methamphetamine interactions. Ann N Y Acad Sci 1074: 178–190.

    Article  CAS  PubMed  Google Scholar 

  • Theodore S, Cass WA, Nath A, Maragos WF (2007). Progress in understanding basal ganglia dysfunction as a common target for methamphetamine abuse and HIV-1 neurodegeneration. Curr HIV Res 5: 301–313.

    Article  CAS  PubMed  Google Scholar 

  • Vigliano P, Boffi P, Bonassi E, Gandione M, Marotta C, Raino E, Russo R, Rigardetto R (2000). Neurophysiologic exploration: a reliable tool in HIV-1 encephalopathy diagnosis in children. Panminerva Med 42: 267–272.

    CAS  PubMed  Google Scholar 

  • Vigliano P, Russo R, Arfelli P, Boffi P, Bonassi E, Gandione M, Raino E, Tovo PA, Taglianti MV, Rigardetto R (1997). Diagnostic value of multimodal evoked potentials in HIV-1 infected children. Neurophysiol Clin 27: 283–292.

    Article  CAS  PubMed  Google Scholar 

  • Wagner GC, Ricaurte GA, Seiden LS, Schuster CR, Miller RJ, Westley J (1980). Long-lasting depletions of striatal dopamine and loss of dopamine uptake sites following repeated administration of methamphetamine. Brain Res 181: 151–160.

    Article  CAS  PubMed  Google Scholar 

  • Wiley CA, Masliah E, Morey M, Lemere C, DeTeresa R, Grafe M, Hansen L, Terry R (1991). Neocortical damage during HIV infection. Ann Neurol 29: 651–657.

    Article  CAS  PubMed  Google Scholar 

  • Wolfson T, Velin R, Marcotte TD, Hesselink JR, Jernigan TL, Chandler J, Wallace M, Abramson I, THE HNRC GROUP (1995). The HNRC 500—neuropsychology of HIV infection at different disease stages. HIV Neurobehavioral Research Center. J Int Neuropsychol Soc 1: 231–251.

    Article  Google Scholar 

  • Woolverton WL, Ricaurte GA, Forno LS, Seiden LS (1989). Long-term effects of chronic methamphetamine administration in rhesus monkeys. Brain Res 486: 73–78.

    Article  CAS  PubMed  Google Scholar 

  • Yu N, Billaud JN, Phillips TR (1998). Effects of feline immunodeficiency virus on astrocyte glutamate uptake: implications for lentivirus-induced central nervous system diseases. Proc Natl Acad Sci U S A 95: 2624–2629.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Tom R. Phillips.

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This work is supported by NIH (P01 DA12444-03/SJH and R24 RR10712/TRP).

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Huitron-Resendiz, S., Henriksen, S.J., Barr, M.C. et al. Methamphetamine and lentivirus interactions: Reciprocal enhancement of central nervous system disease. Journal of NeuroVirology 16, 268–278 (2010). https://doi.org/10.3109/13550284.2010.497807

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