The role of neuroinflammation on the pathogenesis of Parkinson's disease |
Chung, Young-Cheul
(Department of Biochemistry & Molecular Biology, Neurodegeneration Control Research Center, School of Medicine Kyung Hee University)
Ko, Hyuk-Wan (Department of Biochemistry & Molecular Biology, Neurodegeneration Control Research Center, School of Medicine Kyung Hee University) Bok, Eu-Gene (Department of Biochemistry & Molecular Biology, Neurodegeneration Control Research Center, School of Medicine Kyung Hee University) Park, Eun-Soo (Department of Biochemistry & Molecular Biology, Neurodegeneration Control Research Center, School of Medicine Kyung Hee University) Huh, Sue-Hee (Department of Biochemistry & Molecular Biology, Neurodegeneration Control Research Center, School of Medicine Kyung Hee University) Nam, Jin-Han (Department of Biochemistry & Molecular Biology, Neurodegeneration Control Research Center, School of Medicine Kyung Hee University) Jin, Byung-Kwan (Department of Biochemistry & Molecular Biology, Neurodegeneration Control Research Center, School of Medicine Kyung Hee University) |
1 | Hirsch, E. C. and Hunot, S. (2009) Neuroinflammation in Parkinson's disease: a target for neuroprotection? Lancet. Neurol. 8, 382-397 DOI ScienceOn |
2 | Saavedra, A., Baltazar, G., Santos, P., Carvalho, C. M. and Duarte, E. P. (2006) Selective injury to dopaminergic neurons up-regulates GDNF in substantia nigra postnatal cell cultures: role of neuron-glia crosstalk. Neurobiol. Dis. 23, 533-542 DOI ScienceOn |
3 | Jakel, R. J., Townsend, J. A., Kraft, A. D. and Johnson, J. A. (2007) Nrf2-mediated protection against 6-hydroxydopamine. Brain Res. 1144, 192-201 DOI PUBMED ScienceOn |
4 | Kurkowska-Jastrzebska, I., Litwin, T., Joniec, I., Ciesielska, A. Przybylkowski, A., Czlonkowski, A. and Czlonkowska. A. (2004) Dexamethasone protects against dopaminergic neurons damage in a mouse model of Parkinson's disease. Int. Immunopharmacol. 4, 1307-1318 DOI ScienceOn |
5 | Dauer, W. and Przedborski, S. (2003) Parkinson's disease:mechanisms and models. Neuron 39, 889-909 DOI ScienceOn |
6 | Greenfield, J. G. and Bosanquet, F. D. (1953) The brainstem lesions in Parkinsonism. J. Neurol. Neurosurg. Psychiatry. 16, 213-226 DOI PUBMED |
7 | Block, M. L. and Hong, J. S. (2005) Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol. 76, 77-98 DOI ScienceOn |
8 | Morris, L., Graham, C. F. and Gordon, S. (1991) Macrophages in haemopoietic and other tissues of the developing mouse detected by the monoclonal antibody F4/80. Development 112, 517-526 PUBMED |
9 | Giulian, D., Johnson, B., Krebs, J. F., George, J. K. and Tapscott, M. (1991) Microglial mitogens are produced in the developing and injured mammalian brain. J. Cell. Biol. 112, 323-333 DOI ScienceOn |
10 | Kreutzberg, G. W. (1996) Microglia: a sensor for pathological events in the CNS. Trends. Neurosci. 19, 312-318 DOI PUBMED ScienceOn |
11 | Graeber, M. B., Streit, W. J. and Kreutzberg, G. W. (1988) Axotomy of the rat facial nerve leads to increased CR3 complement receptor expression by activated microglial cells. J. Neurosci. Res. 21, 18-24 DOI ScienceOn |
12 | Nutt, J. G. and Wooten, G. F. (2005) Clinical practice. Diagnosis and initial management of Parkinson's disease. N. Engl. J. Med. 353, 1021-1027 DOI PUBMED ScienceOn |
13 | Mogi, M., Harada, M., Narabayashi, H., Inagaki, H., Minami, M. and Nagatsu, T. (1996) Interleukin (IL)-1 beta, IL-2, IL-4, IL-6 and transforming growth factor-alpha levels are elevated in ventricular cerebrospinal fluid in juvenile parkinsonism and Parkinson's disease. Neurosci. Lett. 211, 13-16 DOI ScienceOn |
14 | Godoy, M. C., Tarelli, R., Ferrari, C. C., Sarchi, M. I. and Pitossi, F. J. (2008) Central and systemic IL-1 exacerbates neurodegeneration and motor symptoms in a model of Parkinson's disease. Brain 131, 1880-1894 DOI ScienceOn |
15 | Danbolt, N. C. (2001) Glutamate uptake. Prog. Neurobiol. 65, 1-105 DOI PUBMED ScienceOn |
16 | Sandhu, J. K., Gardaneh, M., Iwasiow, R., Lanthier, P., Gangaraju, S., Ribecco-Lutkiewicz, M., Tremblay, R., Kiuchi, K. and Sikorska, M. (2009) Astrocyte-secreted GDNF and glutathione antioxidant system protect neurons against 6OHDA cytotoxicity. Neurobiol. Dis. 33, 405-414 DOI ScienceOn |
17 | Voutilainen, M. H., Back, S., Porsti, E., Toppinen, L., Lindgren, L., Lindholm, P., Peranen, J., Saarma, M. and Tuominen, R. K. (2009) Mesencephalic astrocyte-derived neurotrophic factor is neurorestorative in rat model of Parkinson's disease. J. Neurosci. 29, 9651-9659 DOI ScienceOn |
18 | Ghosh, A., Roy, A., Matras, J., Brahmachari, S., Gendelman, H. E. and Pahan, K. (2009) Simvastatin inhibits the activation of p21ras and prevents the loss of dopaminergic neurons in a mouse model of Parkinson's disease. J. Neurosci. 29, 13543-13556 DOI ScienceOn |
19 | Choi, D. K., Pennathur, S., Perier, C., Tieu, K., Teismann, P., Wu, D. C., Jackson-Lewis, V., Vila, M., Vonsattel, J. P., Heinecke, J. W. and Przedborski. S. (2005) Ablation of the inflammatory enzyme myeloperoxidase mitigates features of Parkinson's disease in mice. J. Neurosci. 25, 6594-6600 DOI ScienceOn |
20 | Kurkowska-Jastrzebska, I., Babiuch, M., Joniec, I., Przybylkowski, A., Czlonkowski, A. and Czlonkowska, A. (2002) Indomethacin protects against neurodegeneration caused by MPTP intoxication in mice. Int Immunopharmacol 2, 1213-1218 DOI ScienceOn |
21 | Faucheux, B. A., Bonnet, A. M., Agid, Y. and Hirsch, E. C. (1999) Blood vessels change in the mesencephalon of patients with Parkinson's disease. Lancet 353, 981-982 PUBMED |
22 | Tieu, K., Ischiropoulos, H. and Przedborski. S. (2003) Nitric oxide and reactive oxygen species in Parkinson's disease. IUBMB Life 55, 329-335 DOI ScienceOn |
23 | McGeer, P. L. and McGeer, E. G. (2008) Glial reactions in Parkinson's disease. Mov. Disord. 23, 474-483 DOI ScienceOn |
24 | Block, M. L. and Hong, J. S. (2007) Chronic microglial activation and progressive dopaminergic neurotoxicity. Biochem. Soc. Trans. 35, 1127-1132 DOI ScienceOn |
25 | Li, G., Cui, G., Tzeng, N. S., Wei, S. J., Wang, T., Block, M. L. and Hong, J. S. (2005) Femtomolar concentrations of dextromethorphan protect mesencephalic dopaminergic neurons from inflammatory damage. FASEB J. 19, 489-496 DOI ScienceOn |
26 | Qin, L., Block, M. L., Liu, Y., Bienstock, R. J., Pei, Z., Zhang, W., Wu, X., Wilson, B., Burka, T. and Hong, J. S. (2005) Microglial NADPH oxidase is a novel target for femtomolar neuroprotection against oxidative stress. FASEB J. 19, 550-557 DOI ScienceOn |
27 | Rodriguez-Pallares, J., Parga, J. A., Munoz, A., Rey, P., Guerra, M. J. and Labandeira-Garcia, J. L. (2007) Mechanism of 6-hydroxydopamine neurotoxicity: the role of NADPH oxidase and microglial activation in 6-hydroxydopamineinduced degeneration of dopaminergic neurons. J. Neurochem. 103, 145-156 PUBMED |
28 | Knott, C., Stern, G. and Wilkin, G. P. (2000) Inflammatory regulators in Parkinson's disease: iNOS, lipocortin-1, and cyclooxygenases-1 and -2. Mol. Cell. Neurosci. 16, 724-739 DOI ScienceOn |
29 | Klevenyi, P., Andreassen, O., J. Ferrante, R. J., Schleicher, R., Jr., Friedlander, R. M. and Beal, M. F. (1999) Transgenic mice expressing a dominant negative mutant interleukin-1beta converting enzyme show resistance to MPTP neurotoxicity. Neuroreport 10, 635-638 DOI ScienceOn |
30 | Chesselet, M. F. (2008) In vivo alpha-synuclein overexpression in rodents: a useful model of Parkinson's disease? Exp. Neurol. 209, 22-27 DOI PUBMED ScienceOn |
31 | Tower, D. B. and Young, O. M. (1973) The activities of butyrylcholinesterase and carbonic anhydrase, the rate of anaerobic glycolysis, and the question of a constant density of glial cells in cerebral cortices of various mammalian species from mouse to whale. J. Neurochem. 20, 269-278 DOI PUBMED |
32 | Wilhelmsson, U., Bushong, E. A., Price, D. L., Smarr, B. L., Phung, V., Terada, M., Ellisman, M. H. and Pekny, M. (2006) Redefining the concept of reactive astrocytes as cells that remain within their unique domains upon reaction to injury. Proc. Natl. Acad. Sci. U.S.A. 103, 17513-17518 DOI ScienceOn |
33 | Arimoto, T. and Bing, G. (2003) Up-regulation of inducible nitric oxide synthase in the substantia nigra by lipopolysaccharide causes microglial activation and neurodegeneration. Neurobiol. Dis. 12, 35-45 DOI ScienceOn |
34 | Braak, H., Del Tredici, K., Rub, U., de Vos, R. A., Jansen Steur, E. N. and Braak, E. (2003) Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 24, 197-211 DOI ScienceOn |
35 | Savitt, J. M., Dawson, V. L. and Dawson, T. M. (2006) Diagnosis and treatment of Parkinson disease: molecules to medicine. J. Clin. Invest. 116, 1744-1754 DOI ScienceOn |
36 | Stack, E. C., Ferro, J. L., Kim, J., Del Signore, S. J., Goodrich, S., Matson, S., Hunt, B. B., Cormier, K., Smith, K., Matson, W. R., Ryu, H. and Ferrante, R. J. (2008) Therapeutic attenuation of mitochondrial dysfunction and oxidative stress in neurotoxin models of Parkinson's disease. Biochim. Biophys. Acta. 1782, 151-162 DOI PUBMED ScienceOn |
37 | Woodroofe, M. N., Bellamy, A. S., Feldmann, M., Davison, A. N. and Cuzner, M. L. (1986) Immunocytochemical characterisation of the immune reaction in the central nervous system in multiple sclerosis. Possible role for microglia in lesion growth. J. Neurol. Sci. 74, 135-152 DOI PUBMED ScienceOn |
38 | Orr, C. F., Rowe, D. B. and Halliday, G. M. (2002) An inflammatory review of Parkinson's disease. Prog. Neurobiol. 68, 325-340 DOI ScienceOn |
39 | Wu, D. C., Jackson-Lewis, V., Vila, M., Tieu, K., Teismann, P., Vadseth, C., Choi, D. K., Ischiropoulos, H. and 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, 1763-1771 PUBMED |
40 | Fornai, F., Schluter, O. M., Lenzi, P., Gesi, M., Ruffoli, R., Ferrucci, M., Lazzeri, G., Busceti, C. L., Pontarelli, F., Battaglia, G., Pellegrini, A., Nicoletti, F., Ruggieri, S., Paparelli, A. and Sudhof, T. C. (2005) Parkinson-like syndrome induced by continuous MPTP infusion: convergent roles of the ubiquitin-proteasome system and alphasynuclein. Proc. Natl. Acad. Sci. U.S.A. 102, 3413-3418 DOI PUBMED ScienceOn |
41 | Lawson, L. J., Perry, V. H., Dri, P. and Gordon, S. (1990) Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39, 151-170 DOI ScienceOn |
42 | Gordon, G. R., Choi, H. B., Rungta, R. L., Ellis-Davies, G. C. and MacVicar, B. A. (2008) Brain metabolism dictates the polarity of astrocyte control over arterioles. Nature 456, 745-749 DOI ScienceOn |
43 | Anastasia, A., Torre, L., de Erausquin, G. A. and Masco, D. H. (2009) Enriched environment protects the nigrostriatal dopaminergic system and induces astroglial reaction in the 6-OHDA rat model of Parkinson's disease. J. Neurochem. 109, 755-765 DOI ScienceOn |
44 | Kortekaas, R., Leenders, K. L., van Oostrom, J. C., Vaalburg, W., Bart, J., Willemsen, A. T. and Hendrikse, N. H. (2005) Blood-brain barrier dysfunction in parkinsonian midbrain in vivo. Ann. Neurol. 57, 176-179 DOI ScienceOn |
45 | Ferger, B., Leng, A., Mura, A., Hengerer, B. and Feldon, J. (2004) Genetic ablation of tumor necrosis factor-alpha (TNF-alpha) and pharmacological inhibition of TNF-synthesis attenuates MPTP toxicity in mouse striatum. J. Neurochem. 89, 822-833 DOI ScienceOn |
46 | Sriram, K., Matheson, J. M., Benkovic, S. A., Miller, D. B., Luster, M. I. and O'Callaghan, J. P. (2002) Mice deficient in TNF receptors are protected against dopaminergic neurotoxicity: implications for Parkinson's disease. FASEB J. 16, 1474-1476 DOI PUBMED |
47 | Miller, R. L., James-Kracke, M., Sun, G. Y. and Sun, A. Y. (2009) Oxidative and inflammatory pathways in Parkinson's disease. Neurochem. Res. 34, 55-65 DOI ScienceOn |
48 | Kim, S. R., Chung, E. S., Bok, E., Baik, H. H., Chung, Y. C., Won, S. Y., Joe, E., Kim, T. H., Kim, S. S., Jin, M. Y., Choi, S. H. and Jin, B. K. (2009) Prothrombin kringle-2 induces death of mesencephalic dopaminergic neurons in vivo and in vitro via microglial activation. J. Neurosci. Res. (Epub ahead of print) |
49 | Choi, S. H., Lee, D. Y., Chung, E. S., Hong, Y. B., Kim, S. U. and Jin, B. K. (2005) Inhibition of thrombin-induced microglial activation and NADPH oxidase by minocycline protects dopaminergic neurons in the substantia nigra in vivo. J. Neurochem. 95, 1755-1765 DOI ScienceOn |
50 | Meredith, G. E., Sonsalla, P. K. and Chesselet, M. F. (2008) Animal models of Parkinson's disease progression. Acta. Neuropathol. 115, 385-398 DOI ScienceOn |
51 | Chen, X., Lan, X., Roche, I., Liu, R. and Geiger, J. D. (2008) Caffeine protects against MPTP-induced bloodbrain barrier dysfunction in mouse striatum. J. Neurochem. 107, 1147-1157 PUBMED |
52 | Mogi, M., Harada, M., Riederer, P., Narabayashi, H., Fujita, K. and Nagatsu, T. (1994) Tumor necrosis factor-alpha (TNF-alpha) increases both in the brain and in the cerebrospinal fluid from parkinsonian patients. Neurosci. Lett. 165, 208-210 DOI PUBMED ScienceOn |
53 | Morale, M. C., Serra, P. A., L'Episcopo, F., Tirolo, C., Caniglia, S., Testa, N., Gennuso, F., Giaquinta, G., Rocchitta, G., Desole, M. S., Miele, E. and Marchetti. B. (2006) Estrogen, neuroinflammation and neuroprotection in Parkinson's disease: glia dictates resistance versus vulnerability to neurodegeneration. Neuroscience 138, 869-878 DOI ScienceOn |
54 | Persidsky, Y., Ramirez, S. H., Haorah, J. and Kanmogne, G. D. (2006) Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J. Neuroimmune. Pharmacol. 1, 223-236 DOI ScienceOn |
55 | Zlokovic, B. V. (2008) The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57, 178-201 DOI PUBMED ScienceOn |
56 | Kim, S. U. and de Vellis, J. (2005) Microglia in health and disease. J. Neurosci. Res. 81, 302-313 DOI ScienceOn |
57 | Hirsch, E. C., Hunot, S., Damier, P. and Faucheux, B. (1998) Glial cells and inflammation in Parkinson's disease: a role in neurodegeneration? Ann. Neurol. 44, S115-120 DOI PUBMED ScienceOn |
58 | Liberatore, G. T., Jackson-Lewis, V., Vukosavic, S., Mandir, A. S., Vila, M., McAuliffe, W. G., Dawson, V. L., Dawson, T. M. and Przedborski, S. (1999) Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nat. Med. 5, 1403-1409 DOI ScienceOn |
59 | Yan, E., Castillo-Melendez, M., Nicholls, T., Hirst, J. and Walker, D. (2004) Cerebrovascular responses in the fetal sheep brain to low-dose endotoxin. Pediatr. Res. 55, 855-863 DOI ScienceOn |
60 | Wu, D. C., Teismann, P., Tieu, K., Vila, M., Jackson-Lewis, V., Ischiropoulos, H. and 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. U.S.A. 100, 6145-6150 DOI ScienceOn |
61 | Siebert, A., Desai, V., Chandrasekaran, K., Fiskum, G. and Jafri, M. S. (2009) Nrf2 activators provide neuroprotection against 6-hydroxydopamine toxicity in rat organotypic nigrostriatal cocultures. J. Neurosci. Res. 87, 1659-1669 DOI ScienceOn |
62 | Rite, I., Machado, A., Cano, J. and Venero, J. L. (2007) Bloodbrain barrier disruption induces in vivo degeneration of nigral dopaminergic neurons. J. Neurochem. 101, 1567-1582 DOI ScienceOn |
63 | Ji, K. A., Yang, M. S., Jeong, H. K., Min, K. J., Kang, S. H., Jou, I. and Joe, E. H. (2007) Resident microglia die and infiltrated neutrophils and monocytes become major inflammatory cells in lipopolysaccharide-injected brain. Glia 55, 1577-1588 DOI ScienceOn |
64 | Gao, H. M., Liu, B., Zhang, W. and Hong, J. S. (2003) Critical role of microglial NADPH oxidase-derived free radicals in the in vitro MPTP model of Parkinson's disease. FASEB J. 17, 1954-1956 DOI PUBMED |
65 | Brochard, V., Combadiere, B., Prigent, A., Laouar, Y., Perrin, A., Beray-Berthat, V., Bonduelle, O., Alvarez-Fischer, D., Callebert, J., Launay, J. M., Duyckaerts, C., Flavell, R. A., Hirsch, E. C. and Hunot, S. (2009) Infiltration of CD4+ lymphocytes into the brain contributes to neurodegeneration in a mouse model of Parkinson disease. J. Clin. Invest. 119, 182-192 PUBMED |
66 | Stence, N., Waite, M. and Dailey, M. E. (2001) Dynamics of microglial activation: a confocal time-lapse analysis in hippocampal slices. Glia 33, 256-266 DOI ScienceOn |
67 | Knott, C., Stern, G., Kingsbury, A., Welcher, A. A. and Wilkin, G. P. (2002) Elevated glial brain-derived neurotrophic factor in Parkinson's diseased nigra. Parkinsonism. Relat. Disord. 8, 329-341 DOI ScienceOn |
68 | Min, K. J., Yang, M. S., Kim, S. U., Jou, I. and Joe, E. H. (2006) Astrocytes induce hemeoxygenase-1 expression in microglia: a feasible mechanism for preventing excessive brain inflammation. J. Neurosci. 26, 1880-1887 DOI ScienceOn |
69 | Choi, S. H., Joe, E. H., Kim, S. U. and Jin, B. K. (2003) Thrombin-induced microglial activation produces degeneration of nigral dopaminergic neurons in vivo. J. Neurosci. 23, 5877-5886 PUBMED |
70 | Yasuda, T., Fukuda-Tani, M., Nihira, T., Wada, K., Hattori, N., Mizuno, Y. and Mochizuki, H. (2007) Correlation between levels of pigment epithelium-derived factor and vascular endothelial growth factor in the striatum of patients with Parkinson's disease. Exp. Neurol. 206, 308-317 DOI ScienceOn |
71 | Le, W. D., Rowe, D. B., Jankovic, J., Xie, W. and Appel, S. H. (1999) Effects of cerebrospinal fluid from patients with Parkinson disease on dopaminergic cells. Arch. Neurol. 56, 194-200 DOI ScienceOn |
72 | Popescu, B. O., Toescu, E. C., Popescu, L. M., Bajenaru, O., Muresanu, D. F., Schultzberg, M. and Bogdanovic, N. (2009) Blood-brain barrier alterations in ageing and dementia. J. Neurol. Sci. 283, 99-106 DOI PUBMED ScienceOn |
73 | Chen, P. S., Peng, G. S., Li, G., Yang, S., Wu, X., Wang, C. C., Wilson, B., Lu, R. B., Gean, P. W., Chuang, D. M. and Hong, J. S. (2006) Valproate protects dopaminergic neurons in midbrain neuron/glia cultures by stimulating the release of neurotrophic factors from astrocytes. Mol. Psychiatry. 11, 1116-1125 DOI ScienceOn |
74 | McGeer, P. L., Itagaki, S., Boyes, B. E. and McGeer, E. G. (1988) Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 38, 1285-1291 DOI PUBMED |
75 | Hunot, S., Boissiere, F., Faucheux, B., Brugg, B., Mouatt-Prigent, A., Agid, Y. and Hirsch. E. C., (1996) Nitric oxide synthase and neuronal vulnerability in Parkinson's disease. Neuroscience 72, 355-363 DOI ScienceOn |
76 | Mulligan, S. J. and MacVicar, B. A. (2004) Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431, 195-199 DOI ScienceOn |
77 | Siegel, G. J. and Chauhan, N. B. (2000) Neurotrophic factors in Alzheimer's and Parkinson's disease brain. Brain. Res. Brain. Res. Rev. 33, 199-227 DOI PUBMED ScienceOn |
78 | Nimmerjahn, A., Kirchhoff, F. and Helmchen, F. (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308, 1314-1318 DOI PUBMED ScienceOn |
79 | Whitton, P. S. (2007) Inflammation as a causative factor in the aetiology of Parkinson's disease. Br. J. Pharmacol. 150, 963-976 DOI PUBMED ScienceOn |