Expression of mutant alpha-synuclein modulates microglial phenotype in vitro
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BACKGROUND: Increased reactive microglia are a histological characteristic of Parkinson's disease (PD) brains, positively correlating with levels of deposited α-synuclein protein. This suggests that microglial-mediated inflammatory events may contribute to disease pathophysiology. Mutations in the gene coding for α-synuclein lead to a familial form of PD. Based upon our prior findings that α-synuclein expression regulates microglial phenotype we hypothesized that expression of mutant forms of the protein may contribute to the reactive microgliosis characteristic of PD brains. METHODS: To quantify the effects of wild type and mutant α-synuclein over-expression on microglial phenotype a murine microglial cell line, BV2, was transiently transfected to express human wild type (WT), and mutant α-synuclein (A30P and A53T) proteins. Transfected cells were used to assess changes in microglia phenotype via Western blot analysis, ELISA, phagocytosis, and neurotoxicity assays. RESULTS: As expected, over-expression of α-synuclein induced a reactive phenotype in the transfected cells. Expression of α-synuclein increased protein levels of cycloxygenase-2 (Cox-2). Transfected cells demonstrated increased secretion of the proinflammatory cytokines, tumor necrosis factor-α (TNF-α) and interleukin-6 (IL-6), as well as increased nitric oxide production. Transfected cells also had impaired phagocytic ability correlating with decreased protein levels of lysosomal-associated membrane protein 1 (LAMP-1). In spite of the increased cytokine secretion profile, the transfected cells did not exhibit increased neurotoxic ability above control non-transfected BV2 cells in neuron-microglia co-cultures. CONCLUSIONS: These data demonstrated that over-expression of α-synuclein drives microglial cells into a form of reactive phenotype characterized by elevated levels of arachidonic acid metabolizing enzymes, cytokine secretion, and reactive nitrogen species secretion all superimposed upon impaired phagocytic potential.
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α-Syn has been shown to increase the expression of COX-2 and the activity of microglial NADPH oxidase via CD11b.
“Moreover, α-Syn has been shown to increase the expression of COX-2 [116] and the activity of microglial NADPH oxidase via CD11b [117].”
From Beneficial Effects of Spirulina Consumption on Brain Health (2022) · cites this paper as [116]
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Cites
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302 · see citing works
Mutation in the α-Synuclein Gene Identified in Families with Parkinson's Disease
Polymeropoulos, M. H., Lavedan, C., Leroy, E., Ide, S. E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R., et al. (1997) · Science · doi:10.1126/science.276.5321.2045 · Cited by 8,240 · 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
α-Synuclein Locus Triplication Causes Parkinson's Disease
Singleton, A. B., Farrer, M., Johnson, J., Singleton, A., Hague, S., Kachergus, J., Hulihan, M., Peuralinna, T., Dutra, A., Nussbaum, R., et al. (2003) · Science · doi:10.1126/science.1090278 · Cited by 4,383 · see citing works
AlaSOPro mutation in the gene encoding α-synuclein in Parkinson's disease
Krüger, R., Kuhn, W., Müller, T., Woitalla, D., Graeber, M., Kösel, S., Przuntek, H., Epplen, J. T., Schols, L., & Riess, O. (1998) · Nature Genetics · doi:10.1038/ng0298-106 · Cited by 3,836 · 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
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
Synuclein: a neuron-specific protein localized to the nucleus and presynaptic nerve terminal
Maroteaux, L., Campanelli, J., & Scheller, R. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-08-02804.1988 · Cited by 1,646 · see citing works
MCGEER, P., & MCGEER, E. (1995) · Brain Research Reviews · doi:10.1016/0165-0173(95)00011-9 · Cited by 1,287 · see citing works
Zhang, W., Wang, T., Pei, Z., Miller, D. S., Wu, X., Block, M. L., Wilson, B., Zhang, W., Zhou, Y., Hong, J.-S., et al. (2005) · The FASEB Journal · doi:10.1096/fj.04-2751com · Cited by 1,265 · see citing works
Tumor Necrosis Factor-α: A Mediator of Focal Ischemic Brain Injury
Barone, F. C., Arvin, B., White, R. F., Miller, A., Webb, C. L., Willette, R. N., Lysko, P. G., & Feuerstein, G. Z. (1997) · Stroke · doi:10.1161/01.str.28.6.1233 · Cited by 863 · see citing works
Yeast Cells Provide Insight into Alpha-Synuclein Biology and Pathobiology
Outeiro, T. F., & Lindquist, S. L. (2003) · Science · doi:10.1126/science.1090439 · Cited by 808 · see citing works
Intravesicular Localization and Exocytosis of α-Synuclein and its Aggregates
Lee, H.-J., Patel, S. S., & Lee, S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0692-05.2005 · Cited by 798 · see citing works
Imamura, K., Hishikawa, N., Sawada, M., Nagatsu, T., Yoshida, M., & Hashizume, Y. (2003) · Acta Neuropathologica · doi:10.1007/s00401-003-0766-2 · Cited by 791 · see citing works
Glial reactions in Parkinson's disease
McGeer, P. L., & McGeer, E. G. (2008) · Movement Disorders · doi:10.1002/mds.21751 · Cited by 701 · see citing works
Microglia in health and disease
Kim, S. U., & de Vellis, J. (2005) · Journal of Neuroscience Research · doi:10.1002/jnr.20562 · Cited by 663 · see citing works
Cyclooxygenase-2 is instrumental in Parkinson's disease neurodegeneration
Teismann, P., Tieu, K., Choi, D., Wu, D., Naini, A., Hunot, S., Vila, M., Jackson-Lewis, V. R., & Przedborski, S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0837397100 · Cited by 659 · see citing works
Parkinson's disease: pathophysiology
Agid, Y. (1991) · The Lancet · doi:10.1016/0140-6736(91)92989-f · Cited by 530 · see citing works
The Parkinson's disease protein α-synuclein disrupts cellular Rab homeostasis
Gitler, A. D., Bevis, B. J., Shorter, J., Strathearn, K. E., Hamamichi, S., Su, L. J., Caldwell, K. A., Caldwell, G. A., Rochet, J., McCaffery, J. M., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710685105 · Cited by 527 · see citing works
Rock, C. S., & Lowry, S. F. (1991) · Journal of Surgical Research · doi:10.1016/0022-4804(91)90146-d · Cited by 506 · 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
Synuclein activates microglia in a model of Parkinson's disease
Su, X., Maguire-Zeiss, K. A., Giuliano, R., Prifti, L., Venkatesh, K., & Federoff, H. J. (2008) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.04.006 · Cited by 474 · cited 2× · see citing works
“It is assumed that microgliosis occurs during disease in part due to neuronal secretion of a-synuclein which directly stimulates microglia in a fashion requiring CD36 [16,67].”
BackgroundBraak, H., Sastre, M., & Del Tredici, K. (2007) · Acta Neuropathologica · doi:10.1007/s00401-007-0244-3 · Cited by 462 · 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
Interaction of Human α-Synuclein and Parkinson's Disease Variants with Phospholipids
Perrin, R. J., Woods, W. S., Clayton, D. F., & George, J. M. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m004851200 · Cited by 432 · see citing works
Jenco, J. M., Rawlingson, A., Daniels, B., & Morris, A. J. (1998) · Biochemistry · doi:10.1021/bi972776r · Cited by 431 · see citing works
Hunot, S., Vila, M., Teismann, P., Davis, R. J., Hirsch, É. C., Przedborski, S., RAKIC, P. T., & Flavell, R. A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307453101 · Cited by 427 · see citing works
Brain Dendritic Cells and Macrophages/Microglia in Central Nervous System Inflammation
Fischer, H., & Reichmann, G. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.4.2717 · Cited by 408 · see citing works
Theodore, S., Cao, S., McLean, P. J., & Standaert, D. G. (2008) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e31818e5e99 · Cited by 367 · see citing works
An immortalized cell line expresses properties of activated microglial cells
Bocchini, V., Mazzolla, R., Barluzzi, R., Blasi, E., Sick, P., & Kettenmann, H. (1992) · Journal of Neuroscience Research · doi:10.1002/jnr.490310405 · Cited by 364 · see citing works
Gu, X., Long, C.-X., Sun, L., Xie, C., Lin, X. Z., & Cai, H. (2010) · Molecular Brain · doi:10.1186/1756-6606-3-12 · Cited by 341 · see citing works
Molecular consequences of activated microglia in the brain: overactivation induces apoptosis
Liu, B., Wang, K., Gao, H.-M., Mandavilli, B., Wang, J.-Y., & Hong, J.-S. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.t01-1-00216.x · Cited by 286 · see citing works
Lee, E.-J., Woo, M.-S., Moon, P., Baek, M., Choi, I.-Y., Kim, W.-K., Junn, E., & Kim, H.-S. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0903480 · Cited by 267 · see citing works
Role of the pro‐inflammatory cytokines TNF‐α and IL‐1β in HIV‐associated dementia
Brabers, N. A. C. H., & Nottet, H. S. L. M. (2006) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.2006.01657.x · Cited by 265 · see citing works
Sanchez-Guajardo, V., Febbraro, F., Kirik, D., & Romero-Ramos, M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008784 · Cited by 256 · see citing works
Effect of the overexpression of wild‐type or mutant α‐synuclein on cell susceptibility to insult
Lee, M., Hyun, D., Halliwell, B. B., & Jenner, P. G. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00149.x · Cited by 232 · see citing works
α-Synuclein activates stress signaling protein kinases in THP-1 cells and microglia
Klegeris, A., Pelech, S., Giasson, B. I., Maguire, J., Zhang, H., McGeer, E. G., & McGeer, P. L. (2008) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.11.013 · Cited by 227 · see citing works
Bodner, C. R., Maltsev, A. S., Dobson, C. M., & Bax, A. (2009) · Biochemistry · doi:10.1021/bi901723p · Cited by 227 · see citing works
α-Synuclein Binds Large Unilamellar Vesicles as an Extended Helix
Trexler, A., & Rhoades, E. R. (2009) · Biochemistry · doi:10.1021/bi900114z · Cited by 212 · see citing works
Zhou, W., Hurlbert, M. S., Schaack, J. B., Prasad, K. N., & Freed, C. R. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02215-0 · Cited by 204 · see citing works
Nguyen, H. X., O’Barr, T. J., & Anderson, A. J. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04643.x · Cited by 191 · see citing works
COX‐2 and Neurodegeneration in Parkinson's Disease
Teismann, P., Vila, M., Choi, D., Tieu, K., Wu, D.-C., Jackson-Lewis, V. R., & Przedborski, S. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07482.x · Cited by 178 · see citing works
Mitochondrial localization of alpha-synuclein protein in alpha-synuclein overexpressing cells
Shaik, S., Brown‐Borg, H. M., Ebadi, M., & Porter, J. E. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2008.05.005 · Cited by 161 · see citing works
Efferocytosis impairs pulmonary macrophage and lung antibacterial function via PGE2/EP2 signaling
de Medeiros, A. I., Serezani, C. H., Lee, S. P., & Peters-Golden, M. L. (2009) · The Journal of Experimental Medicine · doi:10.1084/jem.20082058 · Cited by 160 · see citing works
Peng, J., Stevenson, F. F., Doctrow, S. R., & Andersen, J. K. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m500984200 · Cited by 159 · see citing works
Prostaglandin H Synthetase‐Mediated Metabolism of Dopamine: Implication for Parkinson's Disease
Mattammal, M. B., Strong, R., Lakshmi, V. M., Chung, H. D., & Stephenson, A. H. (1995) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1995.64041645.x · Cited by 151 · see citing works
Park, J., Paik, S. R., Jou, I., & Park, S. M. (2008) · Glia · doi:10.1002/glia.20691 · Cited by 151 · see citing works
Mori, F., Tanji, K., Yoshimoto, M., Takahashi, H., & Wakabayashi, K. (2002) · Experimental Neurology · doi:10.1006/exnr.2002.7929 · Cited by 149 · see citing works
Mutant α-Synuclein Overexpression Mediates Early Proinflammatory Activity
Su, X., Federoff, H. J., & Maguire-Zeiss, K. A. (2009) · Neurotoxicity Research · doi:10.1007/s12640-009-9053-x · Cited by 145 · see citing works
Nguyen, H. X., O’Barr, T. J., & Anderson, A. J. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.004643.x · Cited by 145 · see citing works
α-Synuclein Expression Modulates Microglial Activation Phenotype
Austin, S. A., Floden, A. M., Murphy, E. J., & Combs, C. K. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1799-06.2006 · Cited by 142 · see citing works
Self-citationKingham, P. J., Cuzner, M. L., & Pocock, J. M. (1999) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1999.0730538.x · Cited by 138 · see citing works
Ahn, B., Rhim, H., Kim, S. Y., Sung, Y., Lee, M., Choi, J., Wolozin, B. L., Chang, J., Lee, Y. H., Kwon, T. K., et al. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m110414200 · Cited by 136 · see citing works
Levi, G., Minghetti, L., & Aloisi, F. (1998) · Biochimie · doi:10.1016/s0300-9084(00)88886-0 · Cited by 133 · see citing works
α‐Synuclein sequesters arachidonic acid to modulate SNARE‐mediated exocytosis
Darios, F. D., Ruipérez, V., López‐Font, I., Villanueva, J., Gutiérrez, L. M., & Davletov, B. A. (2010) · EMBO Reports · doi:10.1038/embor.2010.66 · Cited by 115 · see citing works
Jin, J., Shie, F., Liu, J., Wang, Y., Davis, J., Schantz, A. M., Montine, K. S., Montine, T. J., & Zhang, J. (2007) · Journal of Neuroinflammation · doi:10.1186/1742-2094-4-2 · Cited by 112 · see citing works
Golovko, M. Y., Færgeman, N. J., Cole, N. B., Castagnet, P. I., Nussbaum, R. L., & Murphy, E. J. (2005) · Biochemistry · doi:10.1021/bi0502137 · Cited by 110 · see citing works
Self-citationLee, P., Lee, J.-S., Kim, S., Lee, M., Yagita∥, H., Kim, S. Y., Kim, H., & Suk, K. (2001) · Brain Research · doi:10.1016/s0006-8993(00)03257-1 · Cited by 109 · see citing works
Phosphorylation, lipid raft interaction and traffic of α-synuclein in a yeast model for Parkinson
Zabrocki, P., Bastiaens, I., Delay, C., Bammens, T., Ghillebert, R., Pellens, K., VIRGILIO, C. D., LEUVEN, F. V., & Winderickx, J. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2008.06.010 · Cited by 109 · see citing works
Fatty acid incorporation is decreased in astrocytes cultured from α‐synuclein gene‐ablated mice
Castagnet, P. I., Golovko, M. Y., Barceló‐Coblijn, G., Nussbaum, R. L., & Murphy, E. J. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03247.x · Cited by 108 · see citing works
Self-citationBrain neutral lipids mass is increased in α‐synuclein gene‐ablated mice
Barceló‐Coblijn, G., Golovko, M. Y., Weinhofer, I., Berger, J., & Murphy, E. J. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.04348.x · Cited by 107 · see citing works
Self-citationStructural Determinants of PLD2 Inhibition by α-Synuclein
Payton, J. E., Perrin, R. J., Woods, W. S., & George, J. M. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.02.014 · Cited by 99 · see citing works
Golovko, M. Y., Rosenberger, T. A., Færgeman, N. J., Feddersen, S., Cole, N. B., Pribill, I., Berger, J., Nussbaum, R. L., & Murphy, E. J. (2006) · Biochemistry · doi:10.1021/bi0600289 · Cited by 85 · see citing works
Self-citationJara, J. H., Singh, B. B., Floden, A. M., & Combs, C. K. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.04330.x · Cited by 83 · see citing works
Self-citationExpression of ??-synuclein in a human glioma cell line and its up-regulation by interleukin-1??
Tanji, K., Imaizumi, T., Yoshida, H., Mori, F., Yoshimoto, M., Satoh, K., & Wakabayashi, K. (2001) · Neuroreport · doi:10.1097/00001756-200107030-00028 · Cited by 81 · see citing works
Golovko, M. Y., Barceló‐Coblijn, G., Castagnet, P. I., Austin, S. A., Combs, C. K., & Murphy, E. J. (2008) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-008-0008-y · Cited by 79 · see citing works
Self-citationGolovko, M. Y., Rosenberger, T. A., Feddersen, S., Færgeman, N. J., & Murphy, E. J. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.04357.x · Cited by 78 · see citing works
Self-citationSelective Modulation of BV-2 Microglial Activation by Prostaglandin E2
Petrova, T. V., Akama, K. T., & Eldik, L. J. V. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.40.28823 · Cited by 77 · see citing works
Function of microglia in organotypic slice cultures
Czapiga, M., & Colton, C. A. (1999) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19990615)56:6 · Cited by 77 · see citing works
Hemmer, K., Fransen, L., Vanderstichele, H., Vanmechelen, E., & Heuschling, P. (2001) · Neurochemistry International · doi:10.1016/s0197-0186(00)00119-4 · Cited by 74 · see citing works
Identification of Proteins Involved in Microglial Endocytosis of α-Synuclein
Liu, J., Zhou, Y. F., Wang, Y., Fong, H. K., Murray, T. M., & Zhang, J. (2007) · Journal of Proteome Research · doi:10.1021/pr0701512 · Cited by 74 · see citing works
DJ‐1 is present in a large molecular complex in human brain tissue and interacts with α‐synuclein
Meulener, M. C., Graves, C. L., Sampathu, D. M., Armstrong‐Gold, C. E., Bonini, N. M., & Giasson, B. I. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03145.x · Cited by 71 · see citing works
COX-2-deficient mice are less prone to MPTP-neurotoxicity than wild-type mice
Feng, Z., Li, D., Fung, P. C. W., Pei, Z., Ramsden, D. B., & Ho, S. (2003) · Neuroreport · doi:10.1097/00001756-200310270-00009 · Cited by 65 · see citing works
α‐Synuclein induces migration of BV‐2 microglial cells by up‐regulation of CD44 and MT1‐MMP
Kim, S., Cho, S., Kim, K. Y., Shin, K. Y., Kim, H., Park, C., Chang, K., Lee, S. H., Cho, D., & Suh, Y. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06075.x · Cited by 61 · see citing works
Upregulation of α‐synuclein by lipopolysaccharide and interleukin‐1 in human macrophages
Tanji, K., Mori, F., Imaizumi, T., Yoshida, H., Matsumiya, T., Tamo, W., Yoshimoto, M., Odagiri, H., Sasaki, M., Takahashi, H., et al. (2002) · Pathology International · doi:10.1046/j.1440-1827.2002.01385.x · Cited by 55 · see citing works
Lee, E. O., Shin, Y. J., & Chong, Y. H. (2004) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2004.05.012 · Cited by 54 · see citing works
Identification of the amino acid sequence motif of α-synuclein responsible for macrophage activation
Lee, S.-B., Park, S. M., Ahn, K. J., Chung, K. C., Paik, S. R., & Kim, J. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.02.002 · Cited by 52 · see citing works
Keene, C. D., Chang, R. C., López-Yglesias, A. H., Shalloway, B. R., Sokal, I., Li, X., Reed, P., Keene, L. M., Montine, K. S., BREYER, R. M., et al. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090840 · Cited by 52 · see citing works
Effects of chronic low dose rotenone treatment on human microglial cells
Shaikh, S. B., & Nicholson, L. F. B. (2009) · Molecular Neurodegeneration · doi:10.1186/1750-1326-4-55 · Cited by 52 · see citing works
Association of α-Synuclein and Mutants with Lipid Membranes: Spin-Label ESR and Polarized IR
Ramakrishnan, M., Jensen, P. H., & Marsh, D. (2006) · Biochemistry · doi:10.1021/bi052344d · Cited by 47 · see citing works
Pierre, S.-R., Lemmens, M. A. M., & Figueiredo‐Pereira, M. E. (2009) · Journal of Neuroinflammation · doi:10.1186/1742-2094-6-18 · Cited by 43 · see citing works
Lee, H., Bazinet, R. P., Rapoport, S. I., & Bhattacharjee, A. K. (2009) · Neurochemical Research · doi:10.1007/s11064-009-0106-6 · Cited by 40 · see citing works
Stachowska, E., Baśkiewicz‐Masiuk, M., Dziedziejko, V., Adler, G., Bober, J., Machaliński, B., & Chlubek, D. (2007) · Lipids · doi:10.1007/s11745-007-3072-2 · Cited by 37 · see citing works
Brain prostaglandin formation is increased by α-synuclein gene-ablation during global ischemia
Golovko, M. Y., & Murphy, E. J. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.12.031 · Cited by 36 · see citing works
Self-citationHenry, V., Paillé, V., Lelan, F., Brachet, P., & Damier, P. (2009) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3181b767b4 · Cited by 34 · see citing works
Prostaglandin E2 reduces amyloid β-induced phagocytosis in cultured rat microglia
Nagano, T., Kimura, S. H., & Takemura, M. (2010) · Brain Research · doi:10.1016/j.brainres.2010.01.086 · Cited by 30 · see citing works
Chae, S., Kang, B. Y., Hwang, O., et al. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2008.03.031 · Cited by 28 · see citing works
Quan, N., He, L., & Lai, W. (2003) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(03)00122-x · Cited by 20 · see citing works
Brock, T. G., Serezani, C. H., Carstens, J. K., Peters-Golden, M. L., & Aronoff, D. M. (2007) · Experimental Cell Research · doi:10.1016/j.yexcr.2007.10.011 · Cited by 16 · 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
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Fellner, L., Irschick, R., Schanda, K., Reindl, M., Klimaschewski, L., Poewe, W., Wenning, G. K., & Stefanova, N. (2013) · Glia · doi:10.1002/glia.22437 · Cited by 697 · see citing works
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Acetate reduces microglia inflammatory signaling <i>in vitro</i>
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Pabon, M. M., Jernberg, J. N., Morganti, J., Contreras, J., Hudson, C. E., Klein, R. L., & Bickford, P. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045256 · Cited by 90 · see citing works
Blockade of Kv1.3 channels ameliorates radiation-induced brain injury
Peng, Y., Lu, K., Li, Z., Zhao, Y., Wang, Y., Hu, B., Xu, P., Shi, X., Zhou, B., Pennington, M., et al. (2014) · Neuro-Oncology · doi:10.1093/neuonc/not221 · Cited by 78 · see citing works
- Authors
- Rojanathammanee, L., Murphy, E. J., & Combs, C. K.
- Affiliations
- University of North Dakota (US)
- Corresponding author
- Combs, Colin K
- Venue
- Journal of Neuroinflammation
- Published
- 2011-05-09
- Volume
- 8
- Issue
- 1
- Pages
- 44-44
- ISSN
- 1742-2094 (ISSN-L)
- PMC
- PMC3104357
- OpenAlex
- W2106181734
- Cited by
- 106
- References
- 90
- Citations by year
- 2026: 1 · 2025: 8 · 2024: 10 · 2023: 6 · 2022: 8 · 2021: 12 · 2020: 11 · 2019: 4 · 2018: 8 · 2017: 3 · 2016: 6 · 2015: 8 · 2014: 6 · 2013: 8 · 2012: 7
- FWCI
- 3.71
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Journal of Neuroinflammation (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health
- National Institute on Aging (R01AG026330)
- National Institute of Neurological Disorders and Stroke (R21NS060141)
- National Center for Research Resources (2 P20RR017600)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nuclear Receptors and Signaling
- Keywords
- alpha-synuclein, Parkinson's disease, reactive microgliosis, microglial phenotype, cyclooxygenase-2, arachidonic acid metabolism, inflammatory cytokines, TNF-α, interleukin-6, nitric oxide, phagocytosis, LAMP1, neuroinflammation, neurotoxicity
- MeSH terms
- Animals, Cell Line, Humans, Lysosomes, Mice, Inbred C57BL, Mutation, Nitrites, Parkinson Disease, Phagocytosis, Phenotype, Phospholipase D, Tumor Necrosis Factor-alpha, Interleukin-6, Microglia, Reactive Nitrogen Species, Mice, Cyclooxygenase 1, Cyclooxygenase 2, alpha-Synuclein, Lysosomal-Associated Membrane Protein 1
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