Molecular Neurobiology

, Volume 54, Issue 8, pp 5855–5867 | Cite as

Role of Autophagy in HIV Pathogenesis and Drug Abuse

  • Lu Cao
  • Alexey Glazyrin
  • Santosh Kumar
  • Anil Kumar


Autophagy is a highly regulated process in which excessive cytoplasmic materials are captured and degraded during deprivation conditions. The unique nature of autophagy that clears invasive microorganisms has made it an important cellular defense mechanism in a variety of clinical situations. In recent years, it has become increasingly clear that autophagy is extensively involved in the pathology of HIV-1. To ensure survival of the virus, HIV-1 viral proteins modulate and utilize the autophagy pathway so that biosynthesis of the virus is maximized. At the same time, the abuse of illicit drugs such as methamphetamine, cocaine, morphine, and alcohol is thought to be a significant risk factor for the acquirement and progression of HIV-1. During drug-induced toxicity, autophagic activity has been proved to be altered in various cell types. Here, we review the current literature on the interaction between autophagy, HIV-1, and drug abuse and discuss the complex role of autophagy during HIV-1 pathogenesis in co-exposure to illicit drugs.


HIV-1 Autophagy Alcohol Methamphetamine Morphine 


Compliance with Ethical Standards

Grant Support

This work was supported by grants from the National Institute on Alcohol Abuse and Alcoholism AA020806 (AK) and AA022063 (SK).


  1. 1.
    Cuervo AM (2004) Autophagy: in sickness and in health. Trends Cell Biol 14(2):70–77. doi: 10.1016/j.tcb.2003.12.002 PubMedCrossRefGoogle Scholar
  2. 2.
    Klionsky DJ (2005) The molecular machinery of autophagy: unanswered questions. J Cell Sci 118(Pt 1):7–18. doi: 10.1242/jcs.01620 PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Peracchio C, Alabiso O, Valente G, Isidoro C (2012) Involvement of autophagy in ovarian cancer: a working hypothesis. J Ovarian Res 5(1):22. doi: 10.1186/1757-2215-5-22 PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Feng Y, He D, Yao Z, Klionsky DJ (2014) The machinery of macroautophagy. Cell Res 24(1):24–41. doi: 10.1038/cr.2013.168 PubMedCrossRefGoogle Scholar
  5. 5.
    Kroemer G, Marino G, Levine B (2010) Autophagy and the integrated stress response. Mol Cell 40(2):280–293. doi: 10.1016/j.molcel.2010.09.023 PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Yang ZJ, Chee CE, Huang S, Sinicrope FA (2011) The role of autophagy in cancer: therapeutic implications. Mol Cancer Ther 10(9):1533–1541. doi: 10.1158/1535-7163.MCT-11-0047 PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Campoy E, Colombo MI (2009) Autophagy in intracellular bacterial infection. Biochim Biophys Acta 1793(9):1465–1477. doi: 10.1016/j.bbamcr.2009.03.003 PubMedCrossRefGoogle Scholar
  8. 8.
    Nixon RA (2013) The role of autophagy in neurodegenerative disease. Nat Med 19(8):983–997. doi: 10.1038/nm.3232 PubMedCrossRefGoogle Scholar
  9. 9.
    Ashford TP, Porter KR (1962) Cytoplasmic components in hepatic cell lysosomes. J Cell Biol 12:198–202PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Deretic V, Saitoh T, Akira S (2013) Autophagy in infection, inflammation and immunity. Nat Rev Immunol 13(10):722–737. doi: 10.1038/nri3532 PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Deretic V, Jiang S, Dupont N (2012) Autophagy intersections with conventional and unconventional secretion in tissue development, remodeling and inflammation. Trends Cell Biol 22(8):397–406. doi: 10.1016/j.tcb.2012.04.008 PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Levine B, Mizushima N, Virgin HW (2011) Autophagy in immunity and inflammation. Nature 469(7330):323–335. doi: 10.1038/nature09782 PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Espert L, Varbanov M, Robert-Hebmann V, Sagnier S, Robbins I, Sanchez F, Lafont V, Biard-Piechaczyk M (2009) Differential role of autophagy in CD4 T cells and macrophages during X4 and R5 HIV-1 infection. PLoS One 4(6):e5787. doi: 10.1371/journal.pone.0005787 PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Espert L, Denizot M, Grimaldi M, Robert-Hebmann V, Gay B, Varbanov M, Codogno P, Biard-Piechaczyk M (2006) Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4. J Clin Invest 116(8):2161–2172. doi: 10.1172/JCI26185 PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Manceur AP, Driscoll BD, Sun W, Audet J (2009) Selective enhancement of the uptake and bioactivity of a TAT-conjugated peptide inhibitor of glycogen synthase kinase-3. Mol Ther J Am Soc Gene Ther 17(3):500–507. doi: 10.1038/mt.2008.271 CrossRefGoogle Scholar
  16. 16.
    Kyei GB, Dinkins C, Davis AS, Roberts E, Singh SB, Dong C, Wu L, Kominami E, Ueno T, Yamamoto A, Federico M, Panganiban A, Vergne I, Deretic V (2009) Autophagy pathway intersects with HIV-1 biosynthesis and regulates viral yields in macrophages. J Cell Biol 186(2):255–268. doi: 10.1083/jcb.200903070 PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Mizushima N (2007) Autophagy: process and function. Genes Dev 21(22):2861–2873. doi: 10.1101/gad.1599207 PubMedCrossRefGoogle Scholar
  18. 18.
    Mehrpour M, Codogno P (2011) Drug enhanced autophagy to fight mutant protein overload. J Hepatol 54(5):1066–1068. doi: 10.1016/j.jhep.2010.11.032 PubMedCrossRefGoogle Scholar
  19. 19.
    Tooze SA, Yoshimori T (2010) The origin of the autophagosomal membrane. Nat Cell Biol 12(9):831–835. doi: 10.1038/ncb0910-831 PubMedCrossRefGoogle Scholar
  20. 20.
    Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B (2005) Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122(6):927–939. doi: 10.1016/j.cell.2005.07.002 PubMedCrossRefGoogle Scholar
  21. 21.
    Geng J, Klionsky DJ (2008) The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. 'Protein modifications: beyond the usual suspects’ review series. EMBO Rep 9(9):859–864. doi: 10.1038/embor.2008.163 PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Deretic V, Delgado M, Vergne I, Master S, De Haro S, Ponpuak M, Singh S (2009) Autophagy in immunity against mycobacterium tuberculosis: a model system to dissect immunological roles of autophagy. Curr Top Microbiol Immunol 335:169–188. doi: 10.1007/978-3-642-00302-8_8 PubMedPubMedCentralGoogle Scholar
  23. 23.
    Denizot M, Varbanov M, Espert L, Robert-Hebmann V, Sagnier S, Garcia E, Curriu M, Mamoun R, Blanco J, Biard-Piechaczyk M (2008) HIV-1 gp41 fusogenic function triggers autophagy in uninfected cells. Autophagy 4(8):998–1008PubMedCrossRefGoogle Scholar
  24. 24.
    Zhou D, Masliah E, Spector SA (2011) Autophagy is increased in postmortem brains of persons with HIV-1-associated encephalitis. J Infect Dis 203(11):1647–1657. doi: 10.1093/infdis/jir163 PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Spector SA, Zhou D (2008) Autophagy: an overlooked mechanism of HIV-1 pathogenesis and neuroAIDS? Autophagy 4(5):704–706PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Meng L, Zhang Z, Xu K, Qi G (2013) HIV-1 gp120 induces autophagy in cardiomyocytes via the NMDA receptor. Int J Cardiol 167(6):2517–2523. doi: 10.1016/j.ijcard.2012.06.067 PubMedCrossRefGoogle Scholar
  27. 27.
    Van Grol J, Subauste C, Andrade RM, Fujinaga K, Nelson J, Subauste CS (2010) HIV-1 inhibits autophagy in bystander macrophage/monocytic cells through Src-Akt and STAT3. PLoS One 5(7):e11733. doi: 10.1371/journal.pone.0011733 PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Li JC, Au KY, Fang JW, Yim HC, Chow KH, Ho PL, Lau AS (2011) HIV-1 trans-activator protein dysregulates IFN-gamma signaling and contributes to the suppression of autophagy induction. AIDS 25(1):15–25. doi: 10.1097/QAD.0b013e328340fd61 PubMedCrossRefGoogle Scholar
  29. 29.
    Sagnier S, Daussy CF, Borel S, Robert-Hebmann V, Faure M, Blanchet FP, Beaumelle B, Biard-Piechaczyk M, Espert L (2015) Autophagy restricts HIV-1 infection by selectively degrading Tat in CD4+ T lymphocytes. J Virol 89(1):615–625. doi: 10.1128/JVI.02174-14 PubMedCrossRefGoogle Scholar
  30. 30.
    Bruno AP, De Simone FI, Iorio V, De Marco M, Khalili K, Sariyer IK, Capunzo M, Nori SL, Rosati A (2014) HIV-1 Tat protein induces glial cell autophagy through enhancement of BAG3 protein levels. Cell Cycle 13(23):3640–3644. doi: 10.4161/15384101.2014.952959 PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Fields J, Dumaop W, Eleuteri S, Campos S, Serger E, Trejo M, Kosberg K, Adame A, Spencer B, Rockenstein E, He JJ, Masliah E (2015) HIV-1 Tat alters neuronal autophagy by modulating autophagosome fusion to the lysosome: implications for HIV-associated neurocognitive disorders. J Neurosci 35(5):1921–1938. doi: 10.1523/JNEUROSCI.3207-14.2015 PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Gregoire IP, Richetta C, Meyniel-Schicklin L, Borel S, Pradezynski F, Diaz O, Deloire A, Azocar O, Baguet J, Le Breton M, Mangeot PE, Navratil V, Joubert PE, Flacher M, Vidalain PO, Andre P, Lotteau V, Biard-Piechaczyk M, Rabourdin-Combe C, Faure M (2011) IRGM is a common target of RNA viruses that subvert the autophagy network. PLoS Pathog 7(12):e1002422. doi: 10.1371/journal.ppat.1002422 PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Beaupere C, Garcia M, Larghero J, Feve B, Capeau J, Lagathu C (2015) The HIV proteins Tat and Nef promote human bone marrow mesenchymal stem cell senescence and alter osteoblastic differentiation. Aging Cell 14(4):534–546. doi: 10.1111/acel.12308 PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Campbell GR, Rawat P, Bruckman RS, Spector SA (2015) Human immunodeficiency virus type 1 Nef inhibits autophagy through transcription factor EB sequestration. PLoS Pathog 11(6):e1005018. doi: 10.1371/journal.ppat.1005018 PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Saribas AS, Khalili K, Sariyer IK (2015) Dysregulation of autophagy by HIV-1 Nef in human astrocytes. Cell Cycle 14(18):2899–2904. doi: 10.1080/15384101.2015.1069927 PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Sardo L, Iordanskiy S, Klase Z, Kashanchi F (2015) HIV-1 Nef blocks autophagy in human astrocytes. Cell Cycle 14(24):3781–3782. doi: 10.1080/15384101.2015.1105700 PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Blanchet FP, Moris A, Nikolic DS, Lehmann M, Cardinaud S, Stalder R, Garcia E, Dinkins C, Leuba F, Wu L, Schwartz O, Deretic V, Piguet V (2010) Human immunodeficiency virus-1 inhibition of immunoamphisomes in dendritic cells impairs early innate and adaptive immune responses. Immunity 32(5):654–669. doi: 10.1016/j.immuni.2010.04.011 PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Mehla R, Chauhan A (2015) HIV-1 differentially modulates autophagy in neurons and astrocytes. J Neuroimmunol 285:106–118. doi: 10.1016/j.jneuroim.2015.06.001 PubMedCrossRefGoogle Scholar
  39. 39.
    Mothobi NZ, Brew BJ (2012) Neurocognitive dysfunction in the highly active antiretroviral therapy era. Curr Opin Infect Dis 25(1):4–9. doi: 10.1097/QCO.0b013e32834ef586 PubMedCrossRefGoogle Scholar
  40. 40.
    Rumbaugh JA, Steiner J, Sacktor N, Nath A (2008) Developing neuroprotective strategies for treatment of HIV-associated neurocognitive dysfunction. Futur HIV Ther 2(3):271–280. doi: 10.2217/17469600.2.3.271 PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Gresele P, Falcinelli E, Sebastiano M, Baldelli F (2012) Endothelial and platelet function alterations in HIV-infected patients. Thromb Res 129(3):301–308. doi: 10.1016/j.thromres.2011.11.022 PubMedCrossRefGoogle Scholar
  42. 42.
    Kovari H, Weber R (2011) Influence of antiretroviral therapy on liver disease. Curr Opin HIV AIDS 6(4):272–277. doi: 10.1097/COH.0b013e3283473405 PubMedCrossRefGoogle Scholar
  43. 43.
    Calza L (2012) Renal toxicity associated with antiretroviral therapy. HIV clin Trials 13(4):189–211. doi: 10.1310/hct1304-189 PubMedCrossRefGoogle Scholar
  44. 44.
    Bertrand L, Toborek M (2015) Dysregulation of endoplasmic reticulum stress and autophagic responses by the antiretroviral drug efavirenz. Mol Pharmacol 88(2):304–315. doi: 10.1124/mol.115.098590 PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Apostolova N, Gomez-Sucerquia LJ, Gortat A, Blas-Garcia A, Esplugues JV (2011) Compromising mitochondrial function with the antiretroviral drug efavirenz induces cell survival-promoting autophagy. Hepatology 54(3):1009–1019. doi: 10.1002/hep.24459 PubMedCrossRefGoogle Scholar
  46. 46.
    Gibellini L, De Biasi S, Pinti M, Nasi M, Riccio M, Carnevale G, Cavallini GM, Sala de Oyanguren FJ, O'Connor JE, Mussini C, De Pol A, Cossarizza A (2012) The protease inhibitor atazanavir triggers autophagy and mitophagy in human preadipocytes. AIDS 26(16):2017–2026. doi: 10.1097/QAD.0b013e328359b8be PubMedCrossRefGoogle Scholar
  47. 47.
    McLean K, VanDeVen NA, Sorenson DR, Daudi S, Liu JR (2009) The HIV protease inhibitor saquinavir induces endoplasmic reticulum stress, autophagy, and apoptosis in ovarian cancer cells. Gynecol Oncol 112(3):623–630. doi: 10.1016/j.ygyno.2008.11.028 PubMedCrossRefGoogle Scholar
  48. 48.
    Friedman H, Newton C, Klein TW (2003) Microbial infections, immunomodulation, and drugs of abuse. Clin Microbiol Rev 16(2):209–219PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Larsen KE, Fon EA, Hastings TG, Edwards RH, Sulzer D (2002) Methamphetamine-induced degeneration of dopaminergic neurons involves autophagy and upregulation of dopamine synthesis. J Neurosci 22(20):8951–8960PubMedGoogle Scholar
  50. 50.
    Castino R, Lazzeri G, Lenzi P, Bellio N, Follo C, Ferrucci M, Fornai F, Isidoro C (2008) Suppression of autophagy precipitates neuronal cell death following low doses of methamphetamine. J Neurochem 106(3):1426–1439. doi: 10.1111/j.1471-4159.2008.05488.x PubMedCrossRefGoogle Scholar
  51. 51.
    Lin M, Chandramani-Shivalingappa P, Jin H, Ghosh A, Anantharam V, Ali S, Kanthasamy AG, Kanthasamy A (2012) Methamphetamine-induced neurotoxicity linked to ubiquitin-proteasome system dysfunction and autophagy-related changes that can be modulated by protein kinase C delta in dopaminergic neuronal cells. Neuroscience 210:308–332. doi: 10.1016/j.neuroscience.2012.03.004 PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Ma J, Wan J, Meng J, Banerjee S, Ramakrishnan S, Roy S (2014) Methamphetamine induces autophagy as a pro-survival response against apoptotic endothelial cell death through the kappa opioid receptor. Cell Death Dis 5:e1099. doi: 10.1038/cddis.2014.64 PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Kongsuphol P, Mukda S, Nopparat C, Villarroel A, Govitrapong P (2009) Melatonin attenuates methamphetamine-induced deactivation of the mammalian target of rapamycin signaling to induce autophagy in SK-N-SH cells. J Pineal Res 46(2):199–206. doi: 10.1111/j.1600-079X.2008.00648.x PubMedCrossRefGoogle Scholar
  54. 54.
    Li Y, Hu Z, Chen B, Bu Q, Lu W, Deng Y, Zhu R, Shao X, Hou J, Zhao J, Li H, Zhang B, Huang Y, Lv L, Zhao Y, Cen X (2012) Taurine attenuates methamphetamine-induced autophagy and apoptosis in PC12 cells through mTOR signaling pathway. Toxicol Lett 215(1):1–7. doi: 10.1016/j.toxlet.2012.09.019 PubMedCrossRefGoogle Scholar
  55. 55.
    Levine B, Sinha S, Kroemer G (2008) Bcl-2 family members: dual regulators of apoptosis and autophagy. Autophagy 4(5):600–606PubMedCentralCrossRefGoogle Scholar
  56. 56.
    Takeuchi R, Hoshijima H, Nagasaka H, Chowdhury SA, Kikuchi H, Kanda Y, Kunii S, Kawase M, Sakagami H (2006) Induction of non-apoptotic cell death by morphinone in human promyelocytic leukemia HL-60 cells. Anticancer Res 26(5A):3343–3348PubMedGoogle Scholar
  57. 57.
    Zhao L, Zhu Y, Wang D, Chen M, Gao P, Xiao W, Rao G, Wang X, Jin H, Xu L, Sui N, Chen Q (2010) Morphine induces Beclin 1- and ATG5-dependent autophagy in human neuroblastoma SH-SY5Y cells and in the rat hippocampus. Autophagy 6(3):386–394PubMedCrossRefGoogle Scholar
  58. 58.
    Pan J, He L, Li X, Li M, Zhang X, Venesky J, Li Y, Peng Y (2016) Activating autophagy in hippocampal cells alleviates the morphine-induced memory impairment. Mol Neurobiol. doi: 10.1007/s12035-016-9735-3 Google Scholar
  59. 59.
    Cunha-Oliveira T, Rego AC, Garrido J, Borges F, Macedo T, Oliveira CR (2007) Street heroin induces mitochondrial dysfunction and apoptosis in rat cortical neurons. J Neurochem 101(2):543–554. doi: 10.1111/j.1471-4159.2006.04406.x PubMedCrossRefGoogle Scholar
  60. 60.
    Feng YM, Jia YF, Su LY, Wang D, Lv L, Xu L, Yao YG (2013) Decreased mitochondrial DNA copy number in the hippocampus and peripheral blood during opiate addiction is mediated by autophagy and can be salvaged by melatonin. Autophagy 9(9):1395–1406. doi: 10.4161/auto.25468 PubMedCrossRefGoogle Scholar
  61. 61.
    Wan J, Ma J, Anand V, Ramakrishnan S, Roy S (2015) Morphine potentiates LPS-induced autophagy initiation but inhibits autophagosomal maturation through distinct TLR4-dependent and independent pathways. Acta Physiol 214(2):189–199. doi: 10.1111/apha.12506 CrossRefGoogle Scholar
  62. 62.
    Cao L, Walker MP, Vaidya NK, Fu M, Kumar S, Kumar A (2015) Cocaine-mediated autophagy in astrocytes involves sigma 1 receptor, PI3K, mTOR, Atg5/7, Beclin-1 and induces type II programed cell death. Mol Neurobiol. doi: 10.1007/s12035-015-9377-x Google Scholar
  63. 63.
    Guo ML, Liao K, Periyasamy P, Yang L, Cai Y, Callen SE, Buch S (2015) Cocaine-mediated microglial activation involves the ER stress-autophagy axis. Autophagy 11(7):995–1009. doi: 10.1080/15548627.2015.1052205 PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Guha P, Harraz MM, Snyder SH (2016) Cocaine elicits autophagic cytotoxicity via a nitric oxide-GAPDH signaling cascade. Proc Natl Acad Sci U S A 113(5):1417–1422. doi: 10.1073/pnas.1524860113 PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Zakhari S, Li TK (2007) Determinants of alcohol use and abuse: impact of quantity and frequency patterns on liver disease. Hepatology 46(6):2032–2039. doi: 10.1002/hep.22010 PubMedCrossRefGoogle Scholar
  66. 66.
    Lindtner C, Scherer T, Zielinski E, Filatova N, Fasshauer M, Tonks NK, Puchowicz M, Buettner C (2013) Binge drinking induces whole-body insulin resistance by impairing hypothalamic insulin action. Sci Transl Med 5(170):170ra114. doi: 10.1126/scitranslmed.3005123 CrossRefGoogle Scholar
  67. 67.
    Manzo-Avalos S, Saavedra-Molina A (2010) Cellular and mitochondrial effects of alcohol consumption. Int J Environ Res Public Health 7(12):4281–4304. doi: 10.3390/ijerph7124281 PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Poso AR, Hirsimaki P (1991) Inhibition of proteolysis in the liver by chronic ethanol feeding. Biochem J 273(Pt 1):149–152PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Donohue TM Jr, Zetterman RK, Tuma DJ (1989) Effect of chronic ethanol administration on protein catabolism in rat liver. Alcohol Clin Exp Res 13(1):49–57Google Scholar
  70. 70.
    von Haefen C, Sifringer M, Menk M, Spies CD (2011) Ethanol enhances susceptibility to apoptotic cell death via down-regulation of autophagy-related proteins. Alcohol Clin Exp Res 35(8):1381–1391. doi: 10.1111/j.1530-0277.2011.01473.x Google Scholar
  71. 71.
    Guo R, Hu N, Kandadi MR, Ren J (2012) Facilitated ethanol metabolism promotes cardiomyocyte contractile dysfunction through autophagy in murine hearts. Autophagy 8(4):593–608. doi: 10.4161/auto.18997 PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Prock TL, Miranda RC (2007) Embryonic cerebral cortical progenitors are resistant to apoptosis, but increase expression of suicide receptor DISC-complex genes and suppress autophagy following ethanol exposure. Alcohol Clin Exp Res 31(4):694–703. doi: 10.1111/j.1530-0277.2007.00354.x PubMedPubMedCentralGoogle Scholar
  73. 73.
    You M, Matsumoto M, Pacold CM, Cho WK, Crabb DW (2004) The role of AMP-activated protein kinase in the action of ethanol in the liver. Gastroenterology 127(6):1798–1808PubMedCrossRefGoogle Scholar
  74. 74.
    Donohue TM Jr (2009) Autophagy and ethanol-induced liver injury. World J Gastroenterol 15(10):1178–1185Google Scholar
  75. 75.
    Komatsu M, Kurokawa H, Waguri S, Taguchi K, Kobayashi A, Ichimura Y, Sou YS, Ueno I, Sakamoto A, Tong KI, Kim M, Nishito Y, Iemura S, Natsume T, Ueno T, Kominami E, Motohashi H, Tanaka K, Yamamoto M (2010) The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol 12(3):213–223. doi: 10.1038/ncb2021 PubMedGoogle Scholar
  76. 76.
    Kim JS, Nitta T, Mohuczy D, O'Malley KA, Moldawer LL, Dunn WA Jr, Behrns KE (2008) Impaired autophagy: a mechanism of mitochondrial dysfunction in anoxic rat hepatocytes. Hepatology 47(5):1725–1736. doi: 10.1002/hep.22187
  77. 77.
    Thomes PG, Ehlers RA, Trambly CS, Clemens DL, Fox HS, Tuma DJ, Donohue TM (2013) Multilevel regulation of autophagosome content by ethanol oxidation in HepG2 cells. Autophagy 9(1):63–73. doi: 10.4161/auto.22490 PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Ding WX, Li M, Chen X, Ni HM, Lin CW, Gao W, Lu B, Stolz DB, Clemens DL, Yin XM (2010) Autophagy reduces acute ethanol-induced hepatotoxicity and steatosis in mice. Gastroenterology 139(5):1740–1752. doi: 10.1053/j.gastro.2010.07.041 PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Ding WX, Li M, Yin XM (2011) Selective taste of ethanol-induced autophagy for mitochondria and lipid droplets. Autophagy 7(2):248–249PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Eid N, Ito Y, Otsuki Y (2012) Enhanced mitophagy in Sertoli cells of ethanol-treated rats: morphological evidence and clinical relevance. J Mol Histol 43(1):71–80. doi: 10.1007/s10735-011-9372-0 PubMedCrossRefGoogle Scholar
  81. 81.
    Chen G, Ke Z, Xu M, Liao M, Wang X, Qi Y, Zhang T, Frank JA, Bower KA, Shi X, Luo J (2012) Autophagy is a protective response to ethanol neurotoxicity. Autophagy 8(11):1577–1589. doi: 10.4161/auto.21376 PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Pandhare J, Dash C (2011) A prospective on drug abuse-associated epigenetics and HIV-1 replication. Life Sci 88(21–22):995–999. doi: 10.1016/j.lfs.2010.10.005 PubMedCrossRefGoogle Scholar
  83. 83.
    Albertson TE (2014) Recreational drugs of abuse. Clin Rev Allergy Immunol 46(1):1–2. doi: 10.1007/s12016-013-8382-y PubMedCrossRefGoogle Scholar
  84. 84.
    Strathdee SA, Stockman JK (2010) Epidemiology of HIV among injecting and non-injecting drug users: current trends and implications for interventions. Curr HIV/AIDS Rep 7(2):99–106. doi: 10.1007/s11904-010-0043-7 PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Shirazi J, Shah S, Sagar D, Nonnemacher MR, Wigdahl B, Khan ZK, Jain P (2013) Epigenetics, drugs of abuse, and the retroviral promoter. J Neuroimmune Pharm Off J Soc NeuroImmune Pharm 8(5):1181–1196. doi: 10.1007/s11481-013-9508-y CrossRefGoogle Scholar
  86. 86.
    Hagan H, Thiede H, Des Jarlais DC (2005) HIV/hepatitis C virus co-infection in drug users: risk behavior and prevention. AIDS 19(Suppl 3):S199–S207PubMedCrossRefGoogle Scholar
  87. 87.
    Sherman SG, Latkin CA (2001) Intimate relationship characteristics associated with condom use among drug users and their sex partners: a multilevel analysis. Drug Alcohol Depend 64(1):97–104PubMedCrossRefGoogle Scholar
  88. 88.
    Edlin BR, Irwin KL, Faruque S, McCoy CB, Word C, Serrano Y, Inciardi JA, Bowser BP, Schilling RF, Holmberg SD (1994) Intersecting epidemics—crack cocaine use and HIV infection among inner-city young adults. Multicenter Crack Cocaine and HIV Infection Study Team. N Engl J Med 331(21):1422–1427. doi: 10.1056/NEJM199411243312106 PubMedCrossRefGoogle Scholar
  89. 89.
    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(2):93–97PubMedPubMedCentralGoogle Scholar
  90. 90.
    Moore DJ, Blackstone K, Woods SP, Ellis RJ, Atkinson JH, Heaton RK, Grant I, Hnrc G, The Tmarc G (2012) Methamphetamine use and neuropsychiatric factors are associated with antiretroviral non-adherence. AIDS Care 24(12):1504–1513. doi: 10.1080/09540121.2012.672718 PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Ellis RJ, Childers ME, Cherner M, Lazzaretto D, Letendre S, Grant I, Group HIVNRC (2003) Increased human immunodeficiency virus loads in active methamphetamine users are explained by reduced effectiveness of antiretroviral therapy. J Infect Dis 188(12):1820–1826. doi: 10.1086/379894 CrossRefGoogle Scholar
  92. 92.
    Shoptaw S, Stall R, Bordon J, Kao U, Cox C, Li X, Ostrow DG, Plankey MW (2012) Cumulative exposure to stimulants and immune function outcomes among HIV-positive and HIV-negative men in the Multicenter AIDS Cohort Study. Int J STD AIDS 23(8):576–580. doi: 10.1258/ijsa.2012.011322 PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Sriram U, Cenna JM, Haldar B, Fernandes NC, Razmpour R, Fan S, Ramirez SH, Potula R (2016) Methamphetamine induces trace amine-associated receptor 1 (TAAR1) expression in human T lymphocytes: role in immunomodulation. J Leukoc Biol 99(1):213–223. doi: 10.1189/jlb.4A0814-395RR PubMedCrossRefGoogle Scholar
  94. 94.
    Hoefer MM, Sanchez AB, Maung R, de Rozieres CM, Catalan IC, Dowling CC, Thaney VE, Pina-Crespo J, Zhang D, Roberts AJ, Kaul M (2015) Combination of methamphetamine and HIV-1 gp120 causes distinct long-term alterations of behavior, gene expression, and injury in the central nervous system. Exp Neurol 263:221–234. doi: 10.1016/j.expneurol.2014.09.010 PubMedCrossRefGoogle Scholar
  95. 95.
    Shah A, Kumar S, Simon SD, Singh DP, Kumar A (2013) HIV gp120- and methamphetamine-mediated oxidative stress induces astrocyte apoptosis via cytochrome P450 2E1. Cell Death Dis 4:e850. doi: 10.1038/cddis.2013.374 PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Shah A, Silverstein PS, Kumar S, Singh DP, Kumar A (2012) Synergistic cooperation between methamphetamine and HIV-1 gsp120 through the P13K/Akt pathway induces IL-6 but not IL-8 expression in astrocytes. PLoS One 7(12):e52060. doi: 10.1371/journal.pone.0052060 PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Qi L, Gang L, Hang KW, Ling CH, Xiaofeng Z, Zhen L, Wai YD, Sang PW (2011) Programmed neuronal cell death induced by HIV-1 tat and methamphetamine. Microsc Res Tech 74(12):1139–1144. doi: 10.1002/jemt.21006 PubMedCrossRefGoogle Scholar
  98. 98.
    Li Y, Merrill JD, Mooney K, Song L, Wang X, Guo CJ, Savani RC, Metzger DS, Douglas SD, Ho WZ (2003) Morphine enhances HIV infection of neonatal macrophages. Pediatr Res 54(2):282–288. doi: 10.1203/01.PDR.0000074973.83826.4C PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Nair MP, Schwartz SA, Polasani R, Hou J, Sweet A, Chadha KC (1997) Immunoregulatory effects of morphine on human lymphocytes. Clin Diagn Lab Immunol 4(2):127–132PubMedPubMedCentralGoogle Scholar
  100. 100.
    Schweitzer C, Keller F, Schmitt MP, Jaeck D, Adloff M, Schmitt C, Royer C, Kirn A, Aubertin AM (1991) Morphine stimulates HIV replication in primary cultures of human Kupffer cells. Res Virol 142(2–3):189–195PubMedCrossRefGoogle Scholar
  101. 101.
    Dave RS (2012) Morphine affects HIV-induced inflammatory response without influencing viral replication in human monocyte-derived macrophages. FEMS Immunol Med Microbiol 64(2):228–236. doi: 10.1111/j.1574-695X.2011.00894.x PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Samikkannu T, Ranjith D, Rao KV, Atluri VS, Pimentel E, El-Hage N, Nair MP (2015) HIV-1 gp120 and morphine induced oxidative stress: role in cell cycle regulation. Front Microbiol 6:614. doi: 10.3389/fmicb.2015.00614 PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Mahajan SD, Aalinkeel R, Sykes DE, Reynolds JL, Bindukumar B, Fernandez SF, Chawda R, Shanahan TC, Schwartz SA (2008) Tight junction regulation by morphine and HIV-1 tat modulates blood-brain barrier permeability. J Clin Immunol 28(5):528–541. doi: 10.1007/s10875-008-9208-1 PubMedCrossRefGoogle Scholar
  104. 104.
    Hu S, Sheng WS, Lokensgard JR, Peterson PK (2005) Morphine potentiates HIV-1 gp120-induced neuronal apoptosis. J Infect Dis 191(6):886–889. doi: 10.1086/427830 PubMedCrossRefGoogle Scholar
  105. 105.
    El-Hage N, Rodriguez M, Dever SM, Masvekar RR, Gewirtz DA, Shacka JJ (2015) HIV-1 and morphine regulation of autophagy in microglia: limited interactions in the context of HIV-1 infection and opioid abuse. J Virol 89(2):1024–1035. doi: 10.1128/JVI.02022-14 PubMedCrossRefGoogle Scholar
  106. 106.
    Chaisson RE, Bacchetti P, Osmond D, Brodie B, Sande MA, Moss AR (1989) Cocaine use and HIV infection in intravenous drug users in San Francisco. JAMA 261(4):561–565PubMedCrossRefGoogle Scholar
  107. 107.
    Sharpe TT, Lee LM, Nakashima AK, Elam-Evans LD, Fleming PL (2004) Crack cocaine use and adherence to antiretroviral treatment among HIV-infected black women. J Community Health 29(2):117–127PubMedCrossRefGoogle Scholar
  108. 108.
    Kumar S, Rao PS, Earla R, Kumar A (2015) Drug-drug interactions between anti-retroviral therapies and drugs of abuse in HIV systems. Expert Opin Drug Metab Toxicol 11(3):343–355. doi: 10.1517/17425255.2015.996546 PubMedCrossRefGoogle Scholar
  109. 109.
    Roth MD, Tashkin DP, Choi R, Jamieson BD, Zack JA, Baldwin GC (2002) Cocaine enhances human immunodeficiency virus replication in a model of severe combined immunodeficient mice implanted with human peripheral blood leukocytes. J Infect Dis 185(5):701–705. doi: 10.1086/339012 PubMedCrossRefGoogle Scholar
  110. 110.
    Ruiz P, Cleary T, Nassiri M, Steele B (1994) Human T lymphocyte subpopulation and NK cell alterations in persons exposed to cocaine. Clin Immunol Immunopathol 70(3):245–250PubMedCrossRefGoogle Scholar
  111. 111.
    Venkatesan A, Nath A, Ming GL, Song H (2007) Adult hippocampal neurogenesis: regulation by HIV and drugs of abuse. Cell Mol life Sci CMLS 64(16):2120–2132. doi: 10.1007/s00018-007-7063-5 PubMedCrossRefGoogle Scholar
  112. 112.
    Gaskill PJ, Yano HH, Kalpana GV, Javitch JA, Berman JW (2014) Dopamine receptor activation increases HIV entry into primary human macrophages. PLoS One 9(9):e108232. doi: 10.1371/journal.pone.0108232 PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Sharma HS, Muresanu D, Sharma A, Patnaik R (2009) Cocaine-induced breakdown of the blood-brain barrier and neurotoxicity. Int Rev Neurobiol 88:297–334. doi: 10.1016/S0074-7742(09)88011-2 PubMedCrossRefGoogle Scholar
  114. 114.
    Pandhare J, Addai AB, Mantri CK, Hager C, Smith RM, Barnett L, Villalta F, Kalams SA, Dash C (2014) Cocaine enhances HIV-1-induced CD4(+) T-cell apoptosis: implications in disease progression in cocaine-abusing HIV-1 patients. Am J Pathol 184(4):927–936. doi: 10.1016/j.ajpath.2013.12.004 PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    De Simone FI, Darbinian N, Amini S, Muniswamy M, White MK, Elrod JW, Datta PK, Langford D, Khalili K (2016) HIV-1 tat and cocaine impair survival of cultured primary neuronal cells via a mitochondrial pathway. J Neuroimmune Pharm Off J Soc NeuroImmune Pharm 11(2):358–368. doi: 10.1007/s11481-016-9669-6 CrossRefGoogle Scholar
  116. 116.
    Woolf-King SE, Neilands TB, Dilworth SE, Carrico AW, Johnson MO (2014) Alcohol use and HIV disease management: the impact of individual and partner-level alcohol use among HIV-positive men who have sex with men. AIDS Care 26(6):702–708. doi: 10.1080/09540121.2013.855302 PubMedCrossRefGoogle Scholar
  117. 117.
    Pellowski JA, Kalichman SC, Kalichman MO, Cherry C (2016) Alcohol-antiretroviral therapy interactive toxicity beliefs and daily medication adherence and alcohol use among people living with HIV. AIDS Care:1–8. doi: 10.1080/09540121.2016.1154134
  118. 118.
    Miguez MJ, Shor-Posner G, Morales G, Rodriguez A, Burbano X (2003) HIV treatment in drug abusers: impact of alcohol use. Addict Biol 8(1):33–37. doi: 10.1080/1355621031000069855 PubMedCrossRefGoogle Scholar
  119. 119.
    Kumar R, Perez-Casanova AE, Tirado G, Noel RJ, Torres C, Rodriguez I, Martinez M, Staprans S, Kraiselburd E, Yamamura Y, Higley JD, Kumar A (2005) Increased viral replication in simian immunodeficiency virus/simian-HIV-infected macaques with self-administering model of chronic alcohol consumption. J Acquir Immune Defic Syndr 39(4):386–390PubMedCrossRefGoogle Scholar
  120. 120.
    Goral J, Choudhry MA, Kovacs EJ (2004) Acute ethanol exposure inhibits macrophage IL-6 production: role of p38 and ERK1/2 MAPK. J Leukoc Biol 75(3):553–559. doi: 10.1189/jlb.0703350 PubMedCrossRefGoogle Scholar
  121. 121.
    Miguez MJ, Rosenberg R, Burbano-Levy X, Carmona T, Malow R (2012) The effect of alcohol use on IL-6 responses across different racial/ethnic groups. Futur Virol 7(2):205–213. doi: 10.2217/FVL.12.3 CrossRefGoogle Scholar
  122. 122.
    Potula R, Haorah J, Knipe B, Leibhart J, Chrastil J, Heilman D, Dou H, Reddy R, Ghorpade A, Persidsky Y (2006) Alcohol abuse enhances neuroinflammation and impairs immune responses in an animal model of human immunodeficiency virus-1 encephalitis. Am J Pathol 168(4):1335–1344. doi: 10.2353/ajpath.2006.051181 PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Sarkar S, Chang SL (2013) Ethanol concentration-dependent alterations in gene expression during acute binge drinking in the HIV-1 transgenic rat. Alcohol Clin Exp Res 37(7):1082–1090. doi: 10.1111/acer.12077 PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Pandey R, Ghorpade A (2015) HIV-1 and alcohol abuse promote astrocyte inflammation: a mechanistic synergy via the cytosolic phospholipase A2 pathway. Cell Death Dis 6:e2017. doi: 10.1038/cddis.2015.346 PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Acheampong E, Mukhtar M, Parveen Z, Ngoubilly N, Ahmad N, Patel C, Pomerantz RJ (2002) Ethanol strongly potentiates apoptosis induced by HIV-1 proteins in primary human brain microvascular endothelial cells. Virology 304(2):222–234PubMedCrossRefGoogle Scholar
  126. 126.
    Brown JN, Ortiz GM, Angel TE, Jacobs JM, Gritsenko M, Chan EY, Purdy DE, Murnane RD, Larsen K, Palermo RE, Shukla AK, Clauss TR, Katze MG, McCune JM, Smith RD (2012) Morphine produces immunosuppressive effects in nonhuman primates at the proteomic and cellular levels. Mol Cell Proteomics MCP 11(9):605–618. doi: 10.1074/mcp.M111.016121 PubMedCrossRefGoogle Scholar
  127. 127.
    Mata MM, Napier TC, Graves SM, Mahmood F, Raeisi S, Baum LL (2015) Methamphetamine decreases CD4 T cell frequency and alters pro-inflammatory cytokine production in a model of drug abuse. Eur J Pharmacol 752:26–33. doi: 10.1016/j.ejphar.2015.02.002 PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Saito M, Yamaguchi T, Kawata T, Ito H, Kanai T, Terada M, Yokosuka M, Saito TR (2006) Effects of methamphetamine on cortisone concentration, NK cell activity and mitogen response of T-lymphocytes in female cynomolgus monkeys. Exp Anim / Japan Assoc Lab Anim Sci 55(5):477–481Google Scholar
  129. 129.
    Harms R, Morsey B, Boyer CW, Fox HS, Sarvetnick N (2012) Methamphetamine administration targets multiple immune subsets and induces phenotypic alterations suggestive of immunosuppression. PLoS One 7(12):e49897. doi: 10.1371/journal.pone.0049897 PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Bagasra O, Pomerantz RJ (1993) Human immunodeficiency virus type 1 replication in peripheral blood mononuclear cells in the presence of cocaine. J infect dis 168(5):1157–1164PubMedCrossRefGoogle Scholar
  131. 131.
    Peterson PK, Gekker G, Chao CC, Schut R, Molitor TW, Balfour HH Jr (1991) Cocaine potentiates HIV-1 replication in human peripheral blood mononuclear cell cocultures. Involvement of transforming growth factor-beta. J Immunol 146(1):81–84Google Scholar
  132. 132.
    Poundstone KE, Chaisson RE, Moore RD (2001) Differences in HIV disease progression by injection drug use and by sex in the era of highly active antiretroviral therapy. AIDS 15(9):1115–1123PubMedCrossRefGoogle Scholar
  133. 133.
    Moore RD, Keruly JC, Chaisson RE (2004) Differences in HIV disease progression by injecting drug use in HIV-infected persons in care. J Acquir Immune Defic Syndr 35(1):46–51PubMedCrossRefGoogle Scholar
  134. 134.
    Arnsten JH, Demas PA, Grant RW, Gourevitch MN, Farzadegan H, Howard AA, Schoenbaum EE (2002) Impact of active drug use on antiretroviral therapy adherence and viral suppression in HIV-infected drug users. J Gen Intern Med 17(5):377–381PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Bell JE, Arango JC, Anthony IC (2006) Neurobiology of multiple insults: HIV-1-associated brain disorders in those who use illicit drugs. J Neuroimmune Pharm Off J Soc NeuroImmune Pharm 1(2):182–191. doi: 10.1007/s11481-006-9018-2 CrossRefGoogle Scholar
  136. 136.
    Gaskill PJ, Calderon TM, Luers AJ, Eugenin EA, Javitch JA, Berman JW (2009) Human immunodeficiency virus (HIV) infection of human macrophages is increased by dopamine: a bridge between HIV-associated neurologic disorders and drug abuse. Am J Pathol 175(3):1148–1159. doi: 10.2353/ajpath.2009.081067 PubMedPubMedCentralCrossRefGoogle Scholar
  137. 137.
    Turchan-Cholewo J, Dimayuga FO, Gupta S, Keller JN, Knapp PE, Hauser KF, Bruce-Keller AJ (2009) Morphine and HIV-Tat increase microglial-free radical production and oxidative stress: possible role in cytokine regulation. J Neurochem 108(1):202–215. doi: 10.1111/j.1471-4159.2008.05756.x PubMedCrossRefGoogle Scholar
  138. 138.
    Happel C, Kutzler M, Rogers TJ (2011) Opioid-induced chemokine expression requires NF-kappaB activity: the role of PKCzeta. J Leukoc Biol 89(2):301–309. doi: 10.1189/jlb.0710402 PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    Conant K, St Hillaire C, Anderson C, Galey D, Wang J, Nath A (2004) Human immunodeficiency virus type 1 tat and methamphetamine affect the release and activation of matrix-degrading proteinases. J Neurovirol 10(1):21–28PubMedCrossRefGoogle Scholar
  140. 140.
    Fuster D, Cheng DM, Quinn EK, Armah KA, Saitz R, Freiberg MS, Samet JH, Tsui JI (2014) Inflammatory cytokines and mortality in a cohort of HIV-infected adults with alcohol problems. AIDS 28(7):1059–1064. doi: 10.1097/QAD.0000000000000184 PubMedPubMedCentralCrossRefGoogle Scholar
  141. 141.
    Martinez-Vicente M, Talloczy Z, Wong E, Tang G, Koga H, Kaushik S, de Vries R, Arias E, Harris S, Sulzer D, Cuervo AM (2010) Cargo recognition failure is responsible for inefficient autophagy in Huntington's disease. Nat Neurosci 13(5):567–576. doi: 10.1038/nn.2528 PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Winslow AR, Chen CW, Corrochano S, Acevedo-Arozena A, Gordon DE, Peden AA, Lichtenberg M, Menzies FM, Ravikumar B, Imarisio S, Brown S, O'Kane CJ, Rubinsztein DC (2010) Alpha-Synuclein impairs macroautophagy: implications for Parkinson’s disease. J Cell Biol 190(6):1023–1037. doi: 10.1083/jcb.201003122 PubMedPubMedCentralCrossRefGoogle Scholar
  143. 143.
    Wolfe DM, Lee JH, Kumar A, Lee S, Orenstein SJ, Nixon RA (2013) Autophagy failure in Alzheimer’s disease and the role of defective lysosomal acidification. Eur J Neurosci 37(12):1949–1961. doi: 10.1111/ejn.12169 PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Dever SM, Rodriguez M, Lapierre J, Costin BN, El-Hage N (2015) Differing roles of autophagy in HIV-associated neurocognitive impairment and encephalitis with implications for morphine co-exposure. Front Microbiol 6:653. doi: 10.3389/fmicb.2015.00653 PubMedPubMedCentralCrossRefGoogle Scholar
  145. 145.
    Sanchez AB, Varano GP, de Rozieres CM, Maung R, Catalan IC, Dowling CC, Sejbuk NE, Hoefer MM, Kaul M (2015) Antiretrovirals, methamphetamine, and HIV-1 envelope protein gp120 compromise neuronal energy homeostasis in association with various degrees of synaptic and Neuritic damage. Antimicrob Agents Chemother 60(1):168–179. doi: 10.1128/AAC.01632-15 PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Cao L, Fu M, Kumar S, Kumar A (2016) Methamphetamine potentiates HIV-1 gp120-mediated autophagy via Beclin-1 and Atg5/7 as a pro-survival response in astrocytes. Cell death & diseaseGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Division of Pharmacology and Toxicology, School of PharmacyUniversity of Missouri-Kansas CityKansas CityUSA
  2. 2.Department of Pathology, School of Medicine, School of MedicineUniversity of Missouri-Kansas CityKansas CityUSA
  3. 3.Department of Pharmaceutical Sciences, College of PharmacyUniversity of Tennessee Health Science CenterMemphisUSA

Personalised recommendations