Critical Role of Beclin1 in HIV Tat and Morphine-Induced Inflammation and Calcium Release in Glial Cells from Autophagy Deficient Mouse

Barber SA, Uhrlaub JL, DeWitt JB, Tarwater PM, Zink MC (2004) Dysregulation of mitogen-activated protein kinase signaling pathways in simian immunodeficiency virus encephalitis. Am J Pathol 164:355–362. https://doi.org/10.1016/S0002-9440(10)63125-2 Barger SW, Goodwin ME, Porter MM, Beggs ML (2007) Glutamate release from activated microglia requires the oxidative burst and lipid peroxidation. J Neurochem 101:1205–1213. https://doi.org/10.1111/j.1471-4159.2007.04487.x Bokhari SM, Yao H, Bethel-Brown C, Fuwang P, Williams R, Dhillon NK, Hegde R, Kumar A, Buch SJ (2009) Morphine enhances tat-induced activation in murine microglia. J Neuro-Oncol 15:219–228. https://doi.org/10.1080/13550280902913628 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 13:3640–3644. https://doi.org/10.4161/15384101.2014.952959 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:e1005018. https://doi.org/10.1371/journal.ppat.1005018 Cao L, Fu M, Kumar S, Kumar A (2016a) Methamphetamine potentiates HIV-1 gp120-mediated autophagy via Beclin-1 and Atg5/7 as a pro-survival response in astrocytes. Cell Death Dis 7:e2425. https://doi.org/10.1038/cddis.2016.317 Cao L, Glazyrin A, Kumar S, Kumar A (2016b) Role of autophagy in HIV pathogenesis and drug abuse. Mol Neurobiol 54:5855–5867. https://doi.org/10.1007/s12035-016-0118-6 Conant K, Ma M, Nath A, Major EO (1996) Extracellular human immunodeficiency virus type 1 tat protein is associated with an increase in both NF-kappa B binding and protein kinase C activity in primary human astrocytes. J Virol 70:1384–1389 Conant K, Garzino-Demo A, Nath A, McArthur JC, Halliday W, Power C, Gallo RC, Major EO (1998) Induction of monocyte chemoattractant protein-1 in HIV-1 tat-stimulated astrocytes and elevation in AIDS dementia. Proc Natl Acad Sci U S A 95:3117–3121 D'Aversa TG, Yu KO, Berman JW (2004) Expression of chemokines by human fetal microglia after treatment with the human immunodeficiency virus type 1 protein tat. J Neuro-Oncol 10:86–97. https://doi.org/10.1080/13550280490279807 D'Aversa TG, Eugenin EA, Berman JW (2005) NeuroAIDS: contributions of the human immunodeficiency virus-1 proteins tat and gp120 as well as CD40 to microglial activation. J Neurosci Res 81:436–446. https://doi.org/10.1002/jnr.20486 Davis RJ (2000) Signal transduction by the JNK group of MAP kinases. Cell 103:239–252 Deretic V, Saitoh T, Akira S (2013) Autophagy in infection, inflammation and immunity. Nat Rev Immunol 13:722–737. https://doi.org/10.1038/nri3532 Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95. https://doi.org/10.1152/physrev.00018.2001 El-Hage N, Gurwell JA, Singh IN, Knapp PE, Nath A, Hauser KF (2005) Synergistic increases in intracellular Ca2+, and the release of MCP-1, RANTES, and IL-6 by astrocytes treated with opiates and HIV-1 tat. Glia 50:91–106. https://doi.org/10.1002/glia.20148 El-Hage N et al (2006) HIV-1 tat and opiate-induced changes in astrocytes promote chemotaxis of microglia through the expression of MCP-1 and alternative chemokines. Glia 53:132–146. https://doi.org/10.1002/glia.20262 El-Hage N, Bruce-Keller AJ, Yakovleva T, Bazov I, Bakalkin G, Knapp PE, Hauser KF (2008) Morphine exacerbates HIV-1 tat-induced cytokine production in astrocytes through convergent effects on [ca(2+)](i), NF-kappaB trafficking and transcription. PLoS One 3:e4093. https://doi.org/10.1371/journal.pone.0004093 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 89:1024–1035 doi:https://doi.org/10.1128/JVI.02022-14 Ensoli B, Buonaguro L, Barillari G, Fiorelli V, Gendelman R, Morgan RA, Wingfield P, Gallo RC (1993) Release, uptake, and effects of extracellular human immunodeficiency virus type 1 tat protein on cell growth and viral transactivation. J Virol 67:277–287 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:e5787. https://doi.org/10.1371/journal.pone.0005787 Feng Y, He D, Yao Z, Klionsky DJ (2014) The machinery of macroautophagy. Cell Res 24:24–41. https://doi.org/10.1038/cr.2013.168 Fields J, Dumaop W, Elueteri 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 35:1921–1938. https://doi.org/10.1523/JNEUROSCI.3207-14.2015 Friedman H, Pross S, Klein TW (2006) Addictive drugs and their relationship with infectious diseases. FEMS Immunol Med Microbiol 47:330–342. https://doi.org/10.1111/j.1574-695X.2006.00097.x Gurwell JA, Nath A, Sun Q, Zhang J, Martin KM, Chen Y, Hauser KF (2001) Synergistic neurotoxicity of opioids and human immunodeficiency virus-1 tat protein in striatal neurons in vitro. Neuroscience 102:555–563 Haughey NJ, Holden CP, Nath A, Geiger JD (1999) Involvement of inositol 1,4,5-trisphosphate-regulated stores of intracellular calcium in calcium dysregulation and neuron cell death caused by HIV-1 protein tat. J Neurochem 73:1363–1374 Haughey NJ, Nath A, Mattson MP, Slevin JT, Geiger JD (2001) HIV-1 tat through phosphorylation of NMDA receptors potentiates glutamate excitotoxicity. J Neurochem 78:457–467 Hauser KF, El-Hage N, Buch S, Nath A, Tyor WR, Bruce-Keller AJ, Knapp PE (2006) Impact of opiate-HIV-1 interactions on neurotoxic signaling. J NeuroImmune Pharmacol 1(1):98–105. https://doi.org/10.1007/s11481-005-9000-4 Hauser KF, el-Hage N, Stiene-Martin A, Maragos WF, Nath A, Persidsky Y, Volsky DJ, Knapp PE (2007) HIV-1 neuropathogenesis: glial mechanisms revealed through substance abuse. J Neurochem 100:567–586. https://doi.org/10.1111/j.1471-4159.2006.04227.x Hauser KF, Fitting S, Dever SM, Podhaizer EM, Knapp PE (2012) Opiate drug use and the pathophysiology of neuroAIDS. Curr HIV Res 10:435–452 Hui L, Chen X, Haughey NJ, Geiger JD (2012) Role of endolysosomes in HIV-1 tat-induced neurotoxicity. ASN Neuro 4:243–252. https://doi.org/10.1042/AN20120017 Jones M, Olafson K, Del Bigio MR, Peeling J, Nath A (1998) Intraventricular injection of human immunodeficiency virus type 1 (HIV-1) tat protein causes inflammation, gliosis, apoptosis, and ventricular enlargement. J Neuropathol Exp Neurol 57:563–570 Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19:5720–5728. https://doi.org/10.1093/emboj/19.21.5720 Kaul N, Forman HJ (1996) Activation of NF kappa B by the respiratory burst of macrophages. Free Radic Biol Med 21:401–405 Kaul M, Garden GA, Lipton SA (2001) Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410:988–994. https://doi.org/10.1038/35073667 Kiriyama Y, Nochi H (2015) The function of autophagy in neurodegenerative diseases. Int J Mol Sci 16:26797–26812. https://doi.org/10.3390/ijms161125990 Klionsky DJ, Baehrecke EH, Brumell JH, Chu CT, Codogno P, Cuervo AM, Debnath J, Deretic V, Elazar Z, Eskelinen EL, Finkbeiner S, Fueyo-Margareto J, Gewirtz DA, Jäättelä M, Kroemer G, Levine B, Melia TJ, Mizushima N, Rubinsztein DC, Simonsen A, Thorburn A, Thumm M, Tooze SA (2011) A comprehensive glossary of autophagy-related molecules and processes (2nd edition). Autophagy 7:1273–1294. https://doi.org/10.4161/auto.7.11.17661 Kramer-Hammerle S, Rothenaigner I, Wolff H, Bell JE, Brack-Werner R (2005) Cells of the central nervous system as targets and reservoirs of the human immunodeficiency virus. Virus Res 111:194–213. https://doi.org/10.1016/j.virusres.2005.04.009 Kruman II, Nath A, Mattson MP (1998) HIV-1 protein tat induces apoptosis of hippocampal neurons by a mechanism involving caspase activation, calcium overload, and oxidative stress. Exp Neurol 154:276–288. https://doi.org/10.1006/exnr.1998.6958 Kruman II, Nath A, Maragos WF, Chan SL, Jones M, Rangnekar VM, Jakel RJ, Mattson MP (1999) Evidence that Par-4 participates in the pathogenesis of HIV encephalitis. Am J Pathol 155:39–46. https://doi.org/10.1016/S0002-9440(10)65096-1 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 186:255–268. https://doi.org/10.1083/jcb.200903070 Liu Z, Qiao L, Zhang Y, Zang Y, Shi Y, Liu K, Zhang X, Lu X, Yuan L, Su B, Zhang T, Wu H, Chen D (2017) ASPP2 plays a dual role in gp120-induced autophagy and apoptosis of neuroblastoma cells. Front Neurosci 11:150. https://doi.org/10.3389/fnins.2017.00150 Mabrouk K, Van Rietschoten J, Vives E, Darbon H, Rochat H, Sabatier JM (1991) Lethal neurotoxicity in mice of the basic domains of HIV and SIV rev proteins. Study of these regions by circular dichroism. FEBS Lett 289:13–17 Mayne M, Bratanich AC, Chen P, Rana F, Nath A, Power C (1998) HIV-1 tat molecular diversity and induction of TNF-alpha: implications for HIV-induced neurological disease. Neuroimmunomodulation 5:184–192. https://doi.org/10.1159/000026336 McKnight NC et al (2014) Beclin 1 is required for neuron viability and regulates endosome pathways via the UVRAG-VPS34 complex. PLoS Genet 10:e1004626. https://doi.org/10.1371/journal.pgen.1004626 Mehla R, Chauhan A (2015) HIV-1 differentially modulates autophagy in neurons and astrocytes. J Neuroimmunol 285:106–118. https://doi.org/10.1016/j.jneuroim.2015.06.001 Meulendyke KA, Croteau JD, Zink MC (2014) HIV life cycle, innate immunity and autophagy in the central nervous system. Curr Opin HIV AIDS 9:565–571. https://doi.org/10.1097/COH.0000000000000106 Mizushima N, Yoshimori T (2007) How to interpret LC3 immunoblotting. Autophagy 3:542–545 Nath A (2002) Human immunodeficiency virus (HIV) proteins in neuropathogenesis of HIV dementia. J Infect Dis 186(Suppl 2):S193–S198. https://doi.org/10.1086/344528 Nath A, Conant K, Chen P, Scott C, Major EO (1999) Transient exposure to HIV-1 tat protein results in cytokine production in macrophages and astrocytes. A hit and run phenomenon J Biol Chem 274:17098–17102 New DR, Ma M, Epstein LG, Nath A, Gelbard HA (1997) Human immunodeficiency virus type 1 tat protein induces death by apoptosis in primary human neuron cultures. J Neuro-Oncol 3:168–173 Norman JP, Perry SW, Reynolds HM, Kiebala M, de Mesy Bentley KL, Trejo M, Volsky DJ, Maggirwar SB, Dewhurst S, Masliah E, Gelbard HA (2008) HIV-1 tat activates neuronal ryanodine receptors with rapid induction of the unfolded protein response and mitochondrial hyperpolarization. PLoS One 3:e3731. https://doi.org/10.1371/journal.pone.0003731 Philippon V, Vellutini C, Gambarelli D, Harkiss G, Arbuthnott G, Metzger D, Roubin R, Filippi P (1994) The basic domain of the lentiviral tat protein is responsible for damages in mouse brain: involvement of cytokines. Virology 205:519–529. https://doi.org/10.1006/viro.1994.1673 Pocernich CB, Sultana R, Mohmmad-Abdul H, Nath A, Butterfield DA (2005) HIV-dementia, tat-induced oxidative stress, and antioxidant therapeutic considerations. Brain Res Brain Res Rev 50:14–26. https://doi.org/10.1016/j.brainresrev.2005.04.002 Pulliam L, Herndier BG, Tang NM, McGrath MS (1991) Human immunodeficiency virus-infected macrophages produce soluble factors that cause histological and neurochemical alterations in cultured human brains. J Clin Invest 87:503–512. https://doi.org/10.1172/JCI115024 Rodriguez M, Kaushik A, Lapierre J, Dever SM, El-Hage N, Nair M (2017a) Electro-magnetic Nano-particle bound Beclin1 siRNA crosses the blood-brain barrier to attenuate the inflammatory effects of HIV-1 infection in vitro. J NeuroImmune Pharmacol 12:120–132. https://doi.org/10.1007/s11481-016-9688-3 Rodriguez M, Lapierre J, Ojha C, Estrada-Bueno H, Dever S, Gewirtz D, Kashanchi F, el-Hage N (2017b) Importance of autophagy in mediating human immunodeficiency virus (HIV) and morphine-induced metabolic dysfunction and inflammation in human astrocytes. Viruses 9:201. https://doi.org/10.3390/v9080201 Rodriguez M, Lapierre J, Ojha CR, Kaushik A, Batrakova E, Kashanchi F, Dever SM, Nair M, el-Hage N (2017c) Intranasal drug delivery of small interfering RNA targeting Beclin1 encapsulated with polyethylenimine (PEI) in mouse brain to achieve HIV attenuation. Sci Rep 7:1862. https://doi.org/10.1038/s41598-017-01819-9 Rogers TJ, Peterson PK (2003) Opioid G protein-coupled receptors: signals at the crossroads of inflammation. Trends Immunol 24:116–121 Ronaldson PT, Bendayan R (2006) HIV-1 viral envelope glycoprotein gp120 triggers an inflammatory response in cultured rat astrocytes and regulates the functional expression of P-glycoprotein. Mol Pharmacol 70:1087–1098. https://doi.org/10.1124/mol.106.025973 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 89:615–625. https://doi.org/10.1128/JVI.02174-14 Saribas AS, Khalili K, Sariyer IK (2015) Dysregulation of autophagy by HIV-1 Nef in human astrocytes. Cell Cycle 14:2899–2904. https://doi.org/10.1080/15384101.2015.1069927 Steele AD, Henderson EE, Rogers TJ (2003) Mu-opioid modulation of HIV-1 coreceptor expression and HIV-1 replication. Virology 309:99–107 Steiner J, Haughey N, Li W, Venkatesan A, Anderson C, Reid R, Malpica T, Pocernich C, Butterfield DA, Nath A (2006) Oxidative stress and therapeutic approaches in HIV dementia. Antioxid Redox Signal 8:2089–2100. https://doi.org/10.1089/ars.2006.8.2089 Shi B, Raina J, Lorenzo A, Busciglio J, Gabuzda D (1998) Neuronal apoptosis induced by HIV-1 tat protein and TNF-alpha: potentiation of neurotoxicity mediated by oxidative stress and implications for HIV-1 dementia. J Neuro-Oncol 4:281–290 Silverstein PS, Shah A, Weemhoff J, Kumar S, Singh DP, Kumar A (2012) HIV-1 gp120 and drugs of abuse: interactions in the central nervous system. Curr HIV Res 10:369–383 Salminen A, Kaarniranta K, Kauppinen A (2013) Beclin 1 interactome controls the crosstalk between apoptosis, autophagy and inflammasome activation: impact on the aging process. Ageing Res Rev 12:520–534. https://doi.org/10.1016/j.arr.2012.11.004 Streit WJ, Walter SA, Pennell NA (1999) Reactive microgliosis. Prog Neurobiol 57:563–581 Sun Q, Fan J, Billiar TR, Scott MJ (2017) Inflammasome and autophagy regulation - a two-way street. Mol Med 23:1. https://doi.org/10.2119/molmed.2017.00077 Trillo-Pazos G, McFarlane-Abdulla E, Campbell IC, Pilkington GJ, Everall IP (2000) Recombinant nef HIV-IIIB protein is toxic to human neurons in culture. Brain Res 864:315–326 Turchan-Cholewo J, Dimayuga FO, Ding Q, Keller JN, Hauser KF, Knapp PE, Bruce-Keller AJ (2008) Cell-specific actions of HIV-tat and morphine on opioid receptor expression in glia. J Neurosci Res 86:2100–2110. https://doi.org/10.1002/jnr.21653 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 108:202–215. https://doi.org/10.1111/j.1471-4159.2008.05756.x Vogel BE, Lee SJ, Hildebrand A, Craig W, Pierschbacher MD, Wong-Staal F, Ruoslahti E (1993) A novel integrin specificity exemplified by binding of the alpha v beta 5 integrin to the basic domain of the HIV tat protein and vitronectin. J Cell Biol 121:461–468 Wei Y, Sinha S, Levine B (2008) Dual role of JNK1-mediated phosphorylation of Bcl-2 in autophagy and apoptosis regulation. Autophagy 4:949–951 Yue Z, Jin S, Yang C, Levine AJ, Heintz N (2003) Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci U S A 100:15077–15082. https://doi.org/10.1073/pnas.2436255100 Zhou D, Spector SA (2008) Human immunodeficiency virus type-1 infection inhibits autophagy. AIDS (London, England) 22:695–699. https://doi.org/10.1097/QAD.0b013e3282f4a836 Zou S, Fitting S, Hahn YK, Welch SP, El-Hage N, Hauser KF, Knapp PE (2011) Morphine potentiates neurodegenerative effects of HIV-1 tat through actions at mu-opioid receptor-expressing glia. Brain 134:3616–3631. https://doi.org/10.1093/brain/awr281