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Journal of Neuroinflammation
Published in: Journal of Neuroinflammation 1/2014

Open Access 01-12-2014 | Research

Chronic stress enhances microglia activation and exacerbates death of nigral dopaminergic neurons under conditions of inflammation

Authors: Rocío M de Pablos, Antonio J Herrera, Ana M Espinosa-Oliva, Manuel Sarmiento, Mario F Muñoz, Alberto Machado, José L Venero

Published in: Journal of Neuroinflammation | Issue 1/2014

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Abstract

Background

Parkinson’s disease is an irreversible neurodegenerative disease linked to progressive movement disorders and is accompanied by an inflammatory reaction that is believed to contribute to its pathogenesis. Since sensitivity to inflammation is not the same in all brain structures, the aim of this work was to test whether physiological conditions as stress could enhance susceptibility to inflammation in the substantia nigra, where death of dopaminergic neurons takes place in Parkinson’s disease.

Methods

To achieve our aim, we induced an inflammatory process in nonstressed and stressed rats (subject to a chronic variate stress) by a single intranigral injection of lipopolysaccharide, a potent proinflammogen. The effect of this treatment was evaluated on inflammatory markers as well as on neuronal and glial populations.

Results

Data showed a synergistic effect between inflammation and stress, thus resulting in higher microglial activation and expression of proinflammatory markers. More important, the higher inflammatory response seen in stressed animals was associated with a higher rate of death of dopaminergic neurons in the substantia nigra, the most characteristic feature seen in Parkinson’s disease. This effect was dependent on glucocorticoids.

Conclusions

Our data demonstrate that stress sensitises midbrain microglia to further inflammatory stimulus. This suggests that stress may be an important risk factor in the degenerative processes and symptoms of Parkinson’s disease.
Appendix
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Literature
1.
Olanow CW, Shapira AHV, Agid Y: Neuroprotection for Parkinson’s disease: prospects and promises. Ann Neurol. 2003, 53 (Suppl 3): S1-S2.PubMed
2.
Dauer W, Przedborski S: Parkinson’s disease: mechanisms and models. Neuron. 2003, 39: 889-909. 10.1016/S0896-6273(03)00568-3.PubMed
3.
Di Monte DA, Langston JW: Idiopathic and 1-methyl-4phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced Parkinsonism. Neuroglia. Edited by: Kettenmann H, Ransom BR. 1995, New York: Oxford University Press, 989-997.
4.
Lesage S, Brice A: Parkinson’s disease: from monogenic forms to genetic susceptibility factors. Hum Mol Genet. 2009, 18 (R1): R48-R59. 10.1093/hmg/ddp012.PubMed
5.
Gao HM, Liu B, Zhang W, Hong JS: Synergistic dopaminergic neurotoxicity of MPTP and inflammogen lipopolysaccharide: relevance to the etiology of Parkinson’s disease. FASEB J. 2003, 17: 1957-1959.PubMed
6.
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.PubMed
7.
Jenner P: Oxidative stress in Parkinson’s disease. Ann Neurol. 2003, 53 (Suppl 3): S26-S38.PubMed
8.
Marchetti B, Abbracchio MP: To be or not to be (inflamed): Is that the question in anti-inflammatory drug therapy of neurodegenerative disorders?. Trends Pharmacol Sci. 2005, 26: 517-525. 10.1016/j.tips.2005.08.007.PubMed
9.
Marchetti B, Serra PA, L’Episcopo F, Tirolo C, Caniglia S, Testa N, Cioni S, Gennuso F, Rocchitta G, Desole MS, Mazzarino MC, Miele E, Morale MC: Hormones are key actors in gene × environment interactions programming vulnerability to Parkinson’s disease: glia as a common final pathway. Ann N Y Acad Sci. 2005, 1057: 296-318. 10.1196/annals.1356.023.PubMed
10.
Marchetti B, Serra PA, Tirolo C, ’L’Episcopo F, Caniglia S, Gennuso F, Testa N, Miele E, Desole S, Barden N, Morale MC: Glucocorticoid receptor–nitric oxide crosstalk and vulnerability to experimental Parkinsonism: pivotal role for glia–neuron interactions. Brain Res Rev. 2005, 48: 302-321. 10.1016/j.brainresrev.2004.12.030.PubMed
11.
McGeer PL, McGeer EG: Inflammation and neurodegeneration in Parkinson’s disease. Parkinsonism Relat Disord. 2004, 10 (Suppl 1): S3-S7.PubMed
12.
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. 10.1212/WNL.38.8.1285.PubMed
13.
Klegeris A, McGeer EG, McGeer PL: Therapeutic approaches to inflammation in neurodegenerative disease. Curr Opin Neurol. 2007, 20: 351-357. 10.1097/WCO.0b013e3280adc943.PubMed
14.
McGeer PL, McGeer EG: Glial reactions in Parkinson’s disease. Mov Disord. 2008, 23: 474-483. 10.1002/mds.21751.PubMed
15.
Tansey MG, McCoy MK, Frank-Cannon TC: Neuroinflammatory mechanisms in Parkinson’s disease: potential environmental triggers, pathways, and targets for early therapeutic intervention. Exp Neurol. 2007, 208: 1-25. 10.1016/j.expneurol.2007.07.004.PubMedCentralPubMed
16.
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.PubMed
17.
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.PubMed
18.
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.PubMed
19.
Miklossy J, Doudet DD, Schwab C, Yu S, McGeer EG, McGeer PL: Role of ICAM-1 in persisting inflammation in Parkinson disease and MPTP monkeys. Exp Neurol. 2006, 197: 275-283. 10.1016/j.expneurol.2005.10.034.PubMed
20.
Holst O, Ulmer AJ, Brade H, Flad HD, Rietschel ET: Biochemistry and cell biology of bacterial endotoxins. FEMS Immunol Med Microbiol. 1996, 16: 83-104. 10.1111/j.1574-695X.1996.tb00126.x.PubMed
21.
Kielian TL, Blecha F: CD14 and other recognition molecules for lipopolysaccharide: a review. Immunopharmacology. 1995, 29: 187-205. 10.1016/0162-3109(95)00003-C.PubMed
22.
Godoy M, Tarelli R, Ferrari CC, Sarchi MI, Pitossi FJ: Central and systemic IL-1 exacerbates neurodegeneration and motor symptoms in a model of Parkinson’s disease. Brain. 2008, 131: 1880-1894. 10.1093/brain/awn101.PubMedCentral
23.
Chen H, Jacobs E, Schwarzschild MA, McCullough ML, Calle EE, Thun MJ, Ascherio A: Nonsteroidal antiinflammatory drug use and the risk for Parkinson’s disease. Ann Neurol. 2005, 58: 963-967. 10.1002/ana.20682.PubMed
24.
Chen H, Zhang S, Hernán 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.PubMed
25.
Esposito E, Di Matteo V, Benigno A, Pierucci M, Crescimanno G, Di Giovanni G: Non-steroidal anti-inflammatory drugs in Parkinson’s disease. Exp Neurol. 2007, 205: 295-312. 10.1016/j.expneurol.2007.02.008.PubMed
26.
Castaño 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.PubMed
27.
Castaño A, Herrera AJ, Cano J, Machado A: The degenerative effect of a single intranigral injection of LPS on the dopaminergic system is prevented by dexamethasone, and not mimicked by rh-TNF-α, IL-1β and IFN-γ. J Neurochem. 2002, 81: 150-157. 10.1046/j.1471-4159.2002.00799.x.PubMed
28.
Herrera AJ, Castaño A, Venero JL, Cano J, Machado A: The single intranigral injection of LPS as a new model for studying the selective effects of inflammatory reactions on dopaminergic system. Neurobiol Dis. 2000, 7: 429-447. 10.1006/nbdi.2000.0289.PubMed
29.
Kim WG, Mohney RP, Wilson B, Jeohn GH, Liu B, Hong JS: Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J Neurosci. 2000, 20: 6309-6316.PubMed
30.
Gayle DA, Ling Z, Tong C, Landers T, Lipton JW, Carvey PM: Lipopolysaccharide (LPS)-induced dopamine cell loss in culture: roles of tumor necrosis factor-α, interleukin-1β, and nitric oxide. Brain Res Dev Brain Res. 2002, 133: 27-35. 10.1016/S0165-3806(01)00315-7.PubMed
31.
Jeohn GH, Cooper CL, Wilson B, Chang RC, Jang KJ, Kim HC, Liu B, Hong JS: p38 MAP kinase is involved in lipopolysaccharide-induced dopaminergic neuronal cell death in rat mesencephalic neuron-glia cultures. Ann N Y Acad Sci. 2002, 962: 332-346. 10.1111/j.1749-6632.2002.tb04078.x.PubMed
32.
Liu B, Du L, Hong JS: Naloxone protects rat dopaminergic neurons against inflammatory damage through inhibition of microglia activation and superoxide generation. J Pharmacol Exp Ther. 2000, 293: 607-617.PubMed
33.
Liu Y, Qin L, Li G, Zhang W, An L, Liu B, Hong JS: Dextromethorphan protects dopaminergic neurons against inflammation-mediated degeneration through inhibition of microglial activation. J Pharmacol Exp Ther. 2003, 305: 212-218. 10.1124/jpet.102.043166.PubMed
34.
Foley P, Gerlach M, Double KL, Riederer P: Dopamine receptor agonists in the therapy of Parkinson’s disease. J Neural Transm. 2004, 111: 1375-1446. 10.1007/s00702-003-0059-x.PubMed
35.
Caspi A, Sugden K, Moffitt TE, Taylor A, Craig IW, Harrington H, McClay J, Mill J, Martin J, Braithwaite A, Poulton R: Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science. 2003, 301: 386-389. 10.1126/science.1083968.PubMed
36.
Kendler KS, Karkowski-Shuman L: Stressful life events and genetic liability to major depression: genetic control of exposure to the environment?. Psychol Med. 1997, 27: 539-547. 10.1017/S0033291797004716.PubMed
37.
Charcot JM: Lectures on the Diseases of the Nervous System, Volume 1. 1878, London: The New Sydenham Society, (English translation by Sigerson G)
38.
Gowers WR: (American edition). Diseases of the Nervous System. 1888, Philadelphia, PA: Blakiston, Son & Co
39.
McEwen BS: Protective and damaging effects of stress mediators: the good and bad sides of the response to stress. Metabolism. 2002, 51 (6 Suppl 1): 2-4.PubMed
40.
McEwen BS: The neurobiology of stress: from serendipity to clinical relevance. Brain Res. 2000, 886: 172-189. 10.1016/S0006-8993(00)02950-4.PubMed
41.
de Kloet ER, Joles M, Holsboer F: Stress and the brain: from adaptation to disease. Nat Rev Neurosci. 2005, 6: 463-475. 10.1038/nrn1683.PubMed
42.
Joëls M, Krugers H, Karst H: Stress-induced changes in hippocampal function. Prog Brain Res. 2008, 167: 3-15.PubMed
43.
Espinosa-Oliva AM, de Pablos RM, Villarán RF, Arguelles S, Venero JL, Machado A, Cano J: Stress is critical for LPS-induced activation of microglia and damage in the rat hippocampus. Neurobiol Aging. 2011, 32: 85-102. 10.1016/j.neurobiolaging.2009.01.012.PubMed
44.
de Pablos RM, Villaran RF, Argüelles S, Herrera AJ, Venero JL, Ayala A, Cano J, Machado A: Stress increases vulnerability to inflammation in the rat prefrontal cortex. J Neurosci. 2006, 26: 5709-5719. 10.1523/JNEUROSCI.0802-06.2006.PubMed
45.
Paxinos G, Watson C: The Rat Brain in Stereotaxic Coordinates. 1986, London: Academic Press
46.
Gamaro GD, Manoli P, Torres IL, Silveira R, Dalmaz C: Effects of chronic variate stress on feeding behavior and on monoamine levels in different rat brain structures. Neurochem Int. 2003, 42: 107-114. 10.1016/S0197-0186(02)00080-3.PubMed
47.
Konarska M, Stewart RE, McCarty R: Predictability of chronic intermittent stress: effects on sympathetic-adrenal medullary responses of laboratory rats. Behav Neural Biol. 1990, 53: 231-243. 10.1016/0163-1047(90)90458-I.PubMed
48.
Murua VS, Molina VA: Effects of chronic variable stress and antidepressant drugs on behavioral inactivity during an uncontrollable stress: interaction between both treatments. Behav Neural Biol. 1992, 57: 87-89. 10.1016/0163-1047(92)90790-B.PubMed
49.
Muscat R, Papp M, Willner P: Reversal of stress-induced anhedonia by the atypical antidepressants, fluoxetine and maprotiline. Psychopharmacology (Berl). 1992, 109: 433-438. 10.1007/BF02247719.
50.
Papp M, Willner P, Muscat R: An animal model of anhedonia: attenuation of sucrose consumption and place preference conditioning by chronic unpredictable mild stress. Psychopharmacology (Berl). 1991, 104: 255-259. 10.1007/BF02244188.
51.
Willner P, Towell A, Sampson D, Sophokleous S, Muscat R: Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology (Berl). 1987, 93: 358-364.
52.
Gundersen HGJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Møller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sørensen FB, Vesterby A, West MJ: The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS. 1988, 96: 857-881. 10.1111/j.1699-0463.1988.tb00954.x.PubMed
53.
Meltzer JC, Sanders V, Grimm PC, Stern E, Rivier C, Lee S, Rennie SL, Gietz RD, Hole AK, Watson PH, Greenberg AH, Nance DM: Production of digoxigenin-labelled RNA probes and the detection of cytokine mRNA in rat spleen and brain by in situ hybridization. Brain Res Brain Res Protoc. 1998, 2: 339-351. 10.1016/S1385-299X(98)00010-5.PubMed
54.
Lee DY, Oh YJ, Jin BK: Thrombin-activated microglia contributes to death of dopaminergic neurons in rat mesencephalic cultures: dual roles of mitogen-activated protein kinase signaling pathways. Glia. 2005, 51: 98-110. 10.1002/glia.20190.PubMed
55.
Rostworowski M, Balasingam V, Chabot S, Owens T, Yong VW: Astrogliosis in the neonatal and adult murine brain post-trauma: elevation of inflammatory cytokines and the lack of requirement for endogenous interferon-γ. J Neurosci. 1997, 17: 3664-3674.PubMed
56.
Kim YW, Zhao RJ, Park SJ, Lee JR, Cho IJ, Yang CH, Kim SG, Kim SC: Anti-inflammatory effects of liquiritigenin as a consequence of the inhibition of NF-κB-dependent iNOS and pro-inflammatory cytokines production. Br J Pharmacol. 2008, 154: 165-173. 10.1038/bjp.2008.79.PubMedCentralPubMed
57.
Bland ST, Beckley JT, Watkins LR, Maier SF, Bilbo SD: Neonatal Escherichia coli infection alters glial, cytokine, and neuronal gene expression in response to acute amphetamine in adolescent rats. Neurosci Lett. 2010, 474: 52-57. 10.1016/j.neulet.2010.03.006.PubMedCentralPubMed
58.
Zhu J, Zhou Z, Liu Y, Zheng J: Fractalkine and CX3CR1 are involved in the migration of intravenously grafted human bone marrow stromal cells toward ischemic brain lesion in rats. Brain Res. 2009, 1287: 173-183.PubMed
59.
Fryer HJ, Davis GE, Manthorpe M, Varon S: Lowry protein assay using an automatic microtiter plate spectrophotometer. Anal Biochem. 1986, 153: 262-266. 10.1016/0003-2697(86)90090-4.PubMed
60.
Jiang ZY, Woollard AC, Wolff SP: Lipid hydroperoxide measurement by oxidation of Fe2+ in the presence of xylenol orange: comparison with the TBA assay and an iodometric method. Lipids. 1991, 26: 853-856. 10.1007/BF02536169.PubMed
61.
Tomás-Camardiel M, Venero JL, Herrera AJ, de Pablos RM, Pintor-Toro JA, Machado A, Cano J: Blood–brain barrier disruption highly induces aquaporin-4 mRNA and protein in perivascular and parenchymal astrocytes: protective effect by estradiol treatment in ovariectomized animals. J Neurosci Res. 2005, 80: 235-246. 10.1002/jnr.20443.PubMed
62.
Deshmane SL, Kremlev S, Amini S, Sawaya BE: Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res. 2009, 29: 313-326. 10.1089/jir.2008.0027.PubMedCentralPubMed
63.
Hickman SE, El Khoury J: Mechanisms of mononuclear phagocyte recruitment in Alzheimer’s disease. CNS Neurol Disord Drug Targets. 2010, 9: 168-173. 10.2174/187152710791011982.PubMedCentralPubMed
64.
Morimoto M, Morita N, Ozawa H, Yokoyama K, Kawata M: Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study. Neurosci Res. 1996, 26: 235-269. 10.1016/S0168-0102(96)01105-4.PubMed
65.
Venero JL, Burguillos MA, Brundin P, Joseph B: The executioners sing a new song: killer caspases activate microglia. Cell Death Differ. 2011, 18: 1679-1691. 10.1038/cdd.2011.107.PubMedCentralPubMed
66.
Lawson LJ, Perry VH, Dri P, Gordon S: Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience. 1990, 39: 151-170. 10.1016/0306-4522(90)90229-W.PubMed
67.
Smith LK, Jadavji NM, Colwell KL, Katrina Perehudoff S, Metz GA: Stress accelerates neural degeneration and exaggerates motor symptoms in a rat model of Parkinson’s disease. Eur J Neurosci. 2008, 27: 2133-2146. 10.1111/j.1460-9568.2008.06177.x.PubMed
68.
Burguillos MA, Deierborg T, Kavanagh E, Persson A, Hajji N, Garcia-Quintanilla A, Cano J, Brundin P, Englund E, Venero JL, Joseph B: Caspase signalling controls microglia activation and neurotoxicity. Nature. 2011, 472: 319-324. 10.1038/nature09788.PubMed
69.
Frank MG, Miguel ZD, Watkins L, Maier SF: Prior exposure to glucocorticoids sensitizes the neuroinflammatory and peripheral inflammatory responses to E. coli lipopolysaccharide. Brain Behav Immun. 2010, 24: 19-30. 10.1016/j.bbi.2009.07.008.PubMed
70.
Frank MG, Thompson BM, Watkins LR, Maier SF: Glucocorticoids mediate stress-induced priming of microglial pro-inflammatory responses. Brain Behav Immun. 2012, 26: 337-345. 10.1016/j.bbi.2011.10.005.PubMed
71.
Frank MG, Watkins LR, Maier SF: Stress- and glucocorticoid-induced priming of neuroinflammatory responses: potential mechanisms of stress-induced vulnerability to drugs of abuse. Brain Behav Immun. 2011, 25 (Suppl 1): S21-S28.PubMed
72.
Johnson JD, O’Connor KA, Deak T, Stark M, Watkins LR, Maier SF: Prior stressor exposure sensitizes LPS-induced cytokine production. Brain Behav Immun. 2002, 16: 461-476. 10.1006/brbi.2001.0638.PubMed
73.
Perry VH: The influence of systemic inflammation on inflammation in the brain: implications for chronic neurodegenerative disease. Brain Behav Immun. 2004, 18: 407-413. 10.1016/j.bbi.2004.01.004.PubMed
74.
Smyth GP, Stapleton PP, Freeman TA, Concannon EM, Mestre JR, Duff M, Maddali S, Daly JM: Glucocorticoid pretreatment induces cytokine overexpression and nuclear factor-κB activation in macrophages. J Surg Res. 2004, 116: 253-261. 10.1016/S0022-4804(03)00300-7.PubMed
75.
Sorrells SF, Sapolsky RM: An inflammatory review of glucocorticoid actions in the CNS. Brain Behav Immun. 2007, 21: 259-272. 10.1016/j.bbi.2006.11.006.PubMedCentralPubMed
76.
77.
Conductier G, Blondeau N, Guyon A, Nahon JL, Rovère C: The role of monocyte chemoattractant protein MCP1/CCL2 in neuroinflammatory diseases. J Neuroimmunol. 2010, 224: 93-100. 10.1016/j.jneuroim.2010.05.010.PubMed
78.
Barclay AN, Wright GJ, Brooke G, Brown MH: CD200 and membrane protein interactions in the control of myeloid cells. Trends Immunol. 2002, 23: 285-290. 10.1016/S1471-4906(02)02223-8.PubMed
79.
Hoek RM, Ruuls SR, Murphy CA, Wright GJ, Goddard R, Zurawski SM, Blom B, Homola ME, Streit WJ, Brown MH, Barclay AN, Sedgwick JD: Down-regulation of the macrophage lineage through interaction with OX2 (CD200). Science. 2000, 290: 1768-1771.PubMed
80.
Biber K, Neumann H, Inoue K, Boddeke HW: Neuronal ‘On’ and ‘Off’ signals control microglia. Trends Neurosci. 2007, 30: 596-602. 10.1016/j.tins.2007.08.007.PubMed
81.
Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, Huang D, Kidd G, Dombrowski S, Dutta R, Lee JC, Cook DN, Jung S, Lira SA, Littman DR, Ransohoff RM: Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci. 2006, 9: 917-924. 10.1038/nn1715.PubMed
82.
Sozzani S, Zhou D, Locati M, Rieppi M, Proost P, Magazin M, Vita N, van Damme J, Mantovani A: Receptors and transduction pathways for monocyte chemotactic protein-2 and monocyte chemotactic protein-3: Similarities and differences with MCP-1. J Immunol. 1994, 152: 3615-3622.PubMed
83.
Stamatovic SM, Keep RF, Kunkel SL, Andjelkovic AV: Potential role of MCP-1 in endothelial cell tight junction ‘opening’: signaling via Rho and Rho kinase. J Cell Sci. 2003, 116: 4615-4628. 10.1242/jcs.00755.PubMed
84.
Ataka K, Asakawa A, Nagaishi K, Kaimoto K, Sawada A, Hayakawa Y, Tatezawa R, Inui A, Fujimiya M: Bone marrow-derived microglia infiltrate into the paraventricular nucleus of chronic psychological stress-loaded mice. PLoS One. 2013, 8: e81744-10.1371/journal.pone.0081744.PubMedCentralPubMed
85.
Calvez J, Fromentin G, Nadkarni N, Darcel N, Even P, Tomé D, Ballet N, Chaumontet C: Inhibition of food intake induced by acute stress in rats is due to satiation effects. Physiol Behav. 2011, 104: 675-683. 10.1016/j.physbeh.2011.07.012.PubMed
86.
Nair A, Bonneau RH: Stress-induced elevation of glucocorticoids increases microglia proliferation through NMDA receptor activation. J Neuroimmunol. 2006, 171: 72-85. 10.1016/j.jneuroim.2005.09.012.PubMed
87.
Ros-Bernal F, Hunot S, Herrero MT, Parnadeau S, Corvol JC, Lu L, Alvarez-Fischer D, Carrillo-de Sauvage MA, Saurini F, Coussieu C, Kinugawa K, Prigent A, Höglinger G, Hamon M, Tronche F, Hirsch EC, Vyas S: 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.PubMedCentralPubMed
88.
Kim YM, Lee JY, Choi SH, Kim DG, Jahng JW: RU486 blocks fasting-induced decrease of neuronal nitric oxide synthase in the rat paraventricular nucleus. Brain Res. 2004, 1018: 221-226. 10.1016/j.brainres.2004.05.068.PubMed
89.
Mailliet F, Qi H, Rocher C, Spedding M, Svenningsson P, Jay TM: Protection of stress-induced impairment of hippocampal/prefrontal LTP through blockade of glucocorticoid receptors: implication of MEK signaling. Exp Neurol. 2008, 211: 593-596. 10.1016/j.expneurol.2008.02.030.PubMed
90.
Sharrett-Field L, Butler TR, Berry JN, Reynolds AR, Prendergast MA: Mifepristone pretreatment reduces ethanol withdrawal severity in vivo. Alcohol Clin Exp Res. 2013, 37: 1417-1423. 10.1111/acer.12093.PubMedCentralPubMed
91.
Ahima RS, Harlan RE: Charting of type II glucocorticoid receptor-like immunoreactivity in the rat central nervous system. Neuroscience. 1990, 39: 579-604. 10.1016/0306-4522(90)90244-X.PubMed
92.
Ahima RS, Tagoe CNB, Harlan RE: Type II corticosteroid receptor-like immunoreactivity in the rat cerebellar cortex: differential regulation by corticosterone. Neuroendocrinology. 1992, 55: 683-694. 10.1159/000126188.PubMed
93.
Maki BE, McIlroy WE: Influence of arousal and attention on the control of postural sway. J Vestib Res. 1996, 6: 53-59.PubMed
94.
Metz GA, Jadavji NM, Smith LK: Modulation of motor function by stress: a novel concept of the effects of stress on behavior. Eur J Neurosci. 2005, 22: 1190-1200. 10.1111/j.1460-9568.2005.04285.x.PubMed
95.
Metz GAS, Schwab ME, Welzl H: The effects of acute and chronic stress on motor and sensory performance in male Lewis rats. Physiol Behav. 2001, 72: 29-35. 10.1016/S0031-9384(00)00371-1.PubMed
96.
Charlett A, Dobbs RJ, Purkiss AG, Wright DJ, Peterson DW, Weller C, Dobbs SM: Cortisol is higher in parkinsonism and associated with gait deficit. Acta Neurol Scand. 1998, 97: 77-85.PubMed
97.
Kim ST, Choi JH, Chang JW, Kim SW, Hwang O: Immobilization stress causes increases in tetrahydrobiopterin, dopamine, and neuromelanin and oxidative damage in the nigrostriatal system. J Neurochem. 2005, 95: 89-98. 10.1111/j.1471-4159.2005.03342.x.PubMed
98.
Finlay JM, Zigmond MJ: The effects of stress on central dopaminergic neurons: possible clinical implications. Neurochem Res. 1997, 22: 1387-1394. 10.1023/A:1022075324164.PubMed
99.
Izzo E, Sanna PP, Koob GF: Impairment of dopaminergic system function after chronic treatment with corticotropin-releasing factor. Pharmacol Biochem Behav. 2005, 81: 701-708. 10.1016/j.pbb.2005.04.017.PubMed
100.
Pani L, Porcella A, Gessa GL: The role of stress in the pathophysiology of the dopaminergic system. Mol Psychiatry. 2000, 5: 14-21. 10.1038/sj.mp.4000589.PubMed
101.
Smith AD, Castro SL, Zigmond MJ: Stress-induced Parkinson’s disease: a working hypothesis. Physiol Behav. 2002, 77: 527-531. 10.1016/S0031-9384(02)00939-3.PubMed
102.
Zigmond MJ, Abercrombie ED, Berger TW, Grace AA, Stricker EM: Compensatory responses to partial loss of dopaminergic neurons: studies with 6-hydroxydopamine. Current Concepts in Parkinson’s Disease Research. Edited by: Schneider JS, Gupta M. 1993, Toronto: Hogrefe & Huber, 99-140.
103.
Stein-Behrens BA, Elliot EM, Miller CA, Schilling JW, Newcombe R, Sapolsky RM: Glucocorticoids exacerbate kainic acid-induced extracellular accumulation of excitatory amino acids in the rat hippocampus. J Neurochem. 1992, 58: 1730-1735. 10.1111/j.1471-4159.1992.tb10047.x.PubMed
Metadata
Title
Chronic stress enhances microglia activation and exacerbates death of nigral dopaminergic neurons under conditions of inflammation
Authors
Rocío M de Pablos
Antonio J Herrera
Ana M Espinosa-Oliva
Manuel Sarmiento
Mario F Muñoz
Alberto Machado
José L Venero
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2014
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/1742-2094-11-34

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