Cannabinoid rescue of striatal progenitor cells in chronic Borna Disease viral encephalitis in rats

References

• Aguado T, Monory K, Palazuelos J, Stella N, Cravatt B, Lutz B, Marsicano G, Kokaia Z, Guzman M, Galve-Roperh I. The endocannabinoid system drives neural progenitor proliferation. FASEB J 2005; 19: 1704–1706
   PubMed Web of Science ®Google Scholar
• Aguado T, Romero E, Monory K, Palazuelos J, Sendtner M, Marsicano G, Lutz B, Guzman M, Galve-Roperh I. The CB1 cannabinoid receptor mediates excitotoxicity-induced neural progenitor proliferation and neurogenesis. J Biol Chem 2007; 282: 23892–23898
   Google Scholar
• Anthony I C, Crawford D H, Bell J E. Effects of human immunodeficiency virus encephalitis and drug abuse on the B lymphocyte population of the brain. J NeuroVirol 2004; 10: 181–188
   Web of Science ®Google Scholar
• Anthony I C, Ramage S N, Carnie F W, Simmonds P, Bell J E. Does drug abuse alter microglial phenotype and cell turnover in the context of advancing HIV infection?. Neuropathol Appl Neurobiol 2005; 31: 325–338
   PubMed Web of Science ®Google Scholar
• Arango J-C, Simmonds P, Brettle R P, Bell J E. Does drug abuse influence the microglial response in AIDS and HIV encephalitis?. AIDS 2004; 18(Suppl 1)S69–S74
   Google Scholar
• Bagri A, Gurney T, He X, Zou Y R, Littman D R, Tessier-Lavigne M, Pleasure S J. The chemokine SDF1 regulates migration of dentate granule cells. Development 2002; 129: 4249–4260
   PubMed Web of Science ®Google Scholar
• Bauer J, Sminia T, Wouterlood F G, Dijkstra C D. Phagocytic activity of macrophages and microglial cells during the course of acute and chronic relapsing experimental autoimmune encephalomyelitis. J Neurosci Res 1994; 38: 365–375
   Google Scholar
• Bautista J R, Schwartz G J, de la Torre J C, Moran T H, Carbone K M. Early and persistent abnormalities in rats with neonatally acquired Borna disease virus infection. Brain Res Bull 1994; 34: 31–40
   PubMed Web of Science ®Google Scholar
• Benito C, Kim W K, Chavarria I, Hillard C J, Mackie K, Tolon R M, Williams K, Romero J. A glial endogenous cannabinoid system is upregulated in the brains of macaques with simian immunodeficiency virus-induced encephalitis. J Neurosci 2005; 25: 2530–2536
   PubMed Web of Science ®Google Scholar
• Billaud J N, Ly C, Philips T R, de la Torre J C. Borna disease virus persistence causes inhibition of glutamate uptake by feline primary cortical astrocytes. J Virol 2000; 74: 10438–10446
   PubMed Web of Science ®Google Scholar
• Bilzer T, Stitz L. Immune-mediated brain atrophy. CD8+ T cells contribute to tissue destruction during borna disease. J Immunol 1994; 153: 818–823
   Google Scholar
• Carbone K M, Moench T R, Lipkin W I. Borna disease virus replicates in astrocytes, Schwann cells and ependymal cells in persistently infected rats: location of viral genomic and messenger RNAs by in situ hybridization. J Neuropathol Exp Neurol 1991; 50: 205–214
   Google Scholar
• Carbone K M, Trapp B D, Griffin J W, Duchala C S, Narayan O. Astrocytes and Schwann cells are virus-host cells in the nervous system of rats with Borna disease. J Neuropathol Exp Neurol 1989; 48: 631–644
   Google Scholar
• Centonze D, Bari M, Rossi S, Prosperetti C, Furlan R, Fezza F, De Chiara V, Battistini L, Bernardini G, Bernardini S, Martino G, Maccarrone M. The endocannabinoid system is dysregulated in multiple sclerosis and in experimental autoimmune encephalomyelitis. Brain 2007; 130: 2543–2553
   PubMed Web of Science ®Google Scholar
• Cherner M, Letendre S, Heaton R K, Durelle J, Marquie-Beck J, Gragg B, Grant, HNRC Group. Hepatitis C augments cognitive deficits associated with HIV infection and methamphetamine. Neurology 2005; 64: 1343–1347
   PubMed Web of Science ®Google Scholar
• Crews F T, Nixon K. Alcoholism, neural stem cells, and adult neurogenesis. Alcohol Res Health 2003; 27: 197–204
   PubMedGoogle Scholar
• Curtis M A, Faull R L, Glass M. A novel population of progenitor cells expressing cannabinoid receptors in the subependymal layer of the adult normal and Huntington's disease human brain. J Chem Neuroanat 2006; 31: 210–215
   PubMed Web of Science ®Google Scholar
• Czub S, Czub M, Koutsilieri E, Sopper S, Villinger F, Muller J G, Stahl-Hennig C, Riederer P, ter Meulen V, Gosztonyi G. Modulation of simian immunodeficiency virus neuropathology by dopaminergic drugs. Acta Neuropathol 2004; 107: 216–226
   Google Scholar
• Dietz D, Vogel M, Rubin S, Moran T, Carbone K, Pletnikov M. Developmental alterations in serotoninergic neurotransmission in Borna disease virus (BDV)-infected rats: a multidisciplinary analysis. J NeuroVirol 2004; 10: 267–277
   Web of Science ®Google Scholar
• Dominguez-Escriba L, Hernandez-Rabaza V, Soriano-Navarro M, Romero F J, Garcia-Verdugo J M, Canales J J. Chronic cocaine exposure impairs progenitor proliferation but spares survival and maturation of neural precursors in adult rat dentate gyrus. Eur J Neurosci 2006; 24: 586–594
   Google Scholar
• Ehrhart J, Obregon D, Mori T, Hou H, Sun N, Bai Y, Klein T, Fernandez F, Tan J, Shytle R D. Stimulation of cannabinoid receptor (CB2) suppresses microglial activation. J Neuroinflamm 2005; 2: 29
   PubMed Web of Science ®Google Scholar
• Eisch A J, Barrot M, Schad C A, Self D W, Nestler E J. Opiates inhibit neurogenesis in the adult rat hippocampus. Proc Natl Acad Sci U S A 2000; 97: 7579–7584
   PubMed Web of Science ®Google Scholar
• Eisch A J, Harburg G C. Opiates, psychostimulants, and adult hippocampal neurogenesis: insights for addiction and stem cell biology. Hippocampus 2006; 16: 271–286
   Google Scholar
• Ekdahl C T, Claasen J-H, Bonde S, Kokaia Z, Lindvall O. Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci U S A 2003; 100: 13632–13637
   PubMed Web of Science ®Google Scholar
• El-Hage N, Wu G, Wang J, Ambati J, Knapp P E, Reed J L, Bruce-Keller A J, Hauser K F. HIV-1 Tat and opiate-induced changes in astrocytes promote chemotaxis of microglia through the expression of MCP-1 and alternative chemokines. Glia 2006; 53: 132–146
   Web of Science ®Google Scholar
• Fu Z F, Weihe E, Zheng Y M, Schafer M K, Sheng H, Corisdeo S, Rauscher F J, 3rd, Koprowski H, Dietzschold B. Differential effects of rabies and borna disease viruses on immediate-early- and late-response gene expression in brain tissues. J Virol 1993; 67: 6674–6681
   PubMed Web of Science ®Google Scholar
• Garcia-Arencibia M, Gonzalez S, de Lago E, Ramos J A, Mechoulam R, Fernandez-Ruiz J. Evaluation of the neuroprotective effect of cannabinoids in a rat model of Parkinson's disease: importance of antioxidant and cannabinoid receptor-independent properties. Brain Res 2007; 1134: 162–170
   PubMed Web of Science ®Google Scholar
• Gavrilin M A, Mathes L E, Podell M. Methamphetamine enhances cell-associated feline immunodeficiency virus replication in astrocytes. J NeuroVirol 2002; 8: 240–249
   PubMed Web of Science ®Google Scholar
• Gonzalez-Dunia D, Watanabe M, Syan S, Mallory M, Masliah E, De La Torre J C. Synaptic pathology in Borna disease virus persistent infection. J Virol 2000; 74: 3441–3448
   Google Scholar
• Gosztonyi G, Ludwig H. Borna disease-neuropathology and pathogenesis. Curr Top Microbiol Immunol 1995; 190: 39–73
   PubMed Web of Science ®Google Scholar
• Gosztonyi G, Ludwig H. Interactions of viral proteins with neurotransmitter receptors may protect or destroy neurons. Curr Top Microbiol Immunol 2001; 253: 121–144
   Google Scholar
• Guindon J, Hohmann A G. Cannabinoid CB2 receptors: a therapeutic target for the treatment of inflammatory and neuropathic pain. Br J Pharmacol 2008; 153: 319–334
   PubMed Web of Science ®Google Scholar
• Guzman M, Galve-Roperh I. Cannabinoids and cell fate. Pharmacol Ther 2002; 95: 175–184
   PubMed Web of Science ®Google Scholar
• Haas B, Becht H, Rott R. Purification and properties of an intranuclear virus-specific antigen from tissue infected with Borna Disease virus. J Gen Virol 1986; 67: 235–241
   Google Scholar
• Hajos N, Freund T F. Pharmacological separation of cannabinoid-sensitive receptors on hippocampal excitatory and inhibitory fibers. Neuropharmacology 2002; 43: 503–510
   PubMed Web of Science ®Google Scholar
• Hans A, Bajramovic J J, Syan S, Perret E, Dunia I, Brahic M, Gonzalez-Dunia D. Persistent non-cytolytic infection of neurons by Borna disease virus interferes with ERK 1/2 signaling and abrogates BDNF-induced synaptogenesis. FASEB J 2004; 18: 863–865
   Google Scholar
• Harkany T, Guzman M, Galve-Roperh I, Berghuis P, Devi L A, Mackie K. The emerging functions of endocannabinoid signaling during CNS development. Trends Pharmacol Sci 2007; 28: 83–92
   PubMed Web of Science ®Google Scholar
• Hauser K F, El-Hage N, Buch S, Berger J R, Tyor W R, Nath A, Brude-Keller A J, Knapp P E. Molecular targets of opiate drug abuse in neuroAIDS. Neurotox Res 2005; 8: 63–80
   Web of Science ®Google Scholar
• Hornig M, Weissenbock H, Horscroft N, Lipkin W I. An infection-based model of neurodevelopmental damage. Proc Natl Acad Sci U S A 1999; 96: 12102–12107
   PubMed Web of Science ®Google Scholar
• Jhaveri M D, Sagar D R, Elmes S JR, Kendall D A, Chapman V. Cannabinoid CB2 receptor-mediated anti-nociception in models of acute and chronic pain. Mol Neurobiol 2007; 36: 26–35
   PubMed Web of Science ®Google Scholar
• Jiang W, Zhang Y, Xiao L, Van Cleemput J, Ji S P, Bai G, Zhang X. Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic- and antidepressant-like effects. J Clin Invest 2005; 115: 3104–3016
   PubMed Web of Science ®Google Scholar
• Jin K, Xie L, Kim S H, Parmentier-Batteur S, Sun Y, Mao X O, Childs J, Greenberg D A. Defective adult neurogenesis in CB1 cannabinoid receptor knockout mice. Mol Pharmacol 2004; 66: 204–208
   PubMed Web of Science ®Google Scholar
• Kamitani W, Shoya Y, Kobayashi T, Watanabe M, Lee B J, Zhang G, Tomonaga K, Ikuta K. Borna disease virus phosphoprotein binds a neurite outgrowth factor, amphoterin/HMG-1. J Virol 2001; 75: 8742–8751
   Google Scholar
• Kuhn H G, Dickinson-Anson H, Gage F H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor population. J Neurosci 1996; 16: 2027–2033
   PubMed Web of Science ®Google Scholar
• Langford D, Adame A, Grigorian A, Grant I, McCutchan J A, Ellis R J, Marcotte T D, Masliah E, HNRC Group. Patterns of selective neuronal damage in methamphetamine-user AIDS patients. J Acquir Immune Defic Syndr 2003; 34: 467–474
   PubMed Web of Science ®Google Scholar
• LoVerme J, Russo R, La Rana G, Fu J, Farthing J, Mattace-Raso G, Meli R, Hohmann A, Calignano A, Piomelli D. Rapid broad-spectrum analgesia through activation of peroxisome proliferators-activated receptor-alpha. J Pharmacol Exp Ther 2006; 319: 1051–1061
   PubMed Web of Science ®Google Scholar
• Lu M, Grove E A, Miller R J. Abnormal development of the hippocampal dentate gyrus in mice lacking the CXCR4 chemokine receptor. Proc Natl Acad Sci U S A 2002; 99: 7090–7095
   PubMed Web of Science ®Google Scholar
• Mackie K, Stella N. Cannabinoid receptors and endocannabinoids: evidence for new players. AAPS J 2006; 8: E298–E306
   PubMed Web of Science ®Google Scholar
• Mayer D, Fisher H, Schneider U, Heimrich B, Schwemmle M. Borna disease virus replication in organotypic hippocampal slice cultures from rats results in selective damage of dentate granule cells. J Virol 2005; 79: 11716–11723
   Google Scholar
• McCoy K L, Gainey D, Cabral G A. Delta 9-tetrahydrocannabinol modulates antigen processing by macrophages. J Pharmacol Exp Ther 1995; 273: 1216–1223
   PubMed Web of Science ®Google Scholar
• McCoy K L, Matveyeva M, Carlisle S J, Cabral G A. Cannabinoid inhibition of the processing of intact lysozyme by macrophages: evidence for CB2 receptor participation. J Pharmacol Exp Ther 1999; 289: 1620–1625
   PubMed Web of Science ®Google Scholar
• Mechoulam R, Panikashvili D, Shohami E. Cannabinoids and brain injury: therapeutic implications. Trends Mol Med 2002; 8: 58–61
   PubMed Web of Science ®Google Scholar
• Miller A M, Stella N. CB2 receptor-mediated migration of immune cells: it can go either way. Br J Pharmacol 2008; 158: 299–308
   Google Scholar
• Molina P E, McNurlan M, Rathmacher J, Lang C H, Zambell K L, Purcell J, Bohm R P, Zhang P, Bagby G J, Nelson S. Chronic alcohol accentuates nutritional, metabolic, and immune alterations during asymptomatic simian immunodeficiency virus infection. Alcohol Clin Exp Res 2006; 30: 2065–2078
   Google Scholar
• Monje M L, Toda H, Palmer T D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003; 302: 1760–1765
   PubMed Web of Science ®Google Scholar
• Morgese M G, Cassano T, Cuomo V, Giuffrida A. Anti-dyskinetic effects of cannabinoids in a rat model of Parkinson's disease: Role of CB1 and TRPV1 receptors. Exp Neurol 2007; 208: 110–119
   PubMed Web of Science ®Google Scholar
• Narayan O, Herzog S, Frese K, Scheefers H, Rott R. Behavioral disease in rats caused by immunopathological responses to persistent borna virus in the brain. Science 1983; 220: 1401–1403
   PubMed Web of Science ®Google Scholar
• Nilsson O, Fowler C J, Jacobsson S O. The cannabinoid agonist WIN 55212-2 inhibits TNF alpha-induced neutrophil transmigration across ECV304 cells. Eur J Pharmacol 2006; 547: 165–173
   Google Scholar
• Paxinos G, Watson C. The rat brain in stereotaxic coordinates, 4th ed. Academic Press, San Diego 1998
   Google Scholar
• Perez-Casanova A, Noel R J, Jr, Rivera-Amill V, Husain K, Kumar A. Morphine-mediated deterioration of oxidative stress leads to rapid disease progression in SIV/SHIV-infected macaques. AIDS Res Hum Retroviruses 2007; 23: 1004–1007
   Google Scholar
• Planz O, Stitz L. Borna disease virus nucleoprotein (p40) is a major target for CD8(+)-T-cell-mediated immune response. J Virol 1999; 73: 1715–1718
   Google Scholar
• Pletnikov M V, Moran T H, Carbone K M. Borna disease virus infection of the neonatal rat: developmental brain injury model of autism spectrum disorders. Front Biosci 2002; 7: d593–607
   Google Scholar
• Pryce G, Ahmed Z, Hankey D JR, Jackson S J, Corxford J L, Pocock J M, Ledent C, Petzold A, Thompson A J, Giovannoni G, Cuzner M L, Baker D. Cannabinoids inhibit neurodegeneration in models of multiple sclerosis. Brain 2003; 126: 2191–2202
   PubMed Web of Science ®Google Scholar
• Rippeth J D, Heaton R K, Carey C L, Marcotte T D, Moore D J, Gonzalez R, Wolfson T, Grant, HNRC Group. Methamphetamine dependence increases risk of neuropsychological impairment in HIV infected persons. J Int Neuropsychol Soc 2004; 10: 1–14
   PubMed Web of Science ®Google Scholar
• Sagredo O, Garcia-Arencibia M, de Lago E, Finetti S, Decio A, Fernandez-Ruiz J. Cannabinoids and neuroprotection in basal ganglia disorders. Mol Neurobiol 2007; 36: 82–91
   PubMed Web of Science ®Google Scholar
• Sanchez A J, Gonzalez-Perez P, Galve-Roperh I, Garcia-Merino A. R-(+)-[2,3-dihydro-5-methyl-3-(4-morpholinylmethyl)-pyrrolo-[1,2,3-de]-1,4-benzoxazin-6-yl]-1-naphtalenylmethanone (WIN-2) ameliorates experimental autoimmune encephalomyelitis and induces encephalitogenic T cell apoptosis: partial involvement of the CB(2) receptor. Biochem Pharmacol 2006; 72: 1697–1706
   PubMed Web of Science ®Google Scholar
• Sasaki S, Ludwig H. In borna disease virus infected rabbit neurons 100 nm particle structures accumulate at areas of Joest-Degen inclusion bodies. Zentralbl Veterinarmed B 1993; 40: 291–297
   Google Scholar
• Solbrig M V, Adrian R, Baratta J, Lauterborne J, Koob G F. Kappa opioid control of seizures by a virus in an animal model. Brain 2006; 129: 642–654
   Google Scholar
• Solbrig M V, Adrian R, Baratta J, Piomelli D, Giuffrida A. Role for endocannabinoids in viral-induced dyskinetic and convulsive phenomena. Exp Neurol 2005; 194: 355–362
   Google Scholar
• Solbrig M V, Koob G F. Neuropharmacological sequelae of Borna Disease Virus. Pharmacol Biochem Behav 2003; 74: 777–787
   Google Scholar
• Solbrig M V, Koob G F, Fallon J H, Lipkin W I. Tardive dyskinetic syndrome in rats infected with Borna disease virus. Neurobiol Dis 1994; 1: 111–119
   Google Scholar
• Solbrig M V, Koob G F, Lipkin W I. Cocaine sensitivity in Borna disease virus-infected rats. Pharmacol Biochem Behavior 1998; 59: 1047–1052
   Google Scholar
• Solbrig M V, Koob G F, Lipkin W I. Key role for enkephalinergic tone in cortico-striatal-thalamic function. Eur J Neurosci 2002a; 16: 1819–1822
   Google Scholar
• Solbrig M V, Koob G F, Parsons L H, Horscroft N, Kadota T, Briese T, Lipkin W I. Neurotrophic factor expression following CNS viral injury produces enhanced sensitivity to psychostimulants: potential mechanism for addiction vulnerability. J Neurosci 2000; 20(RC104)1–6
   Google Scholar
• Solbrig M V, Schlaberg R, Briese T, Horscroft N, Lipkin W I. Neuroprotection and reduced proliferation of microglia in ribavirin-treated bornavirus-infected rats. Antimicrob Agents Chemother 2002b; 46: 2287–2291
   Google Scholar
• Stitz L, Bilzer T, Planz O. The immunopathogenesis of Borna disease virus infection. Front Biosci 2002; 7: d541–555
   Web of Science ®Google Scholar
• Stumm R K, Zhou C, Ara T, Lazarini F, Dubois-Dalcq M, Nagasawa T, Hollt V, Schulz S. CXCR4 regulates interneuron migration in the developing neocortex. J Neurosci 2003; 23: 5123–5130
   PubMed Web of Science ®Google Scholar
• Venkatesan A, Nath A, Ming G L, Song H. Adult hippocampal neurogenesis: regulation by HIV and drugs of abuse. Cell Mol Life Sci 2007; 64: 2120–2132
   Google Scholar
• Wahner A D, Bronstein J M, Bordelon Y M, Ritz B. Nonsteroidal anti-inflammatory drugs may protect against Parkinson disease. Neurology 2007; 69: 1836–1842
   PubMed Web of Science ®Google Scholar
• Walter L, Stella N. Cannabinoids and neuroinflammation. Br J Pharmacol 2004; 141: 775–785
   PubMed Web of Science ®Google Scholar
• Welch S P, Huffman J W, Lowe J. Differential blockade of the antinociceptive effects of centrally administered cannabinoids by SR141716A. J Pharmacol Exp Ther 1998; 286: 1301–1308
   PubMed Web of Science ®Google Scholar
• Williams B L, Hornig M, Yaddanapudi K, Lipkin W I. Hippocampal PARP-1 and caspase-3 activation in neonatal Bornavirus infection. J Virol 2008; 82: 1748–1758
   Google Scholar
• Williams B L, Yaddanapudi K, Kirk C M, Soman A, Hornig M, Lipkin W I. Metallothioneins and zinc dysregulation contribute to neurodevelopmental damage in a model of perinatal viral infection. Brain Pathol 2006; 16: 1–14
   Google Scholar
• Witting A, Chen L, Cudaback E, Straiker A, Walter L, Rickman B, Moller T, Brosnan C, Stella N. Experimental autoimmune encephalomyelitis disrupts endocannabinoid-mediated neuroprotection. Proc Natl Acad Sci U S A 2006; 103: 6362–6367
   PubMed Web of Science ®Google Scholar
• Yamaguchi M, Suzuki T, Seki T, Namba T, Juan R, Arai H, Hori T, Asada T. Repetitive cocaine administration decreases neurogenesis in adult rat hippocampus. Ann N Y Acad Sci 2004; 1025: 351–362
   Google Scholar