Microglia activation-induced mesencephalic dopaminergic neurodegeneration — an in vitro model for Parkinson’s disease

Arimoto T, Bing G (2003). Up-regulation of inducible nitric oxide synthase in the substantia nigra by lipopolysaccharide causes microglial activation and neurodegeneration. Neurobiol Dis, 12(1): 35–45 Arimoto T, Choi D Y, Lu X, Liu M, Nguyen X V, Zheng N, Stewart C A, Kim H C, Bing G (2007). Interleukin-10 protects against inflammation-mediated degeneration of dopaminergic neurons in substantia nigra. Neurobiol Aging, 28(6): 894–906 Betarbet R, Sherer T B, MacKenzie G, Garcia-Osuna M, Panov A V, Greenamyre J T (2000). Chronic systemic pesticide exposure reproduces features of Parkinson’s disease. Nat Neurosci, 3(12): 1301–1306 Bing G Y, Lu N A, et al (1998). Microglia Mediaed Dopaminergic Cell Death in the Substantia nigra: a New Animal Model for Parkinson’s Disease. Neuroscience Abstracts Blandini F, Armentero M T (2012). Animal models of Parkinson’s disease. FEBS J, 279(7): 1156–1166 Block M L, Hong J S (2005). Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol, 76(2): 77–98 Boka G, Anglade P, Wallach D, Javoy-Agid F, Agid Y, Hirsch E C (1994). Immunocytochemical analysis of tumor necrosis factor and its receptors in Parkinson’s disease. Neurosci Lett, 172(1–2): 151–154 Brooks A I, Chadwick C A, Gelbard H A, Cory-Slechta D A, Federoff H J (1999). Paraquat elicited neurobehavioral syndrome caused by dopaminergic neuron loss. Brain Res, 823(1–2): 1–10 Cannon J R, Tapias V, Na HM, Honick A S, Drolet R E, Greenamyre J T (2009). A highly reproducible rotenone model of Parkinson’s disease. Neurobiol Dis, 34(2): 279–290 Carrasco E, Casper D, Werner P (2007). PGE(2) receptor EP1 renders dopaminergic neurons selectively vulnerable to low-level oxidative stress and direct PGE(2) neurotoxicity. J Neurosci Res, 85(14): 3109–3117 Castaño A, Herrera A J, Cano J, Machado A (1998). Lipopolysaccharide intranigral injection induces inflammatory reaction and damage in nigrostriatal dopaminergic system. J Neurochem, 70(4): 1584–1592 Choi D Y, Liu M, Hunter R L, Cass WA, Pandya J D, Sullivan P G, Shin E J, Kim H C, Gash D M, Bing G (2009). Striatal neuroinflammation promotes Parkinsonism in rats. PLoS ONE, 4(5): e5482 Choi W S, Eom D S, Han B S, Kim W K, Han B H, Choi E J, Oh T H, Markelonis G J, Cho J W, Oh Y J (2004). Phosphorylation of p38 MAPK induced by oxidative stress is linked to activation of both caspase-8- and -9-mediated apoptotic pathways in dopaminergic neurons. J Biol Chem, 279(19): 20451–20460 Dehmer T, Lindenau J, Haid S, Dichgans J, Schulz J B (2000). Deficiency of inducible nitric oxide synthase protects against MPTP toxicity in vivo. J Neurochem, 74(5): 2213–2216 Du Y, Ma Z, Lin S, Dodel R C, Gao F, Bales K R, Triarhou L C, Chernet E, Perry K W, Nelson D L, Luecke S, Phebus L A, Bymaster F P, Paul S M (2001). Minocycline prevents nigrostriatal dopaminergic neurodegeneration in the MPTP model of Parkinson’s disease. Proc Natl Acad Sci USA, 98(25): 14669–14674 Fontaine V, Mohand-Said S (2002). Neurodegenerative and neuroprotective effects of tumor necrosis factor (TNF) in retinal ischemia: opposite roles of TNF receptor 1 and TNF receptor 2. The Journal of neuroscience, 22(7): RC216 Gao H M, Jiang J, Wilson B, Zhang W, Hong J S, Liu B (2002). Microglial activation-mediated delayed and progressive degeneration of rat nigral dopaminergic neurons: relevance to Parkinson’s disease. J Neurochem, 81(6): 1285–1297 Gao H M, Kotzbauer P T (2008). Neuroinflammation and oxidation/nitration of alpha-synuclein linked to dopaminergic neurodegeneration. The Journal of neuroscience, 28(30): 7687–7698 Gao H M, Zhou H (2011). HMGB1 acts on microglia Mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration.” J Neurosci, 31(3): 1081–1092 Gao L, Zackert W E, Hasford J J, Danekis M E, Milne G L, Remmert C, Reese J, Yin H, Tai H H, Dey S K, Porter N A, Morrow J D (2003). Formation of prostaglandins E2 and D2 via the isoprostane pathway: a mechanism for the generation of bioactive prostaglandins independent of cyclooxygenase. J Biol Chem, 278(31): 28479–28489 Gayle D A, Ling Z, Tong C, Landers T, Lipton JW, Carvey P M (2002). Lipopolysaccharide (LPS)-induced dopamine cell loss in culture: roles of tumor necrosis factor-alpha, interleukin-1beta, and nitric oxide. Brain Res Dev Brain Res, 133(1): 27–35 Ghatan S, Larner S, Kinoshita Y, Hetman M, Patel L, Xia Z, Youle R J, Morrison R S (2000). p38 MAP kinase mediates bax translocation in nitric oxide-induced apoptosis in neurons. J Cell Biol, 150(2): 335–347 Gomez-Lazaro M, Galindo M F, Concannon C G, Segura M F, Fernandez-Gomez F J, Llecha N, Comella J X, Prehn J H, Jordan J (2008). 6-Hydroxydopamine activates the mitochondrial apoptosis pathway through p38 MAPK-mediated, p53-independent activation of Bax and PUMA. J Neurochem, 104(6): 1599–1612 Good P F, Hsu A, Werner P, Perl D P, Olanow C W (1998). Protein nitration in Parkinson’s disease. J Neuropathol Exp Neurol, 57(4): 338–342 Hald A, Lotharius J (2005). Oxidative stress and inflammation in Parkinson’s disease: is there a causal link? Exp Neurol, 193(2): 279–290 Hartmann A, Troadec J D, Hunot S, Kikly K, Faucheux B A, Mouatt-Prigent A, Ruberg M, Agid Y, Hirsch E C (2001). Caspase-8 is an effector in apoptotic death of dopaminergic neurons in Parkinson’s disease, but pathway inhibition results in neuronal necrosis. J Neurosci, 21(7): 2247–2255 He Y, Appel S, Le W (2001). Minocycline inhibits microglial activation and protects nigral cells after 6-hydroxydopamine injection into mouse striatum. Brain Res, 909(1–2): 187–193 Herrera A J, Castaño A, Venero J L, Cano J, Machado A (2000). The single intranigral injection of LPS as a new model for studying the selective effects of inflammatory reactions on dopaminergic system. Neurobiol Dis, 7(4): 429–447 Hodara R, Norris E H, Giasson B I, Mishizen-Eberz A J, Lynch D R, Lee V M, Ischiropoulos H (2004). Functional consequences of alphasynuclein tyrosine nitration: diminished binding to lipid vesicles and increased fibril formation. J Biol Chem, 279(46): 47746–47753 Hunot S, Boissière F, Faucheux B, Brugg B, Mouatt-Prigent A, Agid Y, Hirsch E C (1996). Nitric oxide synthase and neuronal vulnerability in Parkinson’s disease. Neuroscience, 72(2): 355–363 Hunot S, Dugas N (1999). FcepsilonRII/CD23 is expressed in Parkinson’s disease and induces, in vitro, production of nitric oxide and tumor necrosis factor-alpha in glial cells. The Journal of neuroscience, 19(9): 3440–3447 Hunter R L, Cheng B, Choi D Y, Liu M, Liu S, Cass W A, Bing G (2009). Intrastriatal lipopolysaccharide injection induces parkinsonism in C57/B6 mice. J Neurosci Res, 87(8): 1913–1921 Hunter R L, Dragicevic N, Seifert K, Choi D Y, Liu M, Kim H C, Cass W A, Sullivan P G, Bing G (2007). Inflammation induces mitochondrial dysfunction and dopaminergic neurodegeneration in the nigrostriatal system. J Neurochem, 100(5): 1375–1386 Iravani M M, Kashefi K, Mander P, Rose S, Jenner P (2002). Involvement of inducible nitric oxide synthase in inflammationinduced dopaminergic neurodegeneration. Neuroscience, 110(1): 49–58 Jenner P, Olanow C W (1996). Oxidative stress and the pathogenesis of Parkinson’s disease. Neurology, 47(6 Suppl 3): S161-S170 Kim W G, Mohney R P (2000). Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J Neurosci, 20(16): 6309–6316 Kirik D, Rosenblad C, Björklund A (1998). Characterization of behavioral and neurodegenerative changes following partial lesions of the nigrostriatal dopamine system induced by intrastriatal 6-hydroxydopamine in the rat. Exp Neurol, 152(2): 259–277 Knott C, Stern G, Wilkin G P (2000). Inflammatory regulators in Parkinson’s disease: iNOS, lipocortin-1, and cyclooxygenases-1 and-2. Mol Cell Neurosci, 16(6): 724–739 Langston J W, Ballard P, Tetrud J W, Irwin I (1983). Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science, 219(4587): 979–980 Lapointe N, St-Hilaire M (2004). Rotenone induces non-specific central nervous system and systemic toxicity. FASEB journal, 18(6): 717–719 Li R, Yang L (2004). Tumor necrosis factor death receptor signaling cascade is required for amyloid-beta protein-induced neuron death. The Journal of neuroscience, 24(7): 1760–1771 Liberatore G T, Jackson-Lewis V, Vukosavic S, Mandir A S, Vila M, McAuliffe W G, Dawson V L, Dawson T M, Przedborski S (1999). Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nat Med, 5(12): 1403–1409 Loeffler D A, DeMaggio A J, Juneau P L, Havaich M K, LeWitt P A (1994). Effects of enhanced striatal dopamine turnover in vivo on glutathione oxidation. Clin Neuropharmacol, 17(4): 370–379 Long-Smith C M, Collins L, Toulouse A, Sullivan A M, Nolan Y M (2010). Interleukin-1β contributes to dopaminergic neuronal death induced by lipopolysaccharide-stimulated rat glia in vitro. J Neuroimmunol, 226(1–2): 20–26 Lozano A M, Lang A E, Hutchison W D, Dostrovsky J O (1998). New developments in understanding the etiology of Parkinson’s disease and in its treatment. Curr Opin Neurobiol, 8(6): 783–790 Marchetti L, Klein M, Schlett K, Pfizenmaier K, Eisel U L (2004). Tumor necrosis factor (TNF)-mediated neuroprotection against glutamate-induced excitotoxicity is enhanced by N-methyl-Daspartate receptor activation. Essential role of a TNF receptor 2-mediated phosphatidylinositol 3-kinase-dependent NF-kappa B pathway. J Biol Chem, 279(31): 32869–32881 McCoy M K, Martinez T N (2006). Blocking soluble tumor necrosis factor signaling with dominant-negative tumor necrosis factor inhibitor attenuates loss of dopaminergic neurons in models of Parkinson’s disease. The Journal of neuroscience, 26(37): 9365–9375 McGeer P L, Itagaki S, Akiyama H, McGeer E G (1988a). Rate of cell death in parkinsonism indicates active neuropathological process. Ann Neurol, 24(4): 574–576 McGeer P L, Itagaki S, Boyes B E, McGeer E G (1988b). Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson’s and Alzheimer’s disease brains. Neurology, 38(8): 1285–1291 McGeer P L, Schwab C, Parent A, Doudet D (2003). Presence of reactive microglia in monkey substantia nigra years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine administration. Ann Neurol, 54(5): 599–604 Mogi M, Harada M, Kondo T, Riederer P, Inagaki H, Minami M, Nagatsu T (1994a). Interleukin-1 beta, interleukin-6, epidermal growth factor and transforming growth factor-alpha are elevated in the brain from parkinsonian patients. Neurosci Lett, 180(2): 147–150 Mogi M, Harada M, Riederer P, Narabayashi H, Fujita K, Nagatsu T (1994b). Tumor necrosis factor-alpha (TNF-alpha) increases both in the brain and in the cerebrospinal fluid from parkinsonian patients. Neurosci Lett, 165(1–2): 208–210 Mogi M, Togari A, Kondo T, Mizuno Y, Komure O, Kuno S, Ichinose H, Nagatsu T (2000). Caspase activities and tumor necrosis factor receptor R1 (p55) level are elevated in the substantia nigra from parkinsonian brain. J Neural Transm, 107(3): 335–341 Murray J, Taylor S W, Zhang B, Ghosh S S, Capaldi R A (2003). Oxidative damage to mitochondrial complex I due to peroxynitrite: identification of reactive tyrosines by mass spectrometry. J Biol Chem, 278(39): 37223–37230 Nagatsu T, Mogi M, Ichinose H, Togari A (2000). Changes in cytokines and neurotrophins in Parkinson’s disease. J Neural Transm Suppl, (60): 277–290 Nakamura Y (2002). Regulating factors for microglial activation. Biol Pharm Bull, 25(8): 945–953 Olanow C W, Tatton W G (1999). Etiology and pathogenesis of Parkinson’s disease. Annu Rev Neurosci, 22(1): 123–144 Pawate S, Shen Q, Fan F, Bhat N R (2004). Redox regulation of glial inflammatory response to lipopolysaccharide and interferongamma. J Neurosci Res, 77(4): 540–551 Paxinou E, Chen Q (2001). Induction of alpha-synuclein aggregation by intracellular nitrative insult. The Journal of neuroscience, 21(20): 8053–8061 Perese D A, Ulman J, Viola J, Ewing S E, Bankiewicz K S (1989). A 6-hydroxydopamine-induced selective parkinsonian rat model. Brain Res, 494(2): 285–293 Przedborski S, Chen Q, Vila M, Giasson B I, Djaldatti R, Vukosavic S, Souza J M, Jackson-Lewis V, Lee V M, Ischiropoulos H (2001). Oxidative post-translational modifications of alpha-synuclein in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) mouse model of Parkinson’s disease. J Neurochem, 76(2): 637–640 Przedborski S, Levivier M, Jiang H, Ferreira M, Jackson-Lewis V, Donaldson D, Togasaki D M (1995). Dose-dependent lesions of the dopaminergic nigrostriatal pathway induced by intrastriatal injection of 6-hydroxydopamine. Neuroscience, 67(3): 631–647 Qin L, Liu Y, Wang T, Wei S J, Block M L, Wilson B, Liu B, Hong J S (2004). NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proinflammatory gene expression in activated microglia. J Biol Chem, 279(2): 1415–1421 Ransohoff R M, Perry V H (2009). Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol, 27(1): 119–145 Shavali S, Combs C K, Ebadi M (2006). Reactive macrophages increase oxidative stress and alpha-synuclein nitration during death of dopaminergic neuronal cells in co-culture: relevance to Parkinson’s disease. Neurochem Res, 31(1): 85–94 Sherer T B, Kim J H, Betarbet R, Greenamyre J T (2003). Subcutaneous rotenone exposure causes highly selective dopaminergic degeneration and alpha-synuclein aggregation. Exp Neurol, 179(1): 9–16 Sherer T B, Richardson J R, Testa C M, Seo B B, Panov A V, Yagi T, Matsuno-Yagi A, Miller GW, Greenamyre J T (2007). Mechanism of toxicity of pesticides acting at complex I: relevance to environmental etiologies of Parkinson’s disease. J Neurochem, 100(6): 1469–1479 Tiwari M, Lopez-Cruzan M, Morgan W W, Herman B (2011). Loss of caspase-2-dependent apoptosis induces autophagy after mitochondrial oxidative stress in primary cultures of young adult cortical neurons. J Biol Chem, 286(10): 8493–8506 Vijitruth R, Liu M, Choi D Y, Nguyen X V, Hunter R L, Bing G (2006). Cyclooxygenase-2 mediates microglial activation and secondary dopaminergic cell death in the mouse MPTP model of Parkinson’s disease. J Neuroinflammation, 3(1): 6 Wang, T., Pei, Z., et al (2005). MPP+-induced COX-2 activation and subsequent dopaminergic neurodegeneration. FASEB journal, 19(9): 1134–1136 Wu D C, Jackson-Lewis V, Vila M, Tieu K, Teismann P, Vadseth C, Choi D K, Ischiropoulos H, Przedborski S (2002). Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J Neurosci, 22(5): 1763–1771 Wu D C, Teismann P, Tieu K, Vila M, Jackson-Lewis V, Ischiropoulos H, Przedborski S (2003). NADPH oxidase mediates oxidative stress in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson’s disease. Proc Natl Acad Sci USA, 100(10): 6145–6150 Xing B, Liu M, Bing G (2007). Neuroprotection with pioglitazone against LPS insult on dopaminergic neurons may be associated with its inhibition of NF-kappaB and JNK activation and suppression of COX-2 activity. J Neuroimmunol, 192(1–2): 89–98 Xing B, Xin T, Hunter R L, Bing G (2008). Pioglitazone inhibition of lipopolysaccharide-induced nitric oxide synthase is associated with altered activity of p38 MAP kinase and PI3K/Akt. J Neuroinflammation, 5(1): 4 Zhang F, Shi J S, Zhou H, Wilson B, Hong J S, Gao H M (2010). Resveratrol protects dopamine neurons against lipopolysaccharideinduced neurotoxicity through its anti-inflammatory actions. Mol Pharmacol, 78(3): 466–477 Zhang J, Perry G, Smith M A, Robertson D, Olson S J, Graham D G, Montine T J (1999). Parkinson’s disease is associated with oxidative damage to cytoplasmic DNA and RNA in substantia nigra neurons. Am J Pathol, 154(5): 1423–1429 Zhang J, Stanton D M, Nguyen X V, Liu M, Zhang Z, Gash D, Bing G (2005). Intrapallidal lipopolysaccharide injection increases iron and ferritin levels in glia of the rat substantia nigra and induces locomotor deficits. Neuroscience, 135(3): 829–838 Zhang W, Wang T (2005). Aggregated alpha-synuclein activates microglia: a process leading to disease progression in Parkinson’s disease. FASEB journal, 19(6): 533–542