Identification of distinct cellular pools of interleukin-1β during the evolution of the neuroinflammatory response induced by transient middle cerebral artery occlusion in the brain of rat

Brain Research

Volumn 1313, Issue , 2010, Pages 259-269

  Amantea, Diana ^a   Bagetta, Giacinto ^a   Tassorelli, Cristina ^b   Mercuri, Nicola Biagio ^c   Corasaniti, Maria Tiziana ^d  

^a UNIVERSITY OF CALABRIA   (Italy)

^b C MONDINO NATIONAL NEUROLOGICAL INSTITUTE   (Italy)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

Author keywords

Brain ischemia; Interleukin 1 ; Neuroinflammation

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1BETA; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN BLOOD FLOW; BRAIN REGION; CELL ACTIVATION; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; ENCEPHALITIS; GLIA CELL; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REPERFUSION INJURY;

ANIMALS; ASTROCYTES; BRAIN; CYTOKINES; DISEASE PROGRESSION; FLUORESCENT ANTIBODY TECHNIQUE; GLIAL FIBRILLARY ACIDIC PROTEIN; INFARCTION, MIDDLE CEREBRAL ARTERY; INTERLEUKIN-1BETA; MALE; MICROGLIA; MICROSCOPY, CONFOCAL; NEUROGLIA; NEUROIMMUNOMODULATION; PYRAMIDAL CELLS; RATS; RATS, WISTAR; REPERFUSION INJURY; TIME FACTORS;

RATTUS;

EID: 74349128043     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.12.017     Document Type: Article

References (53)

1. Abbott N.J., Revest P.A., and Romero I.A. Astrocyte-endothelial interaction: physiology and pathology. Neuropathol. Appl. Neurobiol. 8 (1992) 424-433
2. Amantea D., Russo R., Gliozzi M., Fratto V., Berliocchi L., Bagetta G., Bernardi G., and Corasaniti M.T. Early upregulation of matrix metalloproteinases following reperfusion triggers neuroinflammatory mediators in brain ischemia in rat. Int. Rev. Neurobiol. 82 (2007) 149-169
3. Amantea D., Corasaniti M.T., Mercuri N.B., Bernardi G., and Bagetta G. Brain regional and cellular localization of gelatinase activity in rat that have undergone transient middle cerebral artery occlusion. Neuroscience 152 (2008) 8-17
4. Barone F.C., Irving E.A., Ray A.M., Lee J.C., Kassis S., Kumar S., Badger A.M., Legos J.J., Erhardt J.A., Ohlstein E.H., Hunter A.J., Hrrison D.C., Philpott K., Smith B.R., Adams J.L., and Parsons A.A. Inhibition of p38 mitogen-activated protein kinase provides neuroprotection in cerebral focal ischemia. Med. Res. Rev. 21 (2001) 129-145
5. Black R.A., Kronheim S.R., Cantrell M., Deeley M.C., March C.J., Prockett K.S., Wignall J., Conlon P.J., Cosman D., and Hopp T.P. Generation of biologically active interleukin-1 beta by proteolytic cleavage of the inactive precursor. J. Biol. Chem. 263 (1988) 9437-9442
6. Berti R., Williams A.J., Moffett J.R., Hale S.L., Velarde L.C., Elliott P.J., Yao C., Dave J.R., and Tortella F.C. Quantitative real-time RT-PCR analysis of inflammatory gene expression associated with ischemia-reperfusion brain injury. J. Cereb. Blood Flow Metab. 22 (2002) 1068-1079
7. Block M.L., Zecca L., and Hong J.S. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev., Neurosci. 8 (2007) 57-69
8. Buttini M., Sauter A., and Boddeke H. Induction of interleukin-1beta mRNA after focal ischemia in the rat. Mol. Brain Res. 23 (1994) 126-134
9. Candelario-Jalil E., Yang Y., and Rosenberg G.A. Diverse roles of matrix metalloproteinases and tissue inhibitors of metalloproteinases in neuroinflammation and cerebral ischemia. Neuroscience 158 (2009) 983-994
10. Davies C.A., Loddick S.A., Stroemer R.P., Hunt J., and Rothwell N.J. An integrated analysis of the progression of cell responses induced by permanent focal middle cerebral artery occlusion in the rat. Exp. Neurol. 154 (1998) 199-212
11. Davies C.A., Loddick S.A., Toulmond S., Stroemer R.P., Hunt J., and Rothwell N.J. The progression and topographic distribution of interleukin-1 beta expression after permanent middle cerebral artery occlusion in the rat. J. Cereb. Blood Flow Metab. 19 (1999) 87-98
12. Davis E.J., Foster T.D., and Thomas W.E. Cellular forms and functions of brain microglia. Brain Res. Bull. 34 (1994) 73-78
13. del Zoppo G.J., and Hallenbeck J.M. Advances in the vascular pathophysiology of ischemic stroke. Thromb. Res. 98 (2000) 73-81
14. Dodson R.F., Chu L.W., Welch K.M., and Achar V.S. Acute tissue response to cerebral ischemia in the gerbil: an ultrastructural study. J. Neurol. Sci. 33 (1977) 161-170
15. Fantuzzi G., Ku G., Harding M.W., Livingston D.J., Sipe J.D., Kuida K., Flavell R.A., and Dinarello C.A. Response to local inflammation of IL-1β-converting enzyme-deficient mice. J. Immunol. 158 (1997) 1818-1824
16. Friedlander R.M., and Yuan J. ICE, neuronal apoptosis and neurodegeneration. Cell Death Diff. 5 (1998) 823-831
17. Garcia J.H., Liu K.F., and Relton J.K. Interleukin-1 receptor antagonist decreases the number of necrotic neurons in rats with middle cerebral artery occlusion. Am. J. Pathol. 147 (1995) 1477-1486
18. Hara H., Friedlander R.M., Gagliardini V., Ayata C., Fink K., Huang Z., Shimizu-Sasamata M., Yuan J., and Moskowitz M.A. Inhibition of interleukin 1β converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage. Proc. Natl Acad. Sci. U.S.A. 94 (1997) 2007-2012
19. Howard A.D., Kostura M.J., Thornberry N., Ding G.J.F., Limjuco G., Weidner J., Salley J.P., Hogquist K.A., Chaplin D.D., Mumford R.A., Schmidt J.A., and Tocci M.J. IL-1-converting enzyme requires aspartic acid residues for processing of the IL-1β precursor at two distinct sites and does not cleave 31k-Da IL-1α. J. Immunol. 147 (1991) 2964-2969
20. Irving E.A., Barone F.C., Reith A.D., Hadingham S.J., and Parsons A.A. Differential activation of MAPK/ERK and p38/SAPK in neurons and glia following focal cerebral ischaemia in the rat. Brain Res. 77 (2000) 65-75
21. Ito A., Mukaiyama A., Itoh Y., Nagase H., Thøgersen I.B., Enghild J.J., Sasaguri Y., and Mori Y. Degradation of interleukin 1β by matrix metalloproteinases. J. Biol. Chem. 271 (1996) 14657-14660
22. Jüttler E., Bonmann E., Spranger M., Kolb-Bachofen V., and Suschek C.V. A novel role of interleukin-1-converting enzyme in cytokine-mediated inducible nitric oxide synthase gene expression: implications for neuroinflammatory diseases. Mol. Cell. Neurosci. 34 (2007) 612-620
23. Kato H., Kogure K., Liu X.H., Araki T., and Itoyama Y. Progressive expression of immunomolecules on activated microglia and invading leukocytes following focal cerebral ischemia in the rat. Brain Res. 734 (1996) 203-212
24. Lau L.T., and Yu A.C. Astrocytes produce and release interleukin-1, interleukin-6, tumour necrosis factor alpha and interferon-gamma following traumatic and metabolic injury. J. Neurotrauma 18 (2001) 351-359
25. Legos J.J., Whitmore R.G., Erhardt J.A., Parsons A.A., Tuma R.F., and Barone F.C. Quantitative changes in interleukin proteins following focal stroke in the rat. Neurosci. Lett. 282 (2000) 189-192
26. Liu T., McDonnell P.C., Young P.R., White R.F., Siren A.L., Hallenbeck J.M., Barone F.C., and Feurerstein G.Z. Interleukin-1-beta messenger RNA expression in ischemic rat cortex. Stroke 24 (1993) 1746-1751
27. Longa E.Z., Weinstein P.R., Carlson S., and Cummins R. Reversible middle cerebral artery occlusion without craniotomy in rats. Stroke 20 (1989) 84-91
28. Morganti-Kossmann M.C., Rancan M., Otto V.I., Stahel P.F., and Kossmann T. Role of cerebral inflammation after traumatic brain injury: a revised concept. Shock 16 (2001) 165-177
29. Moynagh P.N. The interleukin-1 signalling pathway in astrocytes: a key contributor to inflammation in the brain. J. Anat. 207 (2005) 265-269
30. Mulcahy N., Ross J., Rothwell N.J., and Loddick S.A. Delayed administration of interleukin-1 receptor antagonist protects against transient cerebral ischemia in the rat. Br. J. Pharmacol. 140 (2003) 471-476
31. Rabuffetti M., Sciorati C., Tarozzo G., Clementi E., Manfredi A.A., and Beltramo M. Inhibition of caspase-1-like activity by Ac-Tyr-Val-Ala-Asp-Chloromethyl Ketone induces long-lasting neuroprotection in cerebral ischemia through apoptosis reduction and decrease of proinflammatory cytokines. J. Neurosci. 20 (2000) 4398-4404
32. Relton J.K., Martin D., Thompson R.C., and Russell D.A. Peripheral administration of interleukin-1 receptor antagonist inhibits brain damage after focal cerebral ischemia in the rat. Exp. Neurol. 138 (1996) 206-213
33. Relton J.K., and Rothwell N.J. Interleukin-1 receptor antagonist inhibits ischaemic and excitotoxic neuronal damage in the rat. Brain Res. Bull. 29 (1992) 242-246
34. Rosenberg G.A., Estrada E.Y., and Dencoff J.E. Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 29 (1998) 2189-2195
35. Ross J., Brough D., Gibson R.M., Loddick S.A., and Rothwell N.J. A selective, non-peptide caspase-1 inhibitor, VRT-018858, markedly reduces brain damage induced by transient ischemia in the rat. Neuropharmacology 53 (2007) 638-642
36. Rothwell N. Interleukin-1 and neuronal injury: mechanisms, modification, and therapeutic potential. Brain Behav. Immunity 17 (2003) 152-157
37. Schielke G.P., Yang G.Y., Shivers B.D., and Betz A.L. Reduced ischemic brain injury in interleukin-1 beta converting enzyme-deficient mice. J. Cereb. Blood Flow Metab. 18 (1998) 180-185
38. Schilling M., Besselmann M., Leonhard C., Mueller M., Ringelstein E.B., and Kiefer R. Microglial activation precedes and predominates over macrophage infiltration in transient focal cerebral ischemia: a study in green fluorescent protein transgenic bone marrow chimeric mice. Exp. Neurol. 183 (2003) 25-33
39. Schönbeck U., Mach F., and Libby P. Generation of biologically active IL-1 beta by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1 beta processing. J. Immunol. 161 (1998) 3340-3346
40. Stanimirovic D., Zhang W., Howlett C., Lemieux P., and Smith C. Inflammatory gene transcription in human astrocytes exposed to hypoxia: roles of the nuclear factor-κB and autocrine stimulation. J. Neuroimmunol. 119 (2001) 365-376
41. Stoll G., Jander S., and Schroeter M. Cytokines in CNS disorders: neurotoxicity versus neuroprotection. J. Neural Transm., Suppl. 59 (2000) 81-89
42. Stoll G., Jander S., and Schroeter M. Detrimental and beneficial effects of injury-induced inflammation and cytokine expression in the nervous system. Adv. Exp. Med. Biol. 513 (2002) 87-113
43. Suzumura A., Takeuchi H., Zhang G., Kuno R., and Mizuno T. Roles of glia-derived cytokines on neuronal degeneration and regeneration. Ann. N.Y. Acad. Sci. 1088 (2006) 219-229
44. Swanson R.A., Ying W., and Kauppinen T.M. Astrocyte influences on ischemic neuronal death. Curr. Mol. Med. 4 (2004) 193-205
45. Thornberry N.A., Bull H.G., Calaycay J.R., Chapman K.T., Howard A.D., Kostura M.J., Miller D.K., Molineaux S.M., Weidner J.R., Aunins J., Elliston K.O., Ayala J.M., Casano F.J., Chin J., Ding G.J.F., Egger L.A., Gaffney E.P., Limjuco G., Palyha O.C., Raju S.M., Rolando A.M., Salley J.P., Yamin T.T., Lee T.D., Shively J.E., Maccross M., Mumford R.A., Schmidt J.A., and Tocci M.J. A novel heterodimeric protease is required for interleukin-1 beta processing in monocytes. Nature 356 (1992) 768-774
46. Viscomi M.T., Florenzano F., Latini L., Amantea D., Bernardi G., and Molinari M. Methylprednisolone treatment delays remote cell death after focal brain lesion. Neuroscience 154 (2008) 1267-1282
47. Wang X.K., Yue T.L., Barone F.C., White R.F., Gagnon R.C., and Feuerstein G.Z. Concomitant cortical expression of TNF-α and IL-1β mRNAs follows early response gene expression in transient focal ischemia. Mol. Chem. Neuropathol. 23 (1994) 103-114
48. Wang X., Li X., Currie R.W., Willette R.N., Barone F.C., and Feuerstein G.Z. Application of real-time polymerase chain reaction to quantitate induced expression of interleukin-1β mRNA in ischemic brain tolerance. J. Neurosci. Res. 59 (2000) 238-246
49. Yamasaki Y., Matsuura N., Shizuhara H., Onodera H., and Itoyama Y.K.K. Interleukin-1 as a pathogenetic mediator of ischemic brain damage in the rats. Stroke 26 (1995) 676-681
50. Zhang Z., Chopp M., and Powers C. Temporal profile of microglial response following transient (2h) middle cerebral artery occlusion. Brain Res. 744 (1997) 189-198
51. Zhang Z., Chopp M., Goussev A., and Powers C. Cerebral vessels express interleukin 1 beta after focal cerebral ischemia. Brain Res. 784 (1998) 210-217
52. Zhang W., Smith C., Howlett C., and Stanimirovic D. Inflammatory activation of human brain endothelial cells by hypoxic astrocytes in vitro is mediated by IL-1β. J. Cereb. Blood Flow Metab. 20 (2000) 967-978
53. Zhang W., Petrovic J.M., Callaghan D., Jones A., Cui H., Howlett C., and Stanimirovic D. Evidence that hypoxia-inducible factor-1 (HIF-1) mediates transcriptional activation of interleukin-1beta (IL-1beta) in astrocytes cultures. J. Neuroimmunol. 174 (2006) 63-73