Intranigral infusion of interleukin-1β activates astrocytes and protects from subsequent 6-hydroxydopamine neurotoxicity

Journal of Neurochemistry

Volumn 85, Issue 3, 2003, Pages 651-661

  Saura, Josep ^a,d   Parés, Mireia ^a   Bové, Jordi ^a   Pezzi, Susana ^b   Alberch, Jordi ^b   Marin, Concepció ^a   Tolosa, Eduardo ^a   Martí, María José ^a,c  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c HOSPITAL CLÍNIC   (Spain)

^d INST D INVESTIGACIONS B   (Spain)

Author keywords

6 hydroxydopamine; Astrocytes; Glial activation; Interleukin 1 ; Microglia; Parkinson's disease

Indexed keywords

AMPHETAMINE; CELL MARKER; GLIAL FIBRILLARY ACIDIC PROTEIN; HEAT SHOCK PROTEIN 25; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 47; INTERLEUKIN 1BETA; OXIDOPAMINE; PROTEIN OX42; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL ACTIVATION; CONTROLLED STUDY; DISEASE MARKER; DISEASE MODEL; DOPAMINERGIC NERVE CELL; GLIA CELL; IMMUNOHISTOCHEMISTRY; MALE; NEUROPROTECTION; NEUROTOXICITY; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; RAT STRAIN;

ANIMALIA;

EID: 0038335842     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.01676.x     Document Type: Article

References (57)

1. Anthony D. C., Bolton S. J., Fearn S. and Perry V. H. (1997) Age-related effects of interleukin-1β on polymorphonuclear neutrophil-dependent increases in blood-brain barrier permeability in rats. Brain 120, 435-444.
2. Ban E. M., Sarlieve L. L. and Haour F. G. (1993) Interleukin-1 binding sites on astrocytes. Neuroscience 52, 725-733.
3. Banati R. B., Daniel S. E. and Blunt S. B. (1988) Glial pathology but absence of apoptotic nigral neurons in long-standing Parkinsons's disease. Mov. Dis. 13, 221-227.
4. Barnéoud P., Parmentier S., Mazadier M., Miquet J. M., Boireau A., Dubédat P. and Blanchard J.-C. (1995) Effects of complete and partial lesions of the dopaminergic mesotelencephalic system on skilled forelimb use in the rat. Neuroscience 67, 837-848.
5. Barone F. C., White R. F., Spera P. A., Ellison J., Currie R. W., Wang X. and Feuerstein G. Z. (1998) Ischemic preconditioning and brain tolerance: temporal histological and fuctional outcomes, protein synthesis requirement, and interleukin-1 receptor antagonist and early gene expression. Stroke 29, 1937-1950.
6. Björklund A., Rosenblad C., Winkler C. and Kirik D. (1997) Studies on neuroprotective and regenerative effects of GDNF in a partial lesion model of Parkinson's disease. Neurobiol. Dis. 4, 186-200.
7. Bronstein D. M., Pérez-Otano I., Sun V., Mullis Sawin S. B., Chan J., Wu G.-C., Hudson P. M., Kong L.-Y., Hong J.-S. and McMillian M. K. (1995) Glia-dependent neurotoxicity and neuroprotection in mesencephalic cultures. Brain Res. 704, 112-116.
8. Busto R., Dietrich W. D., Globus M. Y. T., Valdés I., Scheinberg P. and Ginsberg M. D. (1987) Small differences in intraischemic brain temperature critically determine the extent of ischemic neuronal injury. J. Cereb. Blood Flow Metab. 7, 729-738.
9. Carman-Krzan M., Vige X. and Wise B. C. (1991) Regulation by interleukin-1 of nerve growth factor secretion and nerve growth factor mRNA expression in rat primary astroglial cultures. J. Neurochem. 56, 636-643.
10. Casamenti F., Prosperi C., Scali A., Giovannelli L., Colivicchi M. A., Faussone-Pellegrini M. S. and Pepeu G. (1999) Interleukin-1β activates forebrain glial cells and increases nitric oxide production and cortical glutamate and GABA release in vivo: implications for Alzheimer's disease. Neuroscience 91, 831-842.
11. Castaño A., Herrera A. J., Cano J. and Machado A. (1998) Lipopolysaccharide intranigral injection induces inflammatory reaction and damage in nigrostriatal dopaminergic system. J. Neurochem. 70, 1584-1592.
12. Connor B., Kozlowski D. A., Schallert T., Tillerson J. L., Davidson B. L. and Bohn M. C. (1999) Different effects of glial cell line-derived neurotrophic factor (GDNF) in the striatum and substantia nigra of the aged parkinsonian rat. Gene Ther. 6, 1936-1951.
13. Damier P., Hirsch E. C., Zhang P., Agid Y. and Javoy-Agid F. (1993) Glutathione peroxidase, glial cells and Parkinson's disease. Neuroscience 52, 1-6.
14. Davies C. A., Loddick S. A., Toulmond S., Stroemer R. P., Hunt J. and Rothwell N. J. (1999) The progression and topographic distribution of interleukin-1β expression after permanent middle cerebral artery occlusion in the rat. J. Cereb. Blood Flow Metab. 19, 87-98.
15. Engele J. and Bohm M. C. (1991) The neurotrophic effects of fibroblast growth factors on dopaminergic neurons in vitro are mediated by mesencephalic glia. J. Neurosci. 11, 3070-3078.
16. Giulian D., Baker T. J., Shih L. C. and Lachman L. B. (1986) Interleukin 1 of the central nervous system is produced by ameboid microglia. J. Exp. Med. 164, 594-604.
17. Giulian D., Woodward J., Young D. G., Krebs J. F. and Lachman L. B. (1988) Interleukin-1 injected into mammalian brain stimulates astrogliosis and neovascularization. J. Neurosci. 8, 2485-2490.
18. Hirsch E. C. (2000) Glial cells and Parkinson's disease. J. Neurol. 247, II/58-II/62.
19. Hirsch E. C., Hunot S., Damier P. and Faucheux B. (1998) Glial cells and inflammation in Parkinson's disease: a role in neurodegeneration? Ann. Neurol. 44, S115-S120.
20. Ho A. and Blum M. (1997) Regulation of astroglial-derived dopaminergic neurotrophic factors by interleukin-1 beta in the striatum of young and middle-aged mice. Exp. Neurol. 148, 348-359.
21. Hou J.-G. G., Cohen G. and Mytilineou C. (1997) Basic fibroblast growth factor stimulation of glial cells protects dopamine neurons from 6-hydroxydopamine toxicity: involvement of the glutathione sustem. J. Neurochem. 69, 76-38.
22. Kim W.-G., Mohney R. P., Wilson B., Jeohn G.-H., Liu B. and Hong J.-S. (2000) Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J. Neurosci. 20, 6309-6316.
23. Kirik D., Rosenblad C. and Björklund A. (1998) Characterization of behavioral and neurodegenerative changes following partial lesions of the nigrostriatal dopamine system induced by intrastriatal 6-hydroxydopamine in the rat. Exp. Neurol. 152, 259-277.
24. Kirik D., Rosenblad C. and Björklund A. (2000) Preservation of a functional nigrostriatal dopamine pathway by GDNF in the intrastriatal 6-OHDA lesion model depends on the site of administration of the trophic factor. Eur. J. Neurosci. 12, 3871-3882.
25. Kluger M. J. (1991) Fever: role of pyrogens and cryogens. Physiol. Rev. 71, 93-127.
26. Langston J. W., Forno L. S., Tetrud J., Reeves A. G., Kaplan J. A. and Karluk D. (1999) Evidence of active nerve cell death degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine exposure. Ann. Neurol. 46, 598-605.
27. Lawrence C. B., Allan S. M. and Rothwell N. J. Interleukin-1β and the interleukin-1 receptor antagonist act in the striatum to modify excitotoxic brain damage in the rat. Eur. J. Neurosci. 10, 1188-1195.
28. Lee S. C., Liu W., Dickson D. W., Brosnan C. F. and Berman J. W. (1993) Cytokine production by human fetal microglia and astrocytes. Differential induction by lipopolysaccharide and IL-1 beta. J. Immunol. 150, 2659-2667.
29. Liberatore G. T., Jackson-Lewis V., Vukosavic S., Mandir A. S., Vila M., McAuliffe W. G., Dawson V. L., Dawson T. M. and Przedborski S. (1999) Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson's disease. Nat. Med. 5, 1403-1409.
30. Loddick S. A. and Rothwell N. J. (1996) Neuroprotective effects of human recombinant interleukin-1 receptor antagonist in focal cerebral ischaemia in the rat. J. Cereb. Blood Flow Metab. 16, 932-940.
31. Liu B., Du L., Kong L.-Y., Hudson P. M., Wilson B. C., Chang R. C., Abel H. H. and Hong J.-S. (2000) Reduction by naloxone of lipopolysaccharide-induced neurotoxicity in mouse cortical neuron-glia co-cultures. Neuroscience 97, 749-756.
32. Mautes A. E., Kim D. H., Sharp F. R., Panter S., Sato M., Maida N., Bergeron M., Guenther K. and Nole L. J. (1998) Induction of heme-oxygenase-1 (HO-1) in the contused spinal cord of the rat. Brain Res. 795, 17-24.
33. McGeer P. L., Itagaki S., Boyes B. E. and McGeer E. G. (1988) Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's disease and Alzheimer's disease brains. Neurology 38, 1285-1291.
34. McMillian M. K., Vainio P. J. and Tuominen R. K. (1997) Role of protein kinase C in microglia-induced neurotoxicity in mesencephalic cultures. J. Neuropathol. Exp. Neurol. 56, 301-307.
35. Mirza B., Hadberg H., Thomsen P. and Moos T (2000) The absence of reactive astrocytosis is indicative of a unique inflammatory process in Parkinson's disease. Neuroscience 95, 425-432.
36. Moffett J., Kratz E., Myers J., Stachowiak E. K., Florkiewicz R. Z. and Stachowiak M. K. (1998) Transcriptional regulation of fibroblast growth factor-2 expression in human astrocytes: implications for cell plasticity. Mol. Biol. Cell 9, 2269-2285.
37. Mogi M. and Nagatsu T. (1999) Neurotrophins and cytokines in Parkinson's disease. Adv. Neurol. 80, 135-139.
38. O'Malley E. K., Sieber B. A., Black I. B. and Dreyfus C. F. (1992) Mesencephalic type I astrocytes mediate the survival of substantia nigra dopaminergic neurons in culture. Brain Res. 582, 65-70.
39. Ohtsuki T., Ruetzler C. A., Tasaki K. and Hallenbeck J. M. (1996) Interleukin-1 mediates induction of tolerance to global ischemia in gerbil hippocampal CA1 neurons. J. Cereb. Blood Flow Metab. 16, 1137-1142.
40. Olsson M., Nikkhah G., Bentlage C. and Björklund A. (1995) Forelimb akinesia in the rat Parkinson model: differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J. Neurosci. 15, 3863-3875.
41. Park T. H. and Mytilineou C. (1992) Protection from 1-methyl-4-phenylpyridinium (MPP+) toxicity and stimulation of regrowth of MPP(+)-damaged dopaminergic fibers by treatment of mesencephalic cultures with EGF and basic FGF. Brain Res. 599, 83-97.
42. Plata Salamán C. R., Peloso E. and Satinoff E. (1998) Interleukin-1β-induced fever in young and old Long-Evans rats. Am. J. Physiol. 275, R1633-R1638.
43. Rivera S., Gold S. J. and Gall C. M. (1994) Interleukin-1 beta increases basic fibroblast growth factor mRNA expression in adult rat brain and organotypic hippocampal cultures. Mol. Brain Res. 27, 12-26.
44. Sheng J. G., Ito K., Skinner R. D., Mrak R. E., Rovnaghi C. R., van Eldik L. J. and Griffin S. T. (1996) In vivo and in vitro evidence supporting a role for the inflammatory cytokine interleukin-1 as a driving force in Alzheimer's pathogenesis. Neurobiol. Aging 17 761-766.
45. Siegel G. J. and Chauham N. B. (2000) Neurotrophic factors in Alzheimer's and Parkinson's disease brain. Brain Res. Rev. 33, 199-227.
46. Singh I., Pahan K., Khan M, and Singh A. K. (1998) Cytokine-mediated induction of ceramide production is redox-sensitive. Implications to proinflammatory cytokine-mediated apoptosis in demyelinating diseases. J. Biol. Chem. 273, 20354-20362.
47. Sonti G., Ilyin S. E. and Plata-Salamán C. R. (1996) Anorexia induced by cytokine interactions at pathophysiological concentrations. Am. J. Physiol. 270, R1394-R1402.
48. Spina M. B. and Cohen G. (1989) Dopamine turnover and glutathione oxidation: implications for Parkinson disease. Proc. Natl Acad. Sci. USA 86, 1398-1400.
49. Stroemer R. P. and Rothwell N. J. (1998) Exacerbation of ischemic brain damage by localized striatal injection of interleukin-1β in the rat. J. Cereb. Blood Flow Metab. 18, 833-839.
50. Stroemer R. P., Cartmell T. and Rothwell N. J. (1997) Interleukin-1 receptor antagonist is not upregulated by IL-1β preconditioning. Soc. Neurosci. Abst. 23, 848.11.
51. Tsushima H. and Mori M. (2000) In vivo evidence that activation of tyrosine kinase is a trigger for lipopolysaccharide-induced fever in rats. Brain Res. 852, 367-373.
52. Turnbull A. V. and Rivier C. L. (1999) Regulation of the hypothalamicpituitary-adrenal axis by cytokines: actions and mechanisms of action. Physiol. Rev. 79, 1-71.
53. Turner C. P., Panter S. S. and Sharp F. R. (1999) Anti-oxidants prevent focal rat brain injury as assessed by induction of heat shock proteins (HSP70, HO-1/HSP32, HSP47) following subarachnoid injections of lysed blood. Mol. Brain Res. 65, 87-102.
54. Vitkovic L., Bockaert J. and Jacque C. (2000) 'Inflammatory' cytokines: neuromodulators in normal brain? J. Neurochem. 74, 457-471.
55. Vizuete M. L., Merino M., Venero J. L., Santiago M., Cano J. and Machado A. (2000) Histamine infusion induces a selective dopaminergic neuronal death along with an inflammatory reaction in rat substantia nigra. J. Neurochem. 75, 540-552.
56. Winkler C., Sauer H., Lee C. S. and Björklund A. (1996) Short-term GDNF treatment provides long-term rescue of lesioned nigral dopaminergic neurons in a rat model of Parkinson's disease. J. Neurosci, 16, 7206-7215.
57. Yamasaki Y., Matsuura N., Shozuhara H., Onodera H., Itoyama Y. and Kogure K. (1995) Interleukin-1 as a pathogenetic mediator of ischemic brain damage in rats. Stroke 26, 676-681.