Nigral neurodegeneration triggered by striatal AdIL-1 administration can be exacerbated by systemic IL-1 expression

Journal of Neuroimmunology

Volumn 222, Issue 1-2, 2010, Pages 29-39

  Pott Godoy, María Clara ^a   Ferrari, Carina Cintia ^a   Pitossi, Fernando Juan ^a  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

Author keywords

Cytokine; Dexamethasone; Motor behaviour; Systemic inflammation

Indexed keywords

ADENOVIRUS VECTOR; ANTIINFLAMMATORY AGENT; CYTOKINE; DEXAMETHASONE; INTERLEUKIN 1; INTERLEUKIN 1BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE COURSE; DISEASE EXACERBATION; DOPAMINERGIC NERVE CELL; INFLAMMATION; MALE; MICROGLIA; MOTOR DYSFUNCTION; NERVE CELL DEGENERATION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STRIATONIGRAL DEGENERATION; SUBSTANTIA NIGRA;

ADENOVIRIDAE; ANIMALS; ANTI-INFLAMMATORY AGENTS; CORPUS STRIATUM; DEXAMETHASONE; DISEASE MODELS, ANIMAL; DOPAMINE; ENCEPHALITIS; GENETIC VECTORS; GLIOSIS; INTERLEUKIN-1BETA; MALE; MOVEMENT DISORDERS; NERVE DEGENERATION; NEURAL PATHWAYS; NEURONS; PARKINSONIAN DISORDERS; RATS; RATS, WISTAR; SUBSTANTIA NIGRA; TRANSFECTION; TREATMENT OUTCOME;

EID: 77952292246     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2010.02.018     Document Type: Article

References (82)

1. Arai H., Furuya T., Mizuno Y., Mochizuki H. Inflammation and infection in Parkinson's disease. Histol. Histopathol. 2006, 21(6):673-678.
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. 2003, 12(1):35-45.
3. Aubin L. Parkinson's disease. Soins 1998, 624:XVII-XVIII.
4. Block M.L., Hong J.S. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol. 2005, 76(2):77-98.
5. 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. 2002, 81(1):150-157.
6. Choi D.Y., Liu M., Hunter R.L., Cass W.A., Pandya J.D., Sullivan P.G., Shin E.J., Kim H.C., Gash D.M., Bing G. Striatal neuroinflammation promotes Parkinsonism in rats. PLoS One 2009, 4(5):e5482.
7. Cicchetti F., Brownell A.L., Williams K., Chen Y.I., 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(6):991-998.
8. De Lella Ezcurra A.L., Chertoff M., Ferrari C., Graciarena M., Pitossi F. Chronic expression of low levels of tumor necrosis factor-alpha in the substantia nigra elicits progressive neurodegeneration, delayed motor symptoms and microglia/macrophage activation. Neurobiol. Dis. 2009, 37(3):630-640.
9. Depino A.M., Earl C., Kaczmarczyk E., Ferrari C., Besedovsky H., del Rey A., Pitossi F.J., Oertel W.H. Microglial activation with atypical proinflammatory cytokine expression in a rat model of Parkinson's disease. Eur. J. Neurosci. 2003, 18(10):2731-2742.
10. Dinarello C.A. Interleukin-1. Cytokine Growth Factor Rev. 1997, 8(4):253-265.
11. 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. 2001, 98(25):14669-14674.
12. Epp L.M., Mravec B. Chronic polysystemic candidiasis as a possible contributor to onset of idiopathic Parkinson's disease. Bratisl. Lek. Listy 2006, 107(6-7):227-230.
13. 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(2):295-312.
14. Ferrari C.C., Depino A.M., Prada F., Muraro N., Campbell S., Podhajcer O., Perry V.H., Anthony D.C., Pitossi F.J. Reversible demyelination, blood-brain barrier breakdown, and pronounced neutrophil recruitment induced by chronic IL-1 expression in the brain. Am. J. Pathol. 2004, 165(5):1827-1837.
15. Ferrari C.C., Pott Godoy M.C., Tarelli R., Chertoff M., Depino A.M., Pitossi F.J. Progressive neurodegeneration and motor disabilities induced by chronic expression of IL-1beta in the substantia nigra. Neurobiol. Dis. 2006, 24(1):183-193.
16. Frank-Cannon T.C., Alto L.T., McAlpine F.E., Tansey M.G. Does neuroinflammation fan the flame in neurodegenerative diseases?. Mol. Neurodegener. 2009, 4:47.
17. Gao H.M., Hong J.S., Zhang W., Liu B. Distinct role for microglia in rotenone-induced degeneration of dopaminergic neurons. J. Neurosci. 2002, 22(3):782-790.
18. Gao H.M., Hong J.S., Zhang W., Liu B. Synergistic dopaminergic neurotoxicity of the pesticide rotenone and inflammogen lipopolysaccharide: relevance to the etiology of Parkinson's disease. J. Neurosci. 2003, 23(4):1228-1236.
19. Gao H.M., Liu B., Zhang W., Hong J.S. Novel anti-inflammatory therapy for Parkinson's disease. Trends Pharmacol. Sci. 2003, 24(8):395-401.
20. Godoy M.C., Tarelli R., Ferrari C.C., Sarchi M.I., Pitossi F.J. Central and systemic IL-1 exacerbates neurodegeneration and motor symptoms in a model of Parkinson's disease. Brain 2008, 131(Pt 7):1880-1894.
21. Hald A., Lotharius J. Oxidative stress and inflammation in Parkinson's disease: is there a causal link?. Exp. Neurol. 2005, 193(2):279-290.
22. He Y., Appel S., Le W. Minocycline inhibits microglial activation and protects nigral cells after 6-hydroxydopamine injection into mouse striatum. Brain Res. 2001, 909(1-2):187-193.
23. Herrera A.J., Tomas-Camardiel M., Venero J.L., Cano J., Machado A. Inflammatory process as a determinant factor for the degeneration of substantia nigra dopaminergic neurons. J. Neural. Transm. 2005, 112(1):111-119.
24. Hirsch E.C., Hunot S. Neuroinflammation in Parkinson's disease: a target for neuroprotection?. Lancet Neurol. 2009, 8(4):382-397.
25. 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. 2003, 991:214-228.
26. Hirsch E.C., Hunot S., Hartmann A. Neuroinflammatory processes in Parkinson's disease. Parkinsonism Relat. Disord. 2005, 11(Suppl 1):S9-S15.
27. Hohlfeld R., Kerschensteiner M., Meinl E. Dual role of inflammation in CNS disease. Neurology 2007, 68:S58-S63. 22 Suppl 3, discussion S91-56.
28. 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. 1999, 19(9):3440-3447.
29. Isgreen W.P., Chutorian A.M., Fahn S. Sequential parkinsonism and chorea following "mild" influenza. Trans. Am. Neurol. Assoc. 1976, 101:56-60.
30. Jang H., Boltz D., Sturm-Ramirez K., Shepherd K.R., Jiao Y., Webster R., Smeyne R.J. Highly pathogenic H5N1 influenza virus can enter the central nervous system and induce neuroinflammation and neurodegeneration. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(33):14063-14068.
31. Kaur C., Ling E.A. Study of the transformation of amoeboid microglial cells into microglia labelled with the isolectin Griffonia simplicifolia in postnatal rats. Acta Anat. (Basel) 1991, 142(2):118-125.
32. Kiefer R., Kreutzberg G.W. Effects of dexamethasone on microglial activation in vivo: selective downregulation of major histocompatibility complex class II expression in regenerating facial nucleus. J. Neuroimmunol. 1991, 34(2-3):99-108.
33. Kim S.U., de Vellis J. Microglia in health and disease. J. Neurosci. Res. 2005, 81(3):302-313.
34. Kim Y.S., Joh T.H. Microglia, major player in the brain inflammation: their roles in the pathogenesis of Parkinson's disease. Exp. Mol. Med. 2006, 38(4):333-347.
35. Kimberlin D.W., Willis S.A., McCracken G.H., Nisen P.D. Protein synthesis-dependent induction of interleukin-1 beta by lipopolysaccharide is inhibited by dexamethasone via mRNA destabilization in human astroglial cells. J. Clin. Immunol. 1995, 15(4):199-204.
36. Kolb M., Margetts P.J., Anthony D.C., Pitossi F., Gauldie J. Transient expression of IL-1beta induces acute lung injury and chronic repair leading to pulmonary fibrosis. J. Clin. Invest. 2001, 107(12):1529-1536.
37. Koprich J.B., Reske-Nielsen C., Mithal P., Isacson O. Neuroinflammation mediated by IL-1beta increases susceptibility of dopamine neurons to degeneration in an animal model of Parkinson's disease. J. Neuroinflammation 2008, 5:8.
38. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 1996, 19(8):312-318.
39. Kurkowska-Jastrzebska I., Litwin T., Joniec I., Ciesielska A., Przybylkowski A., Czlonkowski A., Czlonkowska A. Dexamethasone protects against dopaminergic neurons damage in a mouse model of Parkinson's disease. Int. Immunopharmacol. 2004, 4(10-11):1307-1318.
40. Lee J.K., Tran T., Tansey M.G. Neuroinflammation in Parkinson's disease. J. Neuroimmune Pharmacol. 2009, 4(4):419-429.
41. Lees A.J., Hardy J., Revesz T. Parkinson's disease. Lancet 2009, 373(9680):2055-2066.
42. Long-Smith C.M., Sullivan A.M., Nolan Y.M. The influence of microglia on the pathogenesis of Parkinson's disease. Prog. Neurobiol. 2009, 89(3):277-287.
43. Marttila R.J., Rinne U.K. Arteriosclerosis, heredity, and some previous infections in the etiology of Parkinson's disease. A case-control study. Clin. Neurol. Neurosurg. 1976, 79(1):46-56.
44. McColl B.W., Rothwell N.J., Allan S.M. Systemic inflammatory stimulus potentiates the acute phase and CXC chemokine responses to experimental stroke and exacerbates brain damage via interleukin-1- and neutrophil-dependent mechanisms. J. Neurosci. 2007, 27(16):4403-4412.
45. McColl B.W., Rothwell N.J., Allan S.M. Systemic inflammation alters the kinetics of cerebrovascular tight junction disruption after experimental stroke in mice. J. Neurosci. 2008, 28(38):9451-9462.
46. McGeer E.G., McGeer P.L. The role of anti-inflammatory agents in Parkinson's disease. CNS Drugs 2007, 21(10):789-797.
47. McGeer P.L., McGeer E.G. Glial reactions in Parkinson's disease. Mov. Disord. 2008, 23(4):474-483.
48. McGeer P.L., Itagaki S., Akiyama H., McGeer E.G. Rate of cell death in parkinsonism indicates active neuropathological process. Ann. Neurol. 1988, 24(4):574-576.
49. McGeer P.L., Yasojima K., McGeer E.G. Association of interleukin-1 beta polymorphisms with idiopathic Parkinson's disease. Neurosci. Lett. 2002, 326(1):67-69.
50. McGeer P.L., Schwab C., Parent A., Doudet D. Presence of reactive microglia in monkey substantia nigra years after 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine administration. Ann. Neurol. 2003, 54(5):599-604.
51. Minghetti L. Role of inflammation in neurodegenerative diseases. Curr. Opin. Neurol. 2005, 18(3):315-321.
52. Mogi M., Nagatsu T. Neurotrophins and cytokines in Parkinson's disease. Adv. Neurol. 1999, 80:135-139.
53. Mogi M., Harada M., Kondo T., Riederer P., Inagaki H., Minami M., Nagatsu T. Interleukin-1 beta, interleukin-6, epidermal growth factor and transforming growth factor-alpha are elevated in the brain from parkinsonian patients. Neurosci. Lett. 1994, 180(2):147-150.
54. Muller T., Blum-Degen D., Przuntek H., Kuhn W. Interleukin-6 levels in cerebrospinal fluid inversely correlate to severity of Parkinson's disease. Acta Neurol. Scand. 1998, 98(2):142-144.
55. Nagatsu T., Sawada M. Inflammatory process in Parkinson's disease: role for cytokines. Curr. Pharm. Des. 2005, 11(8):999-1016.
56. Nagatsu T., Mogi M., Ichinose H., Togari A. Cytokines in Parkinson's disease. J. Neural. Transm. Suppl. 2000, (58):143-151.
57. Orr C.F., Rowe D.B., Halliday G.M. An inflammatory review of Parkinson's disease. Prog. Neurobiol. 2002, 68(5):325-340.
58. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1986, Academic Press, Orlando, FL.
59. Perry V.H. The influence of systemic inflammation on inflammation in the brain: implications for chronic neurodegenerative disease. Brain Behav. Immun. 2004, 18(5):407-413.
60. Perry V.H., Cunningham C., Holmes C. Systemic infections and inflammation affect chronic neurodegeneration. Nat. Rev. Immunol. 2007, 7(2):161-167.
61. Qin L., Wu X., Block M.L., Liu Y., Breese G.R., Hong J.S., Knapp D.J., Crews F.T. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 2007, 55(5):453-462.
62. Ravenholt R.T., Foege W.H. 1918 influenza, encephalitis lethargica, parkinsonism. Lancet 1982, 2(8303):860-864.
63. Reale M., Iarlori C., Thomas A., Gambi D., Perfetti B., Di Nicola M., Onofrj M. Peripheral cytokines profile in Parkinson's disease. Brain Behav. Immun. 2009, 23(1):55-63.
64. Sairam K., Saravanan K.S., Banerjee R., Mohanakumar K.P. Non-steroidal anti-inflammatory drug sodium salicylate, but not diclofenac or celecoxib, protects against 1-methyl-4-phenyl pyridinium-induced dopaminergic neurotoxicity in rats. Brain Res. 2003, 966(2):245-252.
65. Sanchez-Pernaute R., Ferree A., Cooper O., Yu M., Brownell A.L., Isacson O. Selective COX-2 inhibition prevents progressive dopamine neuron degeneration in a rat model of Parkinson's disease. J. Neuroinflammation 2004, 1(1):6.
66. Sauer H., Oertel W.H. Progressive degeneration of nigrostriatal dopamine neurons following intrastriatal terminal lesions with 6-hydroxydopamine: a combined retrograde tracing and immunocytochemical study in the rat. Neuroscience 1994, 59(2):401-415.
67. Saura J., Pares M., Bove J., Pezzi S., Alberch J., Marin C., Tolosa E., Marti M.J. Intranigral infusion of interleukin-1beta activates astrocytes and protects from subsequent 6-hydroxydopamine neurotoxicity. J. Neurochem. 2003, 85(3):651-661.
68. Sawada M., Imamura K., Nagatsu T. Role of cytokines in inflammatory process in Parkinson's disease. J. Neural. Transm. Suppl. 2006, (70):373-381.
69. Schallert T., Jones T.A. "Exuberant" neuronal growth after brain damage in adult rats: the essential role of behavioral experience. J. Neural. Transplant. Plast. 1993, 4(3):193-198.
70. Schwab C., Klegeris A., McGeer P.L. Inflammation in transgenic mouse models of neurodegenerative disorders. Biochim. Biophys. Acta 2009, (Oct. 31).
71. Shaftel S.S., Carlson T.J., Olschowka J.A., Kyrkanides S., Matousek S.B., O'Banion M.K. Chronic interleukin-1beta expression in mouse brain leads to leukocyte infiltration and neutrophil-independent blood brain barrier permeability without overt neurodegeneration. J. Neurosci. 2007, 27(35):9301-9309.
72. Spencer S.J., Mouihate A., Pittman Q.J. Peripheral inflammation exacerbates damage after global ischemia independently of temperature and acute brain inflammation. Stroke 2007, 38(5):1570-1577.
73. Takahashi M., Yamada T. Viral etiology for Parkinson's disease-a possible role of influenza A virus infection. Jpn. J. Infect. Dis. 1999, 52(3):89-98.
74. Tansey M.G., Goldberg M.S. Neuroinflammation in Parkinson's disease: its role in neuronal death and implications for therapeutic intervention. Neurobiol. Dis. 2009, 37(3):510-518.
75. Teismann P., Schulz J.B. Cellular pathology of Parkinson's disease: astrocytes, microglia and inflammation. Cell Tissue Res. 2004, 318(1):149-161.
76. Teismann P., Tieu K., Choi D.K., Wu D.C., Naini A., Hunot S., Vila M., Jackson-Lewis V., Przedborski S. Cyclooxygenase-2 is instrumental in Parkinson's disease neurodegeneration. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(9):5473-5478.
77. Teismann P., Vila M., Choi D.K., Tieu K., Wu D.C., Jackson-Lewis V., Przedborski S. COX-2 and neurodegeneration in Parkinson's disease. Ann. N. Y. Acad. Sci. 2003, 991:272-277.
78. Unlap T., Jope R.S. Diurnal variation in kainate-induced AP-1 activation in rat brain: influence of glucocorticoids. Brain Res. Mol. Brain Res. 1995, 28(2):193-200.
79. Vazquez-Claverie M., Garrido-Gil P., San Sebastian W., Izal-Azcarate A., Belzunegui S., Marcilla I., Lopez B., Luquin M.R. Acute and chronic 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine administrations elicit similar microglial activation in the substantia nigra of monkeys. J. Neuropathol. Exp. Neurol. 2009, 68(9):977-984.
80. Vila M., Jackson-Lewis V., Guegan C., Wu D.C., Teismann P., Choi D.K., Tieu K., Przedborski S. The role of glial cells in Parkinson's disease. Curr. Opin. Neurol. 2001, 14(4):483-489.
81. Whitton P.S. Inflammation as a causative factor in the aetiology of Parkinson's disease. Br. J. Pharmacol. 2007, 150(8):963-976.
82. 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. 2002, 22(5):1763-1771.