Minocycline reduces the lipopolysaccharide-induced inflammatory reaction, peroxynitrite-mediated nitration of proteins, disruption of the blood-brain barrier, and damage in the nigral dopaminergic system

Neurobiology of Disease

Volumn 16, Issue 1, 2004, Pages 190-201

  Tomás Camardiel, Mayka ^a   Rite, Inmaculada ^a   Herrera, Antonio J ^a   De Pablos, Rocio M ^a   Cano, Josefina ^a   Machado, Alberto ^a   Venero, José L ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

Author keywords

3 nitrotyrosine; 3 NT; BBB; blood brain barrier; DA; dopamine; Dopaminergic system; GFAP; glial fibrillary acidic protein; IL; inducible nitric oxide synthase; iNOS; interleukin; lipopolysaccharide; LPS; Microglia; Parkinson's disease; Peroxynitrites; Substantia nigra

Indexed keywords

3 NITROTYROSINE; IMMUNOGLOBULIN G; INTERLEUKIN 1ALPHA; LIPOPOLYSACCHARIDE; MESSENGER RNA; MINOCYCLINE; NEUROPROTECTIVE AGENT; PEROXYNITRITE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; CELL DEATH; CELL PROTECTION; CONTROLLED STUDY; CORRELATION ANALYSIS; DOPAMINERGIC SYSTEM; DRUG EFFICACY; DRUG SCREENING; FEMALE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFLAMMATION; MESENCEPHALON; MICROGLIA; NERVE DEGENERATION; NEUROPROTECTION; NITRATION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUBSTANTIA NIGRA;

ANIMALS; BLOOD-BRAIN BARRIER; DOPAMINE; FEMALE; INFLAMMATION; LIPOPOLYSACCHARIDES; MINOCYCLINE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; PEROXYNITROUS ACID; RATS; RATS, WISTAR; SUBSTANTIA NIGRA;

EID: 2342538502     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2004.01.010     Document Type: Article

References (78)

1. Amin A.R., Attur M.G., Thakker G.D., Patel P.D., Vyas P.R., Patel R.N., Patel I.R., Abramson S.B. A novel mechanism of action of tetracyclines: effects on nitric oxide synthases. Proc. Natl. Acad. Sci. U. S. A. 93:1996;14014-14019
2. Arimoto T., Bing G. Up-regulation of inducible nitric oxide synthase in the substantia nigra by lipopolysaccharide causes microglial activation and neurodegeneration. Neurobiol. Dis. 12:2003;35-45
3. Arvin K.L., Han B.H., Du Y., Lin S.Z., Paul S.M., Holtzman D.M. Minocycline markedly protects the neonatal brain against hypoxic-ischemic injury. Ann. Neurol. 52:2002;54-61
4. Ayata C., Ropper A.H. Ischaemic brain oedema. J. Clin. Neurosci. 9:2002;113-124
5. Beal M.F. Mitochondrial dysfunction in neurodegenerative diseases. Biochim. Biophys. Acta. 1366:1998;211-223
6. Beal M.F. Mitochondria, oxidative damage, and inflammation in Parkinson's disease. Ann. N. Y. Acad. Sci. 991:2003;120-131
7. Bessler H., Mendel C., Straussberg R., Gurary N., Aloni D., Sirota L. Effects of dexamethasone on IL-1beta, IL-6, and TNF-alpha production by mononuclear cells of newborns and adults. Biol. Neonate. 75:1999;225-233
8. Blum-Degen D., Muller T., Kuhn W., Gerlach M., Przuntek H., Riederer P. Interleukin-1 beta and interleukin-6 are elevated in the cerebrospinal fluid of Alzheimer's and de novo Parkinson's disease patients. Neurosci. Lett. 202:1995;17-20
9. Boka G., Anglade P., Wallach D., Javoy-Agid F., Agid Y., Hirsch E.C. Immunocytochemical analysis of tumor necrosis factor and its receptors in Parkinson's disease. Neurosci. Lett. 172:1994;151-154
10. Calingasan N.Y., Park L.C., Calo L.L., Trifiletti R.R., Gandy S.E., Gibson G.E. Induction of nitric oxide synthase and microglial responses precede selective cell death induced by chronic impairment of oxidative metabolism. Am. J. Pathol. 153:1998;599-610
11. Carreño-Müller E., Herrera A.J., de Pablos R.M., Tomás-Camardiel M., Venero J.L., Cano J., Machado A. Thrombin induces in vivo degeneration of nigral dopaminergic neurons along with the activation of microglia. J. Neurochem. 84:2003;1201-1214
12. Cassarino D.S., Bennett J.P. Jr. An evaluation of the role of mitochondria in neurodegenerative diseases: mitochondrial mutations and oxidative pathology, protective nuclear responses, and cell death in neurodegeneration. Brain Res. Rev. 29:1999;1-25
13. Castano A., Herrera A.J., Cano J., Machado A. Lipopolysaccharide intranigral injection induces inflammatory reaction and damage in nigrostriatal dopaminergic system. J. Neurochem. 70:1998;1584-1592
14. Castano A., Herrera A.J., 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-alpha, IL-1beta and IFN-gamma. J. Neurochem. 81:2002;150-157
15. Chen M., Ona V.O., Li M., Ferrante R.J., Fink K.B., Zhu S., Bian J., Guo L., Farrell L.A., Hersch S.M., Hobbs W., Vonsattel J.P., Cha J.H., Friedlander R.M. Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat. Med. 6:2000;797-801
16. Czlonkowska A., Kurkowska-Jastrzebska I., Czlonkowski A., Peter D., Stefano G. Immune processes in the pathogenesis of Parkinson's disease D a potential role for microglia and nitric oxide. Med. Sci. Monit. 8:2002;165-177
17. 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., Luecke S., Phebus L.A., Bymaster F.P., Paul S.M. Minocycline prevents nigrostriatal dopaminergic neurodegeneration in the MPTP model of Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 98:2001;14669-14674
18. Fornstedt B., Pileblad E., Carlsson A. In vivo autoxidation of dopamine in guinea pig striatum increases with age. J. Neurochem. 55:1990;655-659
19. Gao H.M., Jiang J., Wilson B., Zhang W., Hong J.S., Liu B. Microglial activation-mediated delayed and progressive degeneration of rat nigral dopaminergic neurons: relevance to Parkinson's disease. J. Neurochem. 81:2002;1285-1297
20. Gayle D.A., Ling Z., Tong C., Landers T., Lipton J.W., Carvey P.M. Lipopolysaccharide (LPS)-induced dopamine cell loss in culture: roles of tumor necrosis factor-alpha, interleukin-1beta, and nitric oxide. Brain Res. Dev. Brain Res. 133:2002;27-35
21. Gingrich M.B., Traynelis S.F. Serine proteases and brain damage - Is there a link? Trends Neurosci. 23:2000;399-407
22. Golub L.M., Lee H.M., Ryan M.E., Giannobile W.V., Payne J., Sorsa T. Tetracyclines inhibit connective tissue breakdown by multiple non-antimicrobial mechanisms. Adv. Dent. Res. 12:1998;12-26
23. Graham D.G. Oxidative pathways for catecholamines in the genesis of neuromelanin and cytotoxic quinones. Mol. Pharmacol. 14:1978;633-643
24. Gundersen H.G.J., Bagger P., Bendtsen T.F., Evans S.M., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., Pakkenberg B., Sorensen F.B., Vesterby A., West M.J. The new stereological tools: dissector, fractionator, nucleator, and point sampled intercepts and their use in pathological research and diagnosis. Acta Pathol., Microbiol. Immunol. Scand. 96:1988;857-881
25. Hasegawa Y., Inagaki T., Sawada M., Suzumura A. Impaired cytokine production by peripheral blood mononuclear cells and monocytes/macrophages in Parkinson's disease. Acta Neurol. Scand. 101:2000;159-164
26. Hastings T.G. Enzymatic oxidation of dopamine: the role of prostaglandin H synthase. J. Neurochem. 64:1995;919-924
27. He Y., Appel S., Le W. Minocycline inhibits microglial activation and protects nigral cells after 6-hydroxydopamine injection into mouse striatum. Brain Res. 909:2001;187-193
28. Heikkila R., Cohen G. Further studies on the generation of hydrogen peroxide by 6-hydroxydopamine. Potentiation by ascorbic acid. Mol. Pharmacol. 8:1972;241-248
29. Herrera A.J., Castano A., Venero J.L., 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. 7:2000;429-447
30. Hirafuji M., Tsunoda M., Machida T., Hamaue N., Endo T., Miyamoto A., Minami M. Reduced expressions of inducible nitric oxide synthase and cyclooxygenase-2 in vascular smooth muscle cells of stroke-prone spontaneously hypertensive rats. Life Sci. 70:2002;917-926
31. Hirsch E.C., Breidert T., Rousselet E., Hunot S., Hartmann A., Michel P.P. The role of glial reaction and inflammation in Parkinson's disease. Ann. N. Y. Acad. Sci. 991:2003;214-228
32. Holst O., Ulmer A.J., Brade H., Flad H.D., Rietschel E.T. Biochemistry and cell biology of bacterial endotoxins. FEMS Immunol. Med. Microbiol. 16:1996;83-104
33. Hunot S., Dugas N., Faucheux B., Hartmann A., Tardieu M., Debre P., Agid Y., Dugas B., Hirsch E.C. FcepsilonRII/CD23 is expressed in Parkinson's disease and induces, in vitro, production of nitric oxide and tumor necrosis factor-alpha in glial cells. J. Neurosci. 19:1999;3440-3447
34. Iravani M.M., Kashefi K., Mander P., Rose S., Jenner P. Involvement of inducible nitric oxide synthase in inflammation-induced dopaminergic neurodegeneration. Neuroscience. 110:2002;49-58
35. Jenner P. Oxidative stress in Parkinson's disease. Ann. Neurol. 53(Suppl. 3):2003;S26-S36
36. Jenner P., Olanow C.W. Oxidative stress and the pathogenesis of Parkinson's disease. Neurology. 47(Suppl. 3):1996;S161-S170
37. Jeohn G.H., Cooper C.L., Wilson B., Chang R.C., Jang K.J., Kim H.C., Liu B., Hong J.S. p38 MAP kinase is involved in lipopolysaccharide-induced dopaminergic neuronal cell death in rat mesencephalic neuron-glia cultures. Ann. N. Y. Acad. Sci. 62:2002;332-346
38. Kielian T.L., Blecha F. CD14 and other recognition molecules for lipopolysaccharide: a review. Immunopharmacology. 29:1995;187-205
39. Kim W.G., Mohney R.P., Wilson B., Jeohn G.H., Liu B., Hong J.S. Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J. Neurosci. 20:2000;6309-6316
40. Koutsilieri E., Scheller C., Grunblatt E., Nara K., Li J., Riederer P. Free radicals in Parkinson's disease. J. Neurol. (Suppl. 2):2002;II1-II5
41. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19:1996;312-318
42. Lawson L.J., Perry V.H., Dri P., Gordon S. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience. 39:1990;151-170
43. Liu B., Hong J.S. Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention. J. Pharmacol. Exp. Ther. 304:2003;1-7
44. Liu D., Smith C.L., Barone F.C., Ellison J.A., Lysko P.G., Li K., Simpson I.A. Astrocytic demise precedes delayed neuronal death in focal ischemic rat brain. Mol. Brain Res. 68:1999;29-41
45. Liu B., Du L., Hong J.S. Naloxone protects rat dopaminergic neurons against inflammatory damage through inhibition of microglia activation and superoxide generation. J. Pharmacol. Exp. Ther. 293:2000;607-617
46. Liu B., Jiang J.W., Wilson B.C., Du L., Yang S.N., Wang J.Y., Wu G.C., Cao X.D., Hong J.S. Systemic infusion of naloxone reduces degeneration of rat substantia nigral dopaminergic neurons induced by intranigral injection of lipopolysaccharide. J. Pharmacol. Exp. Ther. 295:2000;125-132
47. Liu B., Qin L., Yang S.N., Wilson B.C., Liu Y., Hong J.S. Femtomolar concentrations of dynorphins protect rat mesencephalic dopaminergic neurons against inflammatory damage. J. Pharmacol. Exp. Ther. 298:2001;1133-1141
48. Liu Y., Qin L., Li G., Zhang W., An L., Liu B., Hong J.S. Dextromethorphan protects dopaminergic neurons against inflammation-mediated degeneration through inhibition of microglial activation. J. Pharmacol. Exp. Ther. 305:2003;212-218
49. Lu X., Bing G., Hagg T. Naloxone prevents microglia-induced degeneration of dopaminergic substantia nigra neurons in adult rats. Neuroscience. 97:2000;285-291
50. McGeer P.L., McGeer E.G. The inflammatory response system of brain: implications for therapy of Alzheimer and other neurodegenerative diseases. Brain Res. Rev. 21:1995;195-218
51. Meltzer J.C., Sanders V., Grimm P.C., Stern E., Rivier C., Lee S., Rennie S.L., Gietz R.D., Hole A.K., Watson P.H., Greenberg A.H., Nance D.M. Production of digoxigenin-labelled RNA probes and the detection of cytokine mRNA in rat spleen and brain by in situ hybridization. Brain Res. Protoc. 2:1998;339-351
52. Mogi M., Harada M., Narabayashi H., Inagaki H., Minami M., Nagatsu T. 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. 211:1996;13-16
53. Nedergaard M., Ramson B., Goldman S.A. New roles for astrocytes: Redefining the functional architecture of the brain. Trends Neurosci. 10:2003;523-530
54. Nicklas W.J., Vyas I., Heikkila R.E. Inhibition of NADH-linked oxidation in brain mitochondria by 1-methyl-4-phenyl-pyridine, a metabolite of the neurotoxin, 1-methyl-4-phenyl-1, 2, 5, 6-tetrahydropyridine. Life Sci. 36:1985;2503-2508
55. Obeso J.A., Rodriguez-Oroz M.C., Rodriguez M., Lanciego J.L., Artieda J., Gonzalo N., Olanow C.W. Pathophysiology of the basal ganglia in Parkinson's disease. Trends Neurosci. 23(Suppl. 10):2000;S8-S19
56. O'Neil M.J. Merck Man. Diagn. Ther. seventeenth ed. 1999;2833 Merck, Whitehouse Station, NJ
57. Orr C.F., Rowe D.B., Halliday G.M. An inflammatory review of Parkinson's disease. Prog. Neurobiol. 68:2002;325-340
58. Papadopoulos M.C., Saadoun S., Davies D.C., Bell B.A. Emerging molecular mechanisms of brain tumour oedema. Br. J. Neurosurg. 15:2001;101-108. (Review)
59. Paxinos G., Watson C. The rat brain in stereotaxic coordinates. Coordinates. 1986;Academic Press, London
60. Popovic N., Schubart A., Goetz B.D., Zhang S.C., Linington C., Duncan I.D. Inhibition of autoimmune encephalomyelitis by a tetracycline. Ann. Neurol. 51:2002;215-223
61. Ransom B., Behar T., Nedergaard M. New roles for astrocytes (stars at last). Trends Neurosci. 10:2003;520-522
62. Rifkin B.R., Vernillo A.T., Golub L.M., Ramamurthy N.S. Modulation of bone resorption by tetracyclines. Ann. N. Y. Acad. Sci. 732:1994;165-180
63. Rostworowski M., Balasingam V., Chabot S., Owens T., Yong V.W. Astrogliosis in the neonatal and adult murine brain post-trauma: elevation of inflammatory cytokines and the lack of requirement for endogenous interferon-gamma. J. Neurosci. 17:1997;3664-3674
64. Sánchez-Mejia R.O., Ona V.O., Li M., Friedlander R.M. Minocycline reduces traumatic brain injury-mediated caspase-1 activation, tissue damage, and neurological dysfunction. Neurosurgery. 48:2001;1393-1399
65. Schmidt-Kastner R., Meller D., Bellander B.M., Stromberg I., Olson L., Ingvar M. A one-step immunohistochemical method for detection of blood-brain barrier disturbances for immunoglobulins in lesioned rat brain with special reference to false-positive labelling in immunohistochemistry. J. Neurosci. Methods. 46:1993;121-132
66. Shukla A., Dikshit M., Srimal R.C. Nitric oxide modulates blood-brain barrier permeability during infections with an inactivated bacterium. NeuroReport. 6:1995;1629-1632
67. Stern E.L., Quan N., Proescholdt M.G., Herkenham M. Spatiotemporal induction patterns of cytokine and related immune signal molecule mRNAs in response to intrastriatal injection of lipopolysaccharide. J. Neuroimmunol. 109:2000;245-260
68. Streit W.J. Microglial response to brain injury: a brief synopsis. Toxicol. Pathol. 28:2000;28-30
69. Tikka T., Fiebich B.L., Goldsteins G., Keinanen R., Koistinaho J. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J. Neurosci. 21:2001;2580-2588
70. Torreilles F., Salman-Tabcheh S., Guerin M., Torreilles J. Neurodegenerative disorders: the role of peroxynitrite. Brain Res. Rev. 30:1999;153-163
71. Wang C.X., Yang T., Noor R., Shuaib A. Delayed minocycline but not delayed mild hypothermia protects embolic stroke. BMC Neurol. 2:2002;2
72. Warner T.T., Schapira A.H. Genetic and environmental factors in the cause of Parkinson's disease. Ann. Neurol. 53(Suppl. 3):2003;S16-S23
73. Wu D.C., Jackson-Lewis V., Vila M., Tieu K., Teismann P., Vadseth C., Choi D.K., Ischiropoulos H., Przedborski S. Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine mouse model of Parkinson disease. J. Neurosci. 22:2002;1763-1771
74. Wullner U., Klockgether T. Inflammation in Parkinson's disease. J. Neurol. 250(Suppl. 1):2003;I35-I38
75. Yrjanheikki J., Keinanen R., Pellikka M., Hokfelt T., Koistinaho J. Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc. Natl. Acad. Sci. U. S. A. 95:1998;15769-15774
76. Yrjanheikki J., Tikka T., Keinanen R., Goldsteins G., Chan P.H., Koistinaho J. A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc. Natl. Acad. Sci. U. S. A. 96:1999;13496-13500
77. Zhao X., Ahram A., Berman R.F., Muizelaar J.P., Lyeth B.G. Early loss of astrocytes after experimental traumatic brain injury. Glia. 44:2003;140-152
78. Zhu S., Stavrovskaya I.G., Drozda M., Kim B.Y., Ona V., Li M., Sarang S., Liu A.S., Hartley D.M., Wu du C., Gullans S., Ferrante R.J., Przedborski S., Kristal B.S., Friedlander R.M. Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature. 417:2002;74-78