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Methamphetamine enhances cell-associated feline immunodeficiency virus replication in astrocytes

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Abstract

Human immunodeficiency virus (HIV) infection among substance abusers is on the rise worldwide. Psychostimulants, and in particular methamphetamine (METH), have detrimental effects on the immune system as well as causing a progressive neurodegeneration, similar to HIV infection. Many Lentivirinae, including feline immunodeficiency virus (FIV), penetrate into the central nervous system early in the course of infection with astrocytes serving as a reservoir of chronic brain infection. We demonstrate that the FIV-Maryland isolate infects feline primary and cell line (G355-5)-cultured astrocytes only under cell-associated conditions. Infected astrocytes yielded a new astrocytotropic isolate, capable of cell-free infection (termed FIV-MD-A). This isolate contained four amino acid substitutions in the envelope polyprotein resulting in a change in net charge as compared to FIV-MD. Infection for both isolates was dependent upon a functional astrocyte CXCR4 receptor. Methamphetamine increased significantly FIV replication in feline astrocytes for cell-associated infection only, with no effect on peripheral blood mononuclear cells or astrocytes infected with FIV-MD-A. This viral replication was related to proviral copy number, suggesting the effect of METH is at the viral entry or integration into host genome levels, but not at the translational level. Thus, lentiviral infection of the brain in the presence of the psychostimulant METH may result in enhanced astrocyte viral replication, producing a more rapid and increased brain viral load.

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References

  • Asanuma M, Hayashi T, Ordonez SV, Ogawa N, Cadet JL (2000). Direct interactions of methamphetamine with the nucleus. Brain Res Mol Brain Res 80: 237–243.

    Article  CAS  PubMed  Google Scholar 

  • Bagasra O, Pomerantz RJ (1993a). Human immunodeficiency virus type I provirus is demonstrated in peripheral blood monocytes in vivo: a study utilizing an in situ polymerase chain reaction. AIDS Res Hum Retroviruses 9: 69–76.

    Article  CAS  PubMed  Google Scholar 

  • Bagasra O, Pomerantz RJ (1993b). The role of CD8-positive lymphocytes in the control of HIV-1 infection of peripheral blood mononuclear cells. Immunol Lett 35: 83–92.

    Article  CAS  PubMed  Google Scholar 

  • Belman AL (1994). HIV-1-associated CNS disease in infants and children. Res Publ Assoc Res Nerv Ment Dis 72: 289–310.

    CAS  PubMed  Google Scholar 

  • Billaud JN, Selway D, Yu N, Phillips TR (2000). Replication rate of feline immunodeficiency virus in astrocytes is envelope dependent: implications for glutamate uptake. Virology 266: 180–188.

    Article  CAS  PubMed  Google Scholar 

  • Blumberg BM, Gelbard HA, Epstein LG (1994). HIV-1 infection of the developing nervous system: central role of astrocytes in pathogenesis. Virus Res 32: 253–267.

    Article  CAS  PubMed  Google Scholar 

  • Boutet A, Salim H, Taoufik Y, Lledo PM, Vincent JD, Delfraissy JF, Tardieu M (2001). Isolated human astrocytes are not susceptible to infection by M- and T-tropic HIV-1 strains despite functional expression of the chemokine receptors CCR5 and CXCR4. Glia 34: 165–177.

    Article  CAS  PubMed  Google Scholar 

  • Brack-Werner R (1999a). Astrocytes: HIV cellular reservoirs and important participants in neuropathogenesis. AIDS 13: 1–22.

    Article  CAS  PubMed  Google Scholar 

  • Brack-Werner R (1999b). Replication of HIV-1 in human astrocytes. NeuroAIDS 2: www.sciencemag.org/NAIDS.

  • Cadet JL, Jayanthi S, McCoy MT, Vawter M, Ladenheim B (2001). Temporal profiling of methamphetamine-induced changes in gene expression in the mouse brain: evidence from cDNA array. Synapse 41: 40–48.

    Article  CAS  PubMed  Google Scholar 

  • Centers for Disease Control (1995). Increasing morbidity and mortality associated with abuse of methamphetamine—United States, 1991–1994. MMWR Morb Mort Wkly Rep 44: 882–886.

    Google Scholar 

  • Chapman DE, Hanson GR, Kesner RP, Keefe KA (2001). Long-term changes in basal ganglia function after a neurotoxic regimen of methamphetamine. J Pharmacol Exp Ther 296: 520–527.

    CAS  PubMed  Google Scholar 

  • Cole SW, Jamieson BD, Zack JA (1999). cAMP up-regulates cell surface expression of lymphocyte CXCR4: implications for chemotaxis and HIV-1 infection. J Immunol 162: 1392–1400.

    CAS  PubMed  Google Scholar 

  • Cole SW, Korin YD, Fahey JL, Zack JA (1998). Norepinephrine accelerates HIV replication via protein kinase A-dependent effects on cytokine production. J Immunol 161: 610–616.

    CAS  PubMed  Google Scholar 

  • Cubells JF, Rayport S, Rajendran G, Sulzer D (1994). Methamphetamine neurotoxicity involves vacuolation of endocytic organelles and dopamine-dependent intracellular oxidative stress. J Neurosci 14: 2260–2271.

    CAS  PubMed  Google Scholar 

  • de Parseval A, Elder JH (2001). Binding of recombinant feline immunodeficiency virus surface glycoprotein to feline cells: role of CXCR4, cell-surface heparans, and an unidentified non-CXCR4 receptor. J Virol 75: 4528–4539.

    Article  PubMed Central  PubMed  Google Scholar 

  • Dow SW, Dreitz MJ, Hoover EA (1992). Feline immunodeficiency virus neurotropism: evidence that astrocytes and microglia are the primary target cells. Vet Immunol Immunopathol 35: 23–35.

    Article  CAS  PubMed  Google Scholar 

  • Driscoll RC, Barr FS, Gragg BJ, Moore GW (1971). Determination of therapeutic blood levels of methamphetamine and pentobarbital by GC. J Pharm Sci 60: 1492–1495.

    Article  CAS  PubMed  Google Scholar 

  • Ellison G, Switzer RC (1993). Dissimilar patterns of degeneration in brain following four different addictive stimulants. Neuroreport 5: 17–20.

    Article  CAS  PubMed  Google Scholar 

  • Epstein LG, Gelbard HA (1999). HIV-1-induced neuronal injury in the developing brain. J Leukoc Biol 65: 453–457.

    CAS  PubMed  Google Scholar 

  • Gavrilin MA, Deucher MF, Boeckman F, Kolattukudy PE (2000). Monocyte chemotactic protein 1 upregulates IL-1beta expression in human monocytes. Biochem Biophys Res Commun 277: 37–42.

    Article  CAS  PubMed  Google Scholar 

  • Glass JD, Johnson RT (1996). Human immunodeficiency virus and the brain. Annu Rev Neurosci 19: 1–26.

    Article  CAS  PubMed  Google Scholar 

  • Gorman M (1996). Speed use and HIV transmission. Focus 11: 4–6.

    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 Neuro Virol 4: 415–425.

    CAS  Google Scholar 

  • Hohdatsu T, Hirabayashi H, Motokawa K, Koyama H (1996). Comparative study of the cell tropism of feline immunodeficiency virus isolates of subtypes A, B and D classified on the basis of the env gene V3-V5 sequence. J Gen Virol 77: 93–100.

    Article  CAS  PubMed  Google Scholar 

  • House RV, Thomas PT, Bhargava HN (1994). Comparison of immune functional parameters following in vitro exposure to natural and synthetic amphetamines. Immunopharmacol Immunotoxicol 16: 1–21.

    Article  CAS  PubMed  Google Scholar 

  • Kaul M, Garden GA, Lipton SA (2001). Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410: 988–994.

    Article  CAS  PubMed  Google Scholar 

  • Koirala TR, Sharma S, Morikawa S, Ishida T (2000). Expression of CXCR4 in the brain of feline immunodeficiency virus infected cat. Indian J Pathol Microbiol 43: 285–290.

    CAS  PubMed  Google Scholar 

  • Kolchinsky P, Mirzabekov T, Farzan M, Kiprilov E, Cayabyab M, Mooney LJ, Choe H, Sodroski J (1999). Actaptation of a CCR5-using, primary human immunodeficiency virus type 1 isolate for CD4-independent replication. J Virol 73: 8120–8126.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Krebs FC, Mehrens D, Pomeroy S, Goodenow MM, Wigdahl B (1998). Human immunodeficiency virus type 1 long terminal repeat quasispecies differ in basal transcription and nuclear factor recruitment in human glial cells and lymphocytes. J Biomed Sci 5: 31–44.

    Article  CAS  PubMed  Google Scholar 

  • Lerner DL, Elder JH (2000). Expanded host cell tropism and cytopathic properties of feline immunodeficiency virus strain PPR subsequent to passage through interleukin-2-independent T cells. J Virol 74: 1854–1863.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Levine MS, Hull CD, Garcia-Rill E, Erinoff L, Buchwald NA, Heller A (1980). Long-term decreases in spontaneous firing of caudate neurons induced by amphetamine in cats. Brain Res 194: 263–268.

    Article  CAS  PubMed  Google Scholar 

  • Mack M, Kleinschmidt A, Bruhl H, Klier C, Nelson PJ, Cihak J, Plachy J, Stangassinge M, Erfle V, Schlondorff D (2000). Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection. Nat Med 6: 769–775.

    Article  CAS  PubMed  Google Scholar 

  • McArthur J, Grant I (1998). HIV Neurocognitive Disorders. In: The Neurology of AIDS. Gendelman HE, Lipton SA, Epstein L, Swindells S (eds). New York, Chapman & Hall, pp 499–523.

    Google Scholar 

  • McLeman ER, Warsh JJ, Ang L, Li PP, Kalasinsky KS, Ross BM, Tong J, Schmunk G, Adams V, Kish SJ (2000). The human nucleus accumbens is highly susceptible to G protein down-regulation by methamphetamine and heroin. J Neurochem 74: 2120–2126.

    Article  CAS  PubMed  Google Scholar 

  • Nakagaki K, Nakagaki K, Takahashi K, Schols D, de Clercq E, Tabira T (2001). CXCR4 is the primary receptor for feline immunodeficiency virus in astrocytes. J Neuro Virol 7: 487–492.

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Peterson PK, Gekker G, Schut R, Hu S, Balfour HH Jr, Chao CC (1993). Enhancement of HIV-1 replication by opiates and cocaine: the cytokine connection. Adv Exp Med Biol 335: 181–188.

    Article  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 

  • Podell M, Oglesbee M, Mathes L, Krakowka S, Olmstead R, Lafrado L (1993). AIDS-associated encephalopathy with experimental feline immunodeficiency virus infection. J Acquir Immune Defic Syndr 6: 758–771.

    CAS  PubMed  Google Scholar 

  • Podell M, Hayes K, Oglesbee M, Mathes L (1997). Progressive encephalopathy associated with CD4/CD8 inversion in adult FIV-infected cats. J Acquir Immune Defic Syndr Hum Betrovirol 15: 332–340.

    Article  CAS  Google Scholar 

  • Podell M, March PA, Buck WR, Mathes LE (2000). The feline model of neuroAIDS: understanding the progression towards AIDS dementia. J Psychopharmacol 14: 205–213.

    Article  CAS  PubMed  Google Scholar 

  • Podell M, Maruyama K, Smith M, Hayes KA, Buck WR, Ruehlmann DS, Mathes LE (1999). Frontal lobe neuronal injury correlates to altered function in FIV-infected cats. J Acquir Immune Defic Syndr 22: 10–18.

    Article  CAS  PubMed  Google Scholar 

  • Podell M, Buck WR, Hayes KA, Gavrilin MA, Mathes LE (2001). Animal models of retroviral encephalopathies: Feline model. In: Current Protocols in Neuroscience. Crawley JN, Gerfen CR, Rogawski MA, Sibley DR, Skolnick P, Wray S (eds). New York, John Wiley & Sons, Suppl 17: 9.9.1–9.9.30.

    Google Scholar 

  • Reeves JD, Hibbitts S, Simmons G, McKnight A, Azevedo-Pereira JM, Moniz-Pereira, Clapham PR (1999). Primary human immunodeficiency virus type 2 (HIV-2) isolates infect CD4-negative cells via CCR5 and CXCR4: comparison with HIV-1 and simian immunodeficiency virus and relevance to cell tropism in vivo. J Virol 73: 7795–7804.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Richardson J, Pancino G, Merat R, Leste-Lasserre T, Moraillon A, Schneider-Mergener J, Alizon M, Sonigo P, Heveker N (1999). Sharedusage of the chemokine receptor CXCR4 by primary and laboratory-adapted strains of feline immunodeficiency virus. J Virol 73: 3661–3671.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schmued LC, Bowyer JF (1997). Methamphetamine exposure can produce neuronal degeneration in mouse hippocampal remnants. Brain Bes 759: 135–140.

    Article  CAS  Google Scholar 

  • Speck RF, Esser U, Penn ML, Eckstein DA, Pulliam L, Chan SY, Goldsmith MA (1999). A trans-receptor mechanism for infection of CD4-negative cells by human immunodeficiency virus type 1. Curr Biol 9: 547–550.

    Article  CAS  PubMed  Google Scholar 

  • Squinto SP, Mondal D, Block AL, Prakash O (1990). Morphine-induced transactivation of HIV-1 LTR in human neuroblastoma cells. AIDS Bes Hum Retroviruses 6: 1163–1168.

    Article  CAS  Google Scholar 

  • Stewart JL, Meeker JE (1997). Fetal and infant deaths associated with maternal methamphetamine abuse. J Anal Toxicol 21: 515–517.

    Article  CAS  PubMed  Google Scholar 

  • Vahlenkamp TW, de Ronde A, Schuurman NN, van Vliet AL, van Drunen J, Horzinek MC, Egberink HF (1999). Envelope gene sequences encoding variable regions 3 and 4 are involved in macrophage tropism of feline immunodeficiency virus. J Gen Virol 80: 2639–2646.

    CAS  PubMed  Google Scholar 

  • Verschoor EJ, Boven LA, Blaak H, van Vliet AL, Horzinek MC, de Ronde A (1995). A single mutation within the V3 envelope neutralization domain of feline immunodeficiency virus determines its tropism for CRFK cells. J Virol 69: 4752–4757.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Willett BJ, Hosie MJ (1999). The role of the chemokine receptor CXCR4 in infection with feline immunodeficiency virus. Mol Membr Biol 16: 67–72.

    Article  CAS  PubMed  Google Scholar 

  • World Health Organization (2000). Report on global surveillance of epidemic-prone infectious disease: HIV and AIDS. Geneva, Switzerland, WHO Information Office.

    Google Scholar 

  • Wu DT, Woodman SE, Weiss JM, McManus CM, D’Aversa TG, Hesselgesser J, Major EO, Nath A, Berman JW (2000). Mechanisms of leukocyte trafficking into the CNS. J Neuro Virol 6 (Suppl 1): S82–85.

    CAS  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 USA 95: 2624–2629.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Veterinary Clinical Sciences, College of Veterinary Medicine, The Ohio State University, 601 Tharp Street, 43230, Columbus, OH, USA

    Mikhail A. Gavrilin & Michael Podell

  2. Veterinary Biosciences, College of Veterinary Medicine, The Ohio State University, Columbus, Ohio, USA

    Lawrence E. Mathes

  3. Center for Retrovirus Research, Comprehensive Cancer Center, The Ohio State University, Columbus, Ohio, USA

    Mikhail A. Gavrilin, Lawrence E. Mathes & Michael Podell

  4. Department of Neuroscience, College of Medicine, The Ohio State University, Columbus, Ohio, USA

    Michael Podell

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  1. Mikhail A. Gavrilin
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  2. Lawrence E. Mathes
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  3. Michael Podell
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Correspondence to Michael Podell.

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Funded in part by PHS grant R01-DA13815-01 (MP).

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Gavrilin, M.A., Mathes, L.E. & Podell, M. Methamphetamine enhances cell-associated feline immunodeficiency virus replication in astrocytes. Journal of NeuroVirology 8, 240–249 (2002). https://doi.org/10.1080/13550280290049660

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  • DOI: https://doi.org/10.1080/13550280290049660

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