The role of the MYD88-dependent pathway in MPTP-induced brain dopaminergic degeneration

Journal of Neuroinflammation

Volumn 8, Issue , 2011, Pages

  Drouin Ouellet, Janelle ^a   Gibrat, Claire ^a   Bousquet, Mélanie ^a   Calon, Frédéric ^a,b   Kriz, Jasna ^a,b   Cicchetti, Francesca ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

Dopamine; Inflammation; MPTP; Myd88; Parkinson's disease

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; DOPAMINE; DOPAMINE TRANSPORTER; MYELOID DIFFERENTIATION FACTOR 88; TYROSINE 3 MONOOXYGENASE; 3,4 DIHYDROXYPHENYLACETIC ACID; GLIAL FIBRILLARY ACIDIC PROTEIN; MYD88 PROTEIN, MOUSE; NEUROTOXIN; TOLL LIKE RECEPTOR;

ANATOMICAL VARIATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL DENSITY; CELL LOSS; CONTROLLED STUDY; CORPUS STRIATUM; IMMUNOPATHOGENESIS; INFLAMMATION; INNATE IMMUNITY; MICROGLIA; MOUSE; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA PARS COMPACTA; WILD TYPE; ANIMAL; AUTORADIOGRAPHY; C57BL MOUSE; CYTOLOGY; DOPAMINERGIC NERVE CELL; DRUG EFFECT; GENETICS; HUMAN; INTOXICATION; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; SUBSTANTIA NIGRA;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; 3,4-DIHYDROXYPHENYLACETIC ACID; ANIMALS; ASTROCYTES; AUTORADIOGRAPHY; CORPUS STRIATUM; DOPAMINE; DOPAMINERGIC NEURONS; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MPTP POISONING; MYELOID DIFFERENTIATION FACTOR 88; NEUROTOXINS; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA; TOLL-LIKE RECEPTORS;

EID: 80053634031     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-8-137     Document Type: Article

References (80)

1. Hirsch EC, Hunot S. Neuroinflammation in Parkinson's disease: a target for neuroprotection?. Lancet Neurol 2009, 8:382-397. 10.1016/S1474-4422(09)70062-6, 19296921.
2. McGeer PL, McGeer EG. Inflammation and the degenerative diseases of aging. Ann N Y Acad Sci 2004, 1035:104-116. 10.1196/annals.1332.007, 15681803.
3. Banati RB, Daniel SE, Blunt SB. Glial pathology but absence of apoptotic nigral neurons in long-standing Parkinson's disease. Mov Disord 1998, 13:221-227. 10.1002/mds.870130205, 9539333.
4. Boka G, Anglade P, Wallach D, Javoy-Agid F, Agid Y, Hirsch EC. Immunocytochemical analysis of tumor necrosis factor and its receptors in Parkinson's disease. Neurosci Lett 1994, 172:151-154. 10.1016/0304-3940(94)90684-X, 8084523.
5. Damier P, Hirsch EC, Zhang P, Agid Y, Javoy-Agid F. Glutathione peroxidase, glial cells and Parkinson's disease. Neuroscience 1993, 52:1-6. 10.1016/0306-4522(93)90175-F, 8433802.
6. Hunot S, Boissiere F, Faucheux B, Brugg B, Mouatt-Prigent A, Agid Y, Hirsch EC. Nitric oxide synthase and neuronal vulnerability in Parkinson's disease. Neuroscience 1996, 72:355-363. 10.1016/0306-4522(95)00578-1, 8737406.
7. Hunot S, Dugas N, Faucheux B, Hartmann A, Tardieu M, Debre P, Agid Y, Dugas B, Hirsch EC. FcepsilonRII/CD23 is expressed in Parkinson's disease and induces, in vitro, production of nitric oxide and tumor necrosis factor-alpha in glial cells. J Neurosci 1999, 19:3440-3447.
8. Imamura K, Hishikawa N, Sawada M, Nagatsu T, Yoshida M, Hashizume Y. Distribution of major histocompatibility complex class II-positive microglia and cytokine profile of Parkinson's disease brains. Acta Neuropathol 2003, 106:518-526. 10.1007/s00401-003-0766-2, 14513261.
9. Knott C, Stern G, Wilkin GP. Inflammatory regulators in Parkinson's disease: iNOS, lipocortin-1, and cyclooxygenases-1 and -2. Mol Cell Neurosci 2000, 16:724-739. 10.1006/mcne.2000.0914, 11124893.
10. McGeer PL, Itagaki S, Boyes BE, McGeer EG. Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 1988, 38:1285-1291.
11. Mogi M, Harada M, Kondo T, Narabayashi H, Riederer P, Nagatsu T. Transforming growth factor-beta 1 levels are elevated in the striatum and in ventricular cerebrospinal fluid in Parkinson's disease. Neurosci Lett 1995, 193:129-132. 10.1016/0304-3940(95)11686-Q, 7478158.
12. Mogi M, Harada M, Kondo T, Riederer P, Inagaki H, Minami M, Nagatsu T. Interleukin-1 beta, interleukin-6, epidermal growth factor and transforming growth factor-alpha are elevated in the brain from parkinsonian patients. Neurosci Lett 1994, 180:147-150. 10.1016/0304-3940(94)90508-8, 7700568.
13. Mogi M, Harada M, Kondo T, Riederer P, Nagatsu T. Brain beta 2-microglobulin levels are elevated in the striatum in Parkinson's disease. J Neural Transm Park Dis Dement Sect 1995, 9:87-92. 10.1007/BF02252965, 7605592.
14. Mogi M, Harada M, Kondo T, Riederer P, Nagatsu T. Interleukin-2 but not basic fibroblast growth factor is elevated in parkinsonian brain. Short communication. J Neural Transm 1996, 103:1077-1081. 10.1007/BF01291792, 9013395.
15. Mogi M, Harada M, Riederer P, Narabayashi H, Fujita K, Nagatsu T. Tumor necrosis factor-alpha (TNF-alpha) increases both in the brain and in the cerebrospinal fluid from parkinsonian patients. Neurosci Lett 1994, 165:208-210. 10.1016/0304-3940(94)90746-3, 8015728.
16. Chen H, Zhang SM, Hernan MA, Schwarzschild MA, Willett WC, Colditz GA, Speizer FE, Ascherio A. Nonsteroidal anti-inflammatory drugs and the risk of Parkinson disease. Arch Neurol 2003, 60:1059-1064. 10.1001/archneur.60.8.1059, 12925360.
17. Hernan MA, Logroscino G, Garcia Rodriguez LA. Nonsteroidal anti-inflammatory drugs and the incidence of Parkinson disease. Neurology 2006, 66:1097-1099. 10.1212/01.wnl.0000204446.82823.28, 16606925.
18. Ton TG, Heckbert SR, Longstreth WT, Rossing MA, Kukull WA, Franklin GM, Swanson PD, Smith-Weller T, Checkoway H. Nonsteroidal anti-inflammatory drugs and risk of Parkinson's disease. Mov Disord 2006, 21:964-969. 10.1002/mds.20856, 16550541.
19. Akiyama H, McGeer PL. Microglial response to 6-hydroxydopamine-induced substantia nigra lesions. Brain Res 1989, 489:247-253. 10.1016/0006-8993(89)90857-3, 2501002.
20. Cicchetti F, Brownell AL, Williams K, Chen YI, Livni E, Isacson O. Neuroinflammation of the nigrostriatal pathway during progressive 6-OHDA dopamine degeneration in rats monitored by immunohistochemistry and PET imaging. Eur J Neurosci 2002, 15:991-998. 10.1046/j.1460-9568.2002.01938.x, 11918659.
21. Crotty S, Fitzgerald P, Tuohy E, Harris DM, Fisher A, Mandel A, Bolton AE, Sullivan AM, Nolan Y. Neuroprotective effects of novel phosphatidylglycerol-based phospholipids in the 6-hydroxydopamine model of Parkinson's disease. Eur J Neurosci 2008, 27:294-300. 10.1111/j.1460-9568.2007.06018.x, 18190522.
22. Depino AM, Earl C, Kaczmarczyk E, Ferrari C, Besedovsky H, del Rey A, Pitossi FJ, Oertel WH. Microglial activation with atypical proinflammatory cytokine expression in a rat model of Parkinson's disease. Eur J Neurosci 2003, 18:2731-2742. 10.1111/j.1460-9568.2003.03014.x, 14656322.
23. Koprich JB, Reske-Nielsen C, Mithal P, Isacson O. Neuroinflammation mediated by IL-1beta increases susceptibility of dopamine neurons to degeneration in an animal model of Parkinson's disease. J Neuroinflammation 2008, 5:8. 10.1186/1742-2094-5-8, 2292163, 18304357.
24. McCoy MK, Martinez TN, Ruhn KA, Szymkowski DE, Smith CG, Botterman BR, Tansey KE, Tansey MG. Blocking soluble tumor necrosis factor signaling with dominant-negative tumor necrosis factor inhibitor attenuates loss of dopaminergic neurons in models of Parkinson's disease. J Neurosci 2006, 26:9365-9375. 10.1523/JNEUROSCI.1504-06.2006, 16971520.
25. He Y, Appel S, Le W. Minocycline inhibits microglial activation and protects nigral cells after 6-hydroxydopamine injection into mouse striatum. Brain Res 2001, 909:187-193. 10.1016/S0006-8993(01)02681-6, 11478935.
26. Castano A, Herrera AJ, Cano J, Machado A. Lipopolysaccharide intranigral injection induces inflammatory reaction and damage in nigrostriatal dopaminergic system. J Neurochem 1998, 70:1584-1592.
27. Gao HM, Jiang J, Wilson B, Zhang W, Hong JS, Liu B. Microglial activation-mediated delayed and progressive degeneration of rat nigral dopaminergic neurons: relevance to Parkinson's disease. J Neurochem 2002, 81:1285-1297. 10.1046/j.1471-4159.2002.00928.x, 12068076.
28. Kohutnicka M, Lewandowska E, Kurkowska-Jastrzebska I, Czlonkowski A, Czlonkowska A. Microglial and astrocytic involvement in a murine model of Parkinson's disease induced by 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP). Immunopharmacology 1998, 39:167-180. 10.1016/S0162-3109(98)00022-8, 9754903.
29. Kurkowska-Jastrzebska I, Wronska A, Kohutnicka M, Czlonkowski A, Czlonkowska A. The inflammatory reaction following 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine intoxication in mouse. Exp Neurol 1999, 156:50-61. 10.1006/exnr.1998.6993, 10192776.
30. Sriram K, Matheson JM, Benkovic SA, Miller DB, Luster MI, O'Callaghan JP. Mice deficient in TNF receptors are protected against dopaminergic neurotoxicity: implications for Parkinson's disease. Faseb J 2002, 16:1474-1476.
31. Sriram K, Matheson JM, Benkovic SA, Miller DB, Luster MI, O'Callaghan JP. Deficiency of TNF receptors suppresses microglial activation and alters the susceptibility of brain regions to MPTP-induced neurotoxicity: role of TNF-alpha. Faseb J 2006, 20:670-682. 10.1096/fj.05-5106com, 16581975.
32. Liberatore GT, Jackson-Lewis V, Vukosavic S, Mandir AS, Vila M, McAuliffe WG, Dawson VL, Dawson TM, Przedborski S. Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nat Med 1999, 5:1403-1409. 10.1038/70978, 10581083.
33. Teismann P, Tieu K, Choi DK, Wu DC, Naini A, Hunot S, Vila M, Jackson-Lewis V, Przedborski S. Cyclooxygenase-2 is instrumental in Parkinson's disease neurodegeneration. Proc Natl Acad Sci USA 2003, 100:5473-5478. 10.1073/pnas.0837397100, 154369, 12702778.
34. Teismann P, Vila M, Choi DK, Tieu K, Wu DC, Jackson-Lewis V, Przedborski S. COX-2 and neurodegeneration in Parkinson's disease. Ann N Y Acad Sci 2003, 991:272-277.
35. Wu DC, Teismann P, Tieu K, Vila M, Jackson-Lewis V, Ischiropoulos H, Przedborski S. 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 2003, 100:6145-6150. 10.1073/pnas.0937239100, 156340, 12721370.
36. Zhang W, Wang T, Qin L, Gao HM, Wilson B, Ali SF, Zhang W, Hong JS, Liu B. Neuroprotective effect of dextromethorphan in the MPTP Parkinson's disease model: role of NADPH oxidase. Faseb J 2004, 18:589-591.
37. Babior BM. NADPH oxidase: an update. Blood 1999, 93:1464-1476.
38. Schulz R, Panas DL, Catena R, Moncada S, Olley PM, Lopaschuk GD. The role of nitric oxide in cardiac depression induced by interleukin-1 beta and tumour necrosis factor-alpha. Br J Pharmacol 1995, 114:27-34. 1510184, 7536096.
39. Feng ZH, Wang TG, Li DD, Fung P, Wilson BC, Liu B, Ali SF, Langenbach R, Hong JS. Cyclooxygenase-2-deficient mice are resistant to 1-methyl-4-phenyl1, 2, 3, 6-tetrahydropyridine-induced damage of dopaminergic neurons in the substantia nigra. Neurosci Lett 2002, 329:354-358. 10.1016/S0304-3940(02)00704-8, 12183047.
40. Vijitruth R, Liu M, Choi DY, Nguyen XV, Hunter RL, Bing G. Cyclooxygenase-2 mediates microglial activation and secondary dopaminergic cell death in the mouse MPTP model of Parkinson's disease. J Neuroinflammation 2006, 3:6. 10.1186/1742-2094-3-6, 1440849, 16566823.
41. Needleman P, Isakson PC. The discovery and function of COX-2. J Rheumatol Suppl 1997, 49:6-8.
42. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006, 124:783-801. 10.1016/j.cell.2006.02.015, 16497588.
43. Hoffmann O, Braun JS, Becker D, Halle A, Freyer D, Dagand E, Lehnardt S, Weber JR. TLR2 mediates neuroinflammation and neuronal damage. J Immunol 2007, 178:6476-6481.
44. Kawai T, Akira S. Toll-like receptor and RIG-I-like receptor signaling. Ann N Y Acad Sci 2008, 1143:1-20. 10.1196/annals.1443.020, 19076341.
45. Lehnardt S, Lehmann S, Kaul D, Tschimmel K, Hoffmann O, Cho S, Krueger C, Nitsch R, Meisel A, Weber JR. Toll-like receptor 2 mediates CNS injury in focal cerebral ischemia. J Neuroimmunol 2007, 190:28-33. 10.1016/j.jneuroim.2007.07.023, 17854911.
46. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, Mignot G, Maiuri MC, Ullrich E, Saulnier P, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007, 13:1050-1059. 10.1038/nm1622, 17704786.
47. Vogl T, Tenbrock K, Ludwig S, Leukert N, Ehrhardt C, van Zoelen MA, Nacken W, Foell D, van der Poll T, Sorg C, Roth J. Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat Med 2007, 13:1042-1049. 10.1038/nm1638, 17767165.
48. Janssens S, Beyaert R. A universal role for MyD88 in TLR/IL-1R-mediated signaling. Trends Biochem Sci 2002, 27:474-482. 10.1016/S0968-0004(02)02145-X, 12217523.
49. Dunne A, O'Neill LA. The interleukin-1 receptor/Toll-like receptor superfamily: signal transduction during inflammation and host defense. Sci STKE 2003, 2003:re3.
50. Kang J, Rivest S. MyD88-deficient bone marrow cells accelerate onset and reduce survival in a mouse model of amyotrophic lateral sclerosis. J Cell Biol 2007, 179:1219-1230. 10.1083/jcb.200705046, 2140021, 18086918.
51. Hao W, Liu Y, Liu S, Walter S, Grimm MO, Kiliaan AJ, Penke B, Hartmann T, Rube CE, Menger MD, Fassbender K. Myeloid differentiation factor 88-deficient bone marrow cells improve Alzheimer's disease-related symptoms and pathology. Brain 2011, 134:278-292. 10.1093/brain/awq325, 21115468.
52. Panaro MA, Lofrumento DD, Saponaro C, De Nuccio F, Cianciulli A, Mitolo V, Nicolardi G. Expression of TLR4 and CD14 in the central nervous system (CNS) in a MPTP mouse model of Parkinson's-like disease. Immunopharmacol Immunotoxicol 2008, 30:729-740. 10.1080/08923970802278557, 18686098.
53. Ros-Bernal F, Hunot S, Herrero MT, Parnadeau S, Corvol JC, Lu L, Alvarez-Fischer D, Carrillo-de Sauvage MA, Saurini F, Coussieu C, et al. Microglial glucocorticoid receptors play a pivotal role in regulating dopaminergic neurodegeneration in parkinsonism. Proc Natl Acad Sci USA 2011, 108:6632-6637. 10.1073/pnas.1017820108, 21467220.
54. Stefanova N, Fellner L, Reindl M, Masliah E, Poewe W, Wenning GK. Toll-Like Receptor 4 Promotes alpha-Synuclein Clearance and Survival of Nigral Dopaminergic Neurons. Am J Pathol 2011, 179:954-963. 10.1016/j.ajpath.2011.04.013, 21801874.
55. Cote M, Drouin-Ouellet J, Cicchetti F, Soulet D. The critical role of the MyD88-dependent pathway in non-CNS MPTP-mediated toxicity. Brain Behav Immun 2011, 6:1143-1152.
56. Jackson-Lewis V, Przedborski S. Protocol for the MPTP mouse model of Parkinson's disease. Nat Protoc 2007, 2:141-151.
57. Przedborski S, Jackson-Lewis V, Djaldetti R, Liberatore G, Vila M, Vukosavic S, Almer G. The parkinsonian toxin MPTP: action and mechanism. Restor Neurol Neurosci 2000, 16:135-142.
58. Przedborski S, Jackson-Lewis V, Naini AB, Jakowec M, Petzinger G, Miller R, Akram M. The parkinsonian toxin 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP): a technical review of its utility and safety. J Neurochem 2001, 76:1265-1274. 10.1046/j.1471-4159.2001.00183.x, 11238711.
59. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, Sakagami M, Nakanishi K, Akira S. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 1998, 9:143-150. 10.1016/S1074-7613(00)80596-8, 9697844.
60. Kawai T, Adachi O, Ogawa T, Takeda K, Akira S. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 1999, 11:115-122. 10.1016/S1074-7613(00)80086-2, 10435584.
61. Gibrat C, Saint-Pierre M, Bousquet M, Levesque D, Rouillard C, Cicchetti F. Differences between subacute and chronic MPTP mice models: investigation of dopaminergic neuronal degeneration and alpha-synuclein inclusions. J Neurochem 2009, 109:1469-1482. 10.1111/j.1471-4159.2009.06072.x, 19457163.
62. Lalancette-Hebert M, Phaneuf D, Soucy G, Weng YC, Kriz J. Live imaging of Toll-like receptor 2 response in cerebral ischaemia reveals a role of olfactory bulb microglia as modulators of inflammation. Brain 2009, 132:940-954.
63. Bousquet M, Gue K, Emond V, Julien P, Kang JX, Cicchetti F, Calon F. Transgenic conversion of omega-6 into omega-3 fatty acids in a mouse model of Parkinson's disease. J Lipid Res 2011, 52:263-271. 10.1194/jlr.M011692, 21115966.
64. Franklin KBJ, Paxinos G. The Mouse Brain in Stereotaxic Coordinates, Compact 2008, Academic Press, 3.
65. Glaser JR, Glaser EM. Stereology, morphometry, and mapping: the whole is greater than the sum of its parts. J Chem Neuroanat 2000, 20:115-126. 10.1016/S0891-0618(00)00073-9, 11074348.
66. Calon F, Lavertu N, Lemieux AM, Morissette M, Goulet M, Grondin R, Blanchet PJ, Bedard PJ, Di Paolo T. Effect of MPTP-induced denervation on basal ganglia GABA(B) receptors: correlation with dopamine concentrations and dopamine transporter. Synapse 2001, 40:225-234. 10.1002/syn.1045, 11304760.
67. Breidert T, Callebert J, Heneka MT, Landreth G, Launay JM, Hirsch EC. Protective action of the peroxisome proliferator-activated receptor-gamma agonist pioglitazone in a mouse model of Parkinson's disease. J Neurochem 2002, 82:615-624. 10.1046/j.1471-4159.2002.00990.x, 12153485.
68. Choi DK, Pennathur S, Perier C, Tieu K, Teismann P, Wu DC, Jackson-Lewis V, Vila M, Vonsattel JP, Heinecke JW, Przedborski S. Ablation of the inflammatory enzyme myeloperoxidase mitigates features of Parkinson's disease in mice. J Neurosci 2005, 25:6594-6600. 10.1523/JNEUROSCI.0970-05.2005, 16014720.
69. Smith PF. Inflammation in Parkinson's disease: an update. Curr Opin Investig Drugs 2008, 9:478-484.
70. Brochard V, Combadiere B, Prigent A, Laouar Y, Perrin A, Beray-Berthat V, Bonduelle O, Alvarez-Fischer D, Callebert J, Launay JM, et al. Infiltration of CD4+ lymphocytes into the brain contributes to neurodegeneration in a mouse model of Parkinson disease. J Clin Invest 2009, 119:182-192. 2613467, 19104149.
71. Liu B, Wang K, Gao HM, Mandavilli B, Wang JY, Hong JS. Molecular consequences of activated microglia in the brain: overactivation induces apoptosis. J Neurochem 2001, 77:182-189. 10.1046/j.1471-4159.2001.t01-1-00216.x, 11279274.
72. Peterson JW, Bo L, Mork S, Chang A, Ransohoff RM, Trapp BD. VCAM-1-positive microglia target oligodendrocytes at the border of multiple sclerosis lesions. J Neuropathol Exp Neurol 2002, 61:539-546.
73. Olson JK, Miller SD. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 2004, 173:3916-3924.
74. Furuya T, Hayakawa H, Yamada M, Yoshimi K, Hisahara S, Miura M, Mizuno Y, Mochizuki H. Caspase-11 mediates inflammatory dopaminergic cell death in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine mouse model of Parkinson's disease. J Neurosci 2004, 24:1865-1872. 10.1523/JNEUROSCI.3309-03.2004, 14985426.
75. Mochizuki H, Hayakawa H, Migita M, Shibata M, Tanaka R, Suzuki A, Shimo-Nakanishi Y, Urabe T, Yamada M, Tamayose K, et al. An AAV-derived Apaf-1 dominant negative inhibitor prevents MPTP toxicity as antiapoptotic gene therapy for Parkinson's disease. Proc Natl Acad Sci USA 2001, 98:10918-10923. 10.1073/pnas.191107398, 58574, 11535810.
76. Tatton NA, Kish SJ. In situ detection of apoptotic nuclei in the substantia nigra compacta of 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-treated mice using terminal deoxynucleotidyl transferase labelling and acridine orange staining. Neuroscience 1997, 77:1037-1048. 10.1016/S0306-4522(96)00545-3, 9130785.
77. Kim NG, Lee H, Son E, Kwon OY, Park JY, Park JH, Cho GJ, Choi WS, Suk K. Hypoxic induction of caspase-11/caspase-1/interleukin-1beta in brain microglia. Brain Res Mol Brain Res 2003, 114:107-114.
78. Miller JA, Trout BR, Sullivan KA, Bialecki RA, Roberts RA, Tjalkens RB. Low-dose 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine causes inflammatory activation of astrocytes in nuclear factor-kappaB reporter mice prior to loss of dopaminergic neurons. J Neurosci Res 2011,
79. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004, 4:499-511. 10.1038/nri1391, 15229469.
80. Caso JR, Pradillo JM, Hurtado O, Leza JC, Moro MA, Lizasoain I. Toll-like receptor 4 is involved in subacute stress-induced neuroinflammation and in the worsening of experimental stroke. Stroke 2008, 39:1314-1320. 10.1161/STROKEAHA.107.498212, 18309167.