An inflammatory review of Parkinson's disease
Abstract
The symptoms of Parkinson's disease (PD) were first described nearly two centuries ago and its characteristic pathology identified nearly a century ago, yet its pathogenesis is still poorly understood. Parkinson's disease is the most prevalent neurodegenerative movement disorder and research into its pathogenesis recently accelerated following the identification of a number of causal genetic mutations. The mutant gene products all cause dysfunction of the ubiquitin-proteosome system, identifying protein modification and degradation as critical for pathogenesis. Modified non-degraded intracellular proteins accumulate in certain neuronal populations in all forms of the disease. However, neuronal degeneration is more highly selective and associates with substantial activation of microglia, the inflammatory cells of the brain. We review the current change in thinking regarding the role of microglia in the brain in the context of Parkinson's disease and animal models of the disease. Comparison of the cellular tissue changes across a number of animal models using diverse stimuli to mimic Parkinson's disease reveals a consistent pattern implicating microglia as the effector for the selective degeneration of dopaminergic neurons. While previous reviews have concentrated on the intracellular neuronal changes in Parkinson's disease, we highlight the cell to cell interactions and immune regulation critical for neuronal homeostasis and survival in Parkinson's disease.
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PD is a chronic and progressive movement disorder.
“while the PD is a chronic and progressive movement disorder (Orr et al., 2002).”
From The role of microglia in retinal neurodegeneration: Alzheimer’s disease, parkinson, and glaucoma. (2017) · cites this paper as Orr et al., 2002
Lewy bodies are constituted by α-syn, parkin, phosphorylated neurofilament and components of the protheosomic-ubiquitin pathway.
“These aggregates (deposited in somas and axons) are constituted by α-syn, parkin, phosphorylated neurofilament and components of the protheosomic-ubiquitin pathway (Orr et al., 2002).”
From The role of microglia in retinal neurodegeneration: Alzheimer’s disease, parkinson, and glaucoma. (2017) · cites this paper as Orr et al., 2002
Gliosis in PD is atypical: astrogliosis is largely absent while microglia is highly activated.
“Gliosis in the PD is an atypical activation where astrogliosis is largely absent while the microglia is highly activated by the disease.”
From The role of microglia in retinal neurodegeneration: Alzheimer’s disease, parkinson, and glaucoma. (2017) · cites this paper as Orr et al., 2002
Low astroglial response in PD may be caused by degeneration due to increased α-syn in astrocytes.
“The low astroglial response may be caused by degeneration due to an increase of α-syn in the astrocyte (Stefanova et al., 2001; Orr et al., 2002; Sofroniew and Vinters, 2010).”
From The role of microglia in retinal neurodegeneration: Alzheimer’s disease, parkinson, and glaucoma. (2017) · cites this paper as Orr et al., 2002
Cites
Dahlstroem, A., & Fuxé, K. (1964) · PubMed · Cited by 5,143 · see citing works
Chronic Parkinsonism in Humans Due to a Product of Meperidine-Analog Synthesis
Langston, J. W., Ballard, P., Tetrud, J. W., & Irwin, I. (1983) · Science · doi:10.1126/science.6823561 · Cited by 4,914 · see citing works
Microglia: a sensor for pathological events in the CNS
Kreutzberg, G. W. (1996) · Trends in Neurosciences · doi:10.1016/0166-2236(96)10049-7 · Cited by 4,396 · see citing works
Chronic systemic pesticide exposure reproduces features of Parkinson's disease
Betarbet, R., Sherer, T., Mackenzie, G., Garcia-Osuna, M., Panov, A., & Greenamyre, J. (2000) · Nature Neuroscience · doi:10.1038/81834 · Cited by 3,797 · see citing works
AGEING AND PARKINSON'S DISEASE: SUBSTANTIA NIGRA REGIONAL SELECTIVITY
FEARNLEY, J. M., & LEES, A. J. (1991) · Brain · doi:10.1093/brain/114.5.2283 · Cited by 3,529 · see citing works
McGeer, P. L., Itagaki, S., Boyes, B. E., & McGeer, E. G. (1988) · Neurology · doi:10.1212/wnl.38.8.1285 · Cited by 2,990 · see citing works
Diagnostic Criteria for Parkinson Disease
Gelb, D. J., Oliver, E., & Gilman, S. (1999) · Archives of Neurology · doi:10.1001/archneur.56.1.33 · Cited by 2,822 · see citing works
Wiklund, R. A., & Rosenbaum, S. H. (1997) · New England Journal of Medicine · doi:10.1056/nejm199710163371606 · Cited by 2,159 · see citing works
Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain
Lawson, L. J., Perry, V. H., Dri, P., & Gordon, S. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90229-w · Cited by 2,045 · see citing works
Lang, A. E., & Lozano, A. M. (1998) · New England Journal of Medicine · doi:10.1056/nejm199810083391506 · Cited by 2,041 · see citing works
The substantia nigra of the human brain
Damier, P., Hirsch, É. C., Agid, Y., & Graybiel, A. M. (1999) · Brain · doi:10.1093/brain/122.8.1437 · Cited by 1,772 · see citing works
Aloisi, F. (2001) · Glia · doi:10.1002/glia.1106 · Cited by 1,281 · see citing works
Wu, D. C., Jackson-Lewis, V., Vila, M., Tieu, K., Teismann, P., Vadseth, C., Choi, D.-K., Ischiropoulos, H., & Przedborski, S. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-05-01763.2002 · Cited by 1,183 · see citing works
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) · Nature Medicine · doi:10.1038/70978 · Cited by 1,046 · see citing works
Mogi, M., Harada, M., Riederer, P., Narabayashi, H., Fujita, K., & Nagatsu, T. (1994) · Neuroscience Letters · doi:10.1016/0304-3940(94)90746-3 · Cited by 986 · see citing works
Kim, W., Mohney, R. P., Wilson, B. C., Jeohn, G., Liu, B., & Hong, J. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06309.2000 · Cited by 881 · see citing works
Hoehn, M. M. M., & Yahr, M. D. (1998) · Neurology · doi:10.1212/wnl.50.2.318 · Cited by 873 · see citing works
Raivich, G., Bohatschek, M., Kloss, C. U. A., Werner, A., Jones, L. L., & Kreutzberg, G. W. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00007-7 · Cited by 843 · see citing works
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. G., et al. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.251341998 · Cited by 789 · see citing works
Gao, H., Jiang, J., Wilson, B. C., Zhang, W., Hong, J., & Liu, B. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.00928.x · Cited by 690 · see citing works
Understanding cell death in parkinson's disease
Jenner, P., & Olanow, C. W. (1998) · Annals of Neurology · doi:10.1002/ana.410440712 · Cited by 686 · see citing works
Hunot, S., Brugg, B., Ricard, D., Michel, P. P., Muriel, M., Ruberg, M., Faucheux, B. A., Agid, Y., & Hirsch, É. C. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.14.7531 · Cited by 678 · see citing works
Nitric oxide synthase and neuronal vulnerability in parkinson's disease
Hunot, S., Boissière, F., Faucheux, B., Brugg, B., Mouatt-Prigent, A., Agid, Y., & Hirsch, E. C. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00578-1 · Cited by 595 · see citing works
Immunocytochemical analysis of tumor necrosis factor and its receptors in Parkinson's disease
Boka, G., Anglade, P., Wallach, D., Javoy-Agid, F., Agid, Y., & Hirsch, É. C. (1994) · Neuroscience Letters · doi:10.1016/0304-3940(94)90684-x · Cited by 591 · see citing works
Rate of cell death in parkinsonism indicates active neuropathological process
McGeer, P. L., Itagaki, S., Akiyama, H., & McGeer, E. G. (1988) · Annals of Neurology · doi:10.1002/ana.410240415 · Cited by 557 · see citing works
Quantitative aspects of reactive gliosis: A review
Norton, W. T., Aquino, D. A., Hozumi, I., Chiu, F., & Brosnan, C. F. (1992) · Neurochemical Research · doi:10.1007/bf00993263 · Cited by 549 · see citing works
Mogi, M., Harada, M., Narabayashi, H., Inagaki, H., Minami, M., & Nagatsu, T. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(96)12706-3 · Cited by 545 · see citing works
Protein Nitration in Parkinsonʼs Disease
Good, P. F., Hsu, A., Werner, P., Perl, D. P., & Olanow, C. W. (1998) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/00005072-199804000-00006 · Cited by 540 · see citing works
Prospects for new restorative and neuroprotective treatments in Parkinson's disease
Dunnett, S. B., & Björklund, A. (1999) · Nature · doi:10.1038/399a032 · Cited by 539 · see citing works
Inflammatory Regulators in Parkinson's Disease: iNOS, Lipocortin-1, and Cyclooxygenases-1 and -2
Knott, C., Stern, G., & Wilkin, G. P. (2000) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2000.0914 · Cited by 503 · see citing works
Glutathione peroxidase, glial cells and Parkinson's disease
Damier, P., Hirsch, É. C., Zhang, P., Agid, Y., & Javoy-Agid, F. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90175-f · Cited by 466 · see citing works
Wakabayashi, K., Hayashi, S., Yoshimoto, M., Kudo, H., & Takahashi, H. (2000) · Acta Neuropathologica · doi:10.1007/pl00007400 · Cited by 439 · see citing works
Distinct Role for Microglia in Rotenone-Induced Degeneration of Dopaminergic Neurons
Gao, H., Hong, J., Zhang, W., & Liu, B. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-03-00782.2002 · Cited by 439 · see citing works
Glial pathology but absence of apoptotic nigral neurons in long‐standing Parkinson's disease
Banati, R. B., Daniel, S. E., & Blunt, S. B. (1998) · Movement Disorders · doi:10.1002/mds.870130205 · Cited by 430 · see citing works
Aloisi, F., Ria, F., & Adorini, L. (2000) · Immunology Today · doi:10.1016/s0167-5699(99)01512-1 · Cited by 390 · see citing works
Kurkowska‐Jastrzębska, I., Wrońska, A., Kohutnicka, M., Członkowski, A., & Członkowska, A. (1999) · Experimental Neurology · doi:10.1006/exnr.1998.6993 · Cited by 379 · see citing works
The Sydney multicentre study of Parkinson's disease: progression and mortality at 10 years
Hely, M. A., Morris, J. G., Traficante, R., Reid, W. G. J., O'Sullivan, D. J., & Williamson, P. M. (1999) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.67.3.300 · Cited by 378 · see citing works
Hunot, S., Dugas, N., Faucheux, B. A., Hartmann, A., Tardieu, M., Debré, P., Agid, Y., Dugas, B., & Hirsch, É. C. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-09-03440.1999 · Cited by 365 · see citing works
He, Y., Appel, S. H., & Le, W. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02681-6 · Cited by 350 · see citing works
Liu, B., Du, L., & Hong, J.-S. (2000) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)39275-4 · Cited by 347 · see citing works
Glial cells and inflammation in parkinson's disease: A role in neurodegeneration?
Hirsch, É. C., Hunot, S., Damier, P., & Faucheux, B. A. (1998) · Annals of Neurology · doi:10.1002/ana.410440717 · Cited by 334 · see citing works
Mirza, B., Hadberg, H., Thomsen, P., & Moos, T. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00455-8 · Cited by 327 · see citing works
The role of glial cells in Parkinsonʼs disease
Vila, M., Jackson-Lewis, V., Guégan, C., Chu Wu, D., Teismann, P., Choi, D.-K., Tieu, K., & Przedborski, S. (2001) · Current Opinion in Neurology · doi:10.1097/00019052-200108000-00009 · Cited by 326 · see citing works
Control of glial immune function by neurons
Neumann, H. (2001) · Glia · doi:10.1002/glia.1108 · Cited by 319 · see citing works
The origin and differentiation of microglial cells during development
Cuadros, M. Á. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00035-5 · Cited by 305 · see citing works
A one-hit model of cell death in inherited neuronal degenerations
Clarke, G. D., Collins, R. A., Leavitt, B. R., Andrews, D. F., Hayden, M. R., Lumsden, C. J., & McInnes, R. R. (2000) · Nature · doi:10.1038/35018098 · Cited by 303 · see citing works
Hardman, C. D., Henderson, J. M., Finkelstein, D. I., Horne, M. K., Paxinos, G., & Halliday, G. M. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10165 · Cited by 282 · see citing works
Self-citationGiasson, B. I., Ischiropoulos, H., Lee, V. M. ‐., & Trojanowski, J. Q. (2002) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)00804-3 · Cited by 281 · see citing works
The microglial cell. A historical review
Barron, K. D. (1995) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(95)00209-k · Cited by 279 · see citing works
Perry, V. H. (1998) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(98)00145-3 · Cited by 276 · see citing works
Mediated efflux of IgG molecules from brain to blood across the blood–brain barrier
Zhang, Y., & Pardridge, W. M. (2001) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(01)00242-9 · Cited by 272 · see citing works
Glial cell influence on the human blood‐brain barrier
Prat, A., Biernacki, K., Wosik, K., & Antel, J. P. (2001) · Glia · doi:10.1002/glia.1104 · Cited by 269 · see citing works
Lymphocyte populations in Parkinson's disease and in rat models of parkinsonism
Bas, J. (2001) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(00)00422-7 · Cited by 250 · see citing works
Iravani, M. M., Kashefi, K., Mander, P., Rose, S., & Jenner, P. (2002) · Neuroscience · doi:10.1016/s0306-4522(01)00562-0 · Cited by 247 · see citing works
Ling, Z., Gayle, D. A., Ma, S. Y., Lipton, J. W., Tong, C. W., Hong, J., & Carvey, P. M. (2002) · Movement Disorders · doi:10.1002/mds.10078 · Cited by 241 · see citing works
Williams, K. C., Alvarez, X. A., & Lackner, A. A. (2001) · Glia · doi:10.1002/glia.1105 · Cited by 237 · see citing works
Lewy bodies in Parkinson's disease are recognized by antibodies to complement proteins
Yamada, T., McGeer, P. L., & McGeer, E. G. (1992) · Acta Neuropathologica · doi:10.1007/bf00427222 · Cited by 231 · see citing works
Flaris, N. A., Densmore, T. L., Molleston, M. C., & Hickey, W. F. (1993) · Glia · doi:10.1002/glia.440070108 · Cited by 224 · see citing works
Microglia in neurodegeneration: Molecular aspects
Gebicke‐Haerter, P. J. (2001) · Microscopy Research and Technique · doi:10.1002/jemt.1120 · Cited by 212 · see citing works
Gayle, D. A., Ling, Z., Tong, C. W., Landers, T. M., Lipton, J. W., & Carvey, P. M. (2002) · Developmental Brain Research · doi:10.1016/s0165-3806(01)00315-7 · Cited by 201 · see citing works
Inflammation in Parkinson's disease.
McGeer, P. L., Yasojima, K., & McGeer, E. G. (2001) · PubMed · Cited by 196 · see citing works
Lukiw, W. J., & Bazan, N. G. (1998) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19980901)53:5 · Cited by 183 · see citing works
Amantadine treatment is an independent predictor of improved survival in Parkinson's disease
Uitti, R. J., Rajput, A. H., Ahlskog, J. E., Offord, K. P., Schroeder, D. R., Ho, M. M., Prasad, M., Rajput, A. H., & Basran, P. (1996) · Neurology · doi:10.1212/wnl.46.6.1551 · Cited by 171 · see citing works
Savchenko, V. L., McKanna, J. A., Nikonenko, I., & Skibo, G. G. (2000) · Neuroscience · doi:10.1016/s0306-4522(99)00538-2 · Cited by 168 · see citing works
Flügel, A., Bradl, M., Kreutzberg, G. W., & Graeber, M. B. (2001) · Journal of Neuroscience Research · doi:10.1002/jnr.1198 · Cited by 155 · see citing works
Oxidative damage and cytogenetic analysis in leukocytes of Parkinson’s disease patients
Migliore, L., Petrozzi, L., Lucetti, C., Gambaccini, G., Bernardini, S., Scarpato, R., Trippi, F., Barale, R., Frenzilli, G., Rodilla, V., et al. (2002) · Neurology · doi:10.1212/wnl.58.12.1809 · Cited by 152 · see citing works
Increased cerebrospinal fluid concentration of nitrite in Parkinsonʼs disease
Qureshi, G. A., Baig, S., Bednar, I., Södersten, P., Forsberg, G., & Sidén, Å. (1995) · Neuroreport · doi:10.1097/00001756-199508000-00013 · Cited by 135 · see citing works
Specific A10 Dopaminergic Nuclei in the Midbrain Degenerate in Parkinson's Disease
McRitchie, D. A., Cartwright, H., & Halliday, G. M. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6418 · Cited by 135 · see citing works
Self-citationIncrease in Peripheral CD4 Bright+ CD8 Dull+ T Cells in Parkinson Disease
Hisanaga, K., 浅黄美沙, Itoyama, Y., & Iwasaki, Y. (2001) · Archives of Neurology · doi:10.1001/archneur.58.10.1580 · Cited by 131 · see citing works
Koutsilieri, E., Sopper, S., Scheller, C., et al. (2002) · Journal of Neural Transmission · doi:10.1007/s007020200063 · Cited by 128 · see citing works
Neuronal Control of the Immune Response in the Central Nervous System
Neumann, H., & Wekerle, H. (1998) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199801000-00001 · Cited by 122 · see citing works
Experimental Destruction of Substantia Nigra Initiated by Parkinson Disease Immunoglobulins
Chen, S., Le, W.-D., Xie, W., Alexianu, M. E., Engelhardt, J. I., Siklós, L., & Appel, S. H. (1998) · Archives of Neurology · doi:10.1001/archneur.55.8.1075 · Cited by 118 · see citing works
Midbrain neuropathology in idiopathic Parkinson's disease and diffuse Lewy body disease
Halliday, G. M., McRitchie, D. A., Cartwright, H., Pamphlett, R., Hely, M. A., & Morris, J. G. (1996) · Journal of Clinical Neuroscience · doi:10.1016/s0967-5868(96)90083-1 · Cited by 115 · see citing works
Self-citationKurkowska-Jastrzębska, I., Wrońska, A., Kohutnicka, M., Członkowski, A., & Członkowska, A. (1999) · Acta Neurobiologiae Experimentalis · doi:10.55782/ane-1999-1289 · Cited by 114 · see citing works
Rodrı́guez, M., Barroso‐Chinea, P., Abdala, P., Obeso, J. A., & González‐Hernández, T. (2001) · Experimental Neurology · doi:10.1006/exnr.2000.7624 · Cited by 113 · see citing works
Balancing function vs. self defense: The CNS as an active regulator of immune responses
Carson, M. J., & Sutcliffe, J. G. (1999) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19990101)55:1 · Cited by 99 · see citing works
He, Y., Le, W., & Appel, S. H. (2002) · Experimental Neurology · doi:10.1006/exnr.2002.7946 · Cited by 97 · see citing works
Glial cell death induced by overexpression of α‐synuclein
Stefanova, N., Klimaschewski, L., Poewe, W., Wenning, G. K., & Reindl, M. (2001) · Journal of Neuroscience Research · doi:10.1002/jnr.1171 · Cited by 93 · see citing works
Genetic and environmental risk factors in Parkinson’s disease
Veldman, B. A. J., Wijn, A. M., Knoers, N. V. A. M., Praamstra, P., & Horstink, M. W. I. M. (1998) · Clinical Neurology and Neurosurgery · doi:10.1016/s0303-8467(98)00009-2 · Cited by 91 · see citing works
Neuroprotective Strategies in Parkinson's Disease Using the Models of 6‐Hydroxydopamine and MPTPa
Grünblatt, E., Mandel, S. A., & Youdim, M. B. H. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06192.x · Cited by 91 · see citing works
Mogi, M., Togari, A., Tanaka, K., Ogawa, N., Ichinose, H., & Nagatsu, T. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00388-2 · Cited by 77 · see citing works
Glial cells and Parkinson’s disease
Hirsch, É. C. (2000) · Journal of Neurology · doi:10.1007/pl00007762 · Cited by 76 · see citing works
Aihara, N., Tanno, H., Hall, J. J., Pitts, L. H., & Noble‐Haeusslein, L. J. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903420402 · Cited by 71 · see citing works
Microglia in Cell Culture and in Transplantation Therapy for Central Nervous System Disease
Dobrenis, K. (1998) · Methods · doi:10.1006/meth.1998.0688 · Cited by 68 · see citing works
Togo, T., Iseki, E., Marui, W., Akiyama, H., Uéda, K., & Kosaka, K. (2001) · Journal of the Neurological Sciences · doi:10.1016/s0022-510x(00)00498-6 · Cited by 67 · see citing works
Cortical Inflammation in Alzheimer Disease but Not Dementia With Lewy Bodies
Shepherd, C. E., Thiel, E., McCann, H., Harding, A. J., & Halliday, G. M. (2000) · Archives of Neurology · doi:10.1001/archneur.57.6.817 · Cited by 67 · see citing works
Self-citationAnti-GM1 ganglioside antibodies in Parkinson's disease
Zappia, M., Crescibene, L., Bosco, D., et al. (2002) · Acta Neurologica Scandinavica · doi:10.1034/j.1600-0404.2002.01240.x · Cited by 65 · see citing works
Astroglial ablation prevents MPTP-induced nigrostriatal neuronal death
Takada, M., Li, Z. K., & Hattori, T. (1990) · Brain Research · doi:10.1016/0006-8993(90)90308-x · Cited by 63 · see citing works
Ryu, J. K., Shin, W. H., Kim, J., Joe, E. H., Lee, Y. B., Cho, K. G., Oh, Y. J., Kim, S. U., & Jin, B. K. (2002) · Glia · doi:10.1002/glia.10047 · Cited by 61 · see citing works
Nitric oxide, glial cells and neuronal degeneration in parkinsonism
Hirsch, É. C., & Hunot, S. (2000) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(00)01471-1 · Cited by 58 · see citing works
Preclinical diagnosis of Parkinson's disease.
Horstink, M. W. I. M., & Morrish, P. (1999) · PubMed · Cited by 54 · see citing works
Effects of Cerebrospinal Fluid From Patients With Parkinson Disease on Dopaminergic Cells
Le, W., Rowe, D. B., Jankovic, J. J., Xie, W., & Appel, S. H. (1999) · Archives of Neurology · doi:10.1001/archneur.56.2.194 · Cited by 53 · see citing works
Self-citationBroe, M., Shepherd, C. E., Milward, E. A., & Halliday, G. M. (2001) · Acta Neuropathologica · doi:10.1007/s004010000337 · Cited by 48 · see citing works
Self-citationAnatomy, physiology, and pharmacology of the basal ganglia
Pollack, A. E. (2001) · Neurologic Clinics · doi:10.1016/s0733-8619(05)70032-3 · Cited by 48 · see citing works
Intracerebral regulation of immune responses
Aloisi, F., Ambrosini, E., Cabezas, S. C., Magliozzi, R., & Serafini, B. (2001) · Annals of Medicine · doi:10.3109/07853890108995960 · Cited by 46 · see citing works
McRae‐Degueurce, A., Rosengren, L., Haglid, K. G., et al. (1988) · Neurochemical Research · doi:10.1007/bf00973287 · Cited by 41 · see citing works
Evidence for environmental causation of Parkinson's disease
de la Fuente‐Fernández, R., & Calne, D. B. (2002) · Parkinsonism & Related Disorders · doi:10.1016/s1353-8020(01)00055-4 · Cited by 37 · see citing works
Experimental autoimmune nigral damage in guinea pigs
Le, W. D., Engelhardt, J., Xie, W., et al. (1995) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)00160-p · Cited by 28 · see citing works
Nigral damage and dopaminergic hypofunction in mesencephalon‐immunized guinea pigs
Appel, S. H., Le, W., Tajti, J., Haverkamp, L. J., & Engelhardt, J. I. (1992) · Annals of Neurology · doi:10.1002/ana.410320403 · Cited by 28 · see citing works
Immunoregulation of microglial functional properties
Cross, A. K., & Woodroofe, M. N. (2001) · Microscopy Research and Technique · doi:10.1002/jemt.1115 · Cited by 28 · see citing works
Immunologic Complexity in Neurons
Darnell, R. B. (1998) · Neuron · doi:10.1016/s0896-6273(00)80613-3 · Cited by 23 · see citing works
T-lymphocyte tumor necrosis factor-α receptor binding in patients with Parkinson's disease
Bongioanni, P., Castagna, M., Maltinti, S., Boccardi, B., & Dadone, F. (1997) · Journal of the Neurological Sciences · doi:10.1016/s0022-510x(97)05382-3 · Cited by 18 · see citing works
Tribl, G. G., Wöber, C., Schönborn, V., et al. (2001) · Experimental Gerontology · doi:10.1016/s0531-5565(01)00128-0 · Cited by 17 · see citing works
Jones, K. L., & Barr, G. A. (2000) · Synapse · doi:10.1002/1098-2396(200102)39:2 · Cited by 11 · see citing works
Langston, J. W., Forno, L. S., Tetrud, J., Reeves, A. G., Kaplan, J. A., & Karluk, D. (1999) · Annals of Neurology · doi:10.1002/1531-8249(199910)46:4 · Cited by 1 · see citing works
Zujovic (2000) · doi:10.1002/(sici)1098-1136(20000215)29:4
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- Authors
- Orr, C. F., Rowe, D. B., & Halliday, G. M.
- Affiliations
- Royal North Shore Hospital (AU)
- Corresponding author
- Halliday, G.M
- Venue
- Progress in Neurobiology
- Publisher
- Elsevier BV
- Published
- 2002-12
- Volume
- 68
- Issue
- 5
- Pages
- 325-340
- ISSN
- 0301-0082 (ISSN-L)
- OpenAlex
- W2039542458
- Cited by
- 309
- References
- 106
- Citations by year
- 2026: 2 · 2024: 6 · 2023: 7 · 2022: 10 · 2021: 11 · 2020: 7 · 2019: 10 · 2018: 10 · 2017: 18 · 2016: 15 · 2015: 15 · 2014: 17 · 2013: 15 · 2012: 30
- FWCI
- 2.43
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Progress in Neurobiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nuclear Receptors and Signaling
- Keywords
- Parkinson's disease, neuroinflammation, microglia, dopaminergic neuron loss, ubiquitin-proteasome system, genetic mutations, protein aggregation, Parkinson's disease model, immune regulation, neuronal homeostasis
- MeSH terms
- Animals, Brain, Gangliosides, Humans, Immunologic Surveillance, Lipopolysaccharides, Neurons, Parkinson Disease, Rotenone, Monitoring, Immunologic, Signal Transduction, 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine, Oxidopamine, Microglia
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