Early reperfusion injury is associated to MMP2 and IL-1β elevation in cortical neurons of rats subjected to middle cerebral artery occlusion

Neuroscience

Volumn 277, Issue , 2014, Pages 755-763

  Amantea, D ^a   Certo, M ^a   Russo, R ^a   Bagetta, G ^a   Corasaniti, M T ^b   Tassorelli, C ^c  

^a UNIVERSITY OF CALABRIA   (Italy)

^b UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

^c C MONDINO NATIONAL NEUROLOGICAL INSTITUTE   (Italy)

Author keywords

Brain ischemia; IL 1 ; Matrix metalloproteinases; Neuroinflammation

Indexed keywords

4 [4 (METHANESULFONAMIDE)PHENOXY]PHENYLSULFONYL METHYLTHIIRANE; GELATINASE A; ILOMASTAT; INTERLEUKIN 1BETA; MATRIX METALLOPROTEINASE INHIBITOR; UNCLASSIFIED DRUG; 2 [[(4 PHENOXYPHENYL)SULFONYL]METHYL]THIIRANE; GELATIN; GELATINASE B; GELATINOL; IL1B PROTEIN, RAT; MMP2 PROTEIN, RAT; MMP9 PROTEIN, RAT; NEUROPROTECTIVE AGENT;

ADULT; AMINO ACID BRAIN LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CELL; BRAIN REGION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; RAT; REPERFUSION INJURY; TRANSIENT ISCHEMIC ATTACK; UPREGULATION; ZYMOGRAPHY; DRUG INHIBITION; ENZYME MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; BRAIN CORTEX; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; INFARCTION, MIDDLE CEREBRAL ARTERY; METABOLISM; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZATION; TIME; WISTAR RAT;

ANIMALS; ASTROCYTES; CEREBRAL CORTEX; ENZYME-LINKED IMMUNOSORBENT ASSAY; GELATIN; IMMUNOHISTOCHEMISTRY; INFARCTION, MIDDLE CEREBRAL ARTERY; INTERLEUKIN-1BETA; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASE INHIBITORS; NEURONS; NEUROPROTECTIVE AGENTS; RANDOM ALLOCATION; RATS, WISTAR; REPERFUSION INJURY; TIME FACTORS;

EID: 84907028877     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.07.064     Document Type: Article

References (88)

1. Ahn B.J., Le H., Shin M.W., Bae S.J., Lee E.J., et al. The N-terminal ectodomain of Ninjurin1 liberated by MMP9 has chemotactic activity. Biochem Biophys Res Commun 2012, 428(4):438-444.
2. Allan S.M., Rothwell N.J. Cytokines and acute neurodegeneration. Nat Rev Neurosci 2001, 2:734-744.
3. Allan S.M., Tyrrell P.J., Rothwell N.J. Interleukin-1 and neuronal injury. Nat Rev Immunol 2005, 5:629-640.
4. Amantea D., Russo R., Gliozzi M., Fratto V., Berliocchi L., et al. Early upregulation of matrix metalloproteinases following reperfusion triggers neuroinflammatory mediators in brain ischemia in rat. Int Rev Neurobiol 2007, 82:149-169.
5. Amantea D., Corasaniti M.T., Mercuri N.B., Bernardi G., Bagetta G. Brain regional and cellular localization of gelatinase activity in rat that have undergone transient middle cerebral artery occlusion. Neuroscience 2008, 152:8-17.
6. Amantea D., Bagetta G., Tassorelli C., Mercuri N.B., Corasaniti M.T. Identification of distinct cellular pools of interleukin-1beta during the evolution of the neuroinflammatory response induced by transient middle cerebral artery occlusion in the brain of rat. Brain Res 2010, 1313:259-269.
7. Amantea D., Tassorelli C., Russo R., Petrelli F., Morrone L.A., et al. Neuroprotection by leptin in a rat model of permanent cerebral ischemia: effects on STAT3 phosphorylation in discrete cells of the brain. Cell Death Dis 2011, 2:e238.
8. Amantea D., Tassorelli C., Petrelli F., Certo M., Bezzi P., et al. Understanding the multifaceted role of inflammatory mediators in ischemic stroke. Curr Med Chem 2014, 21:2098-2117.
9. Armogida M., Spalloni A., Amantea D., Nutini M., Petrelli F., et al. The protective role of catalase against cerebral ischemia in vitro and in vivo. Int J Immunopathol Pharmacol 2011, 24:735-747.
10. Asahi M., Asahi K., Jung J.C., del Zoppo G.J., Fini M.E., Lo E.H. Role for matrix metalloproteinase 9 after focal cerebral ischemia: effects of gene knockdown and enzyme inhibition with BB-94. J Cereb Blood Flow Metab 2000, 20:1681-1689.
11. Asahi M., Wang X., Mori T., Sumii T., Jung J.C., et al. Effects of matrix metalloproteinase-9 gene knockout on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J Neurosci 2001, 21:7724-7732.
12. Bandtlow C.E., Meyer M., Lindholm D., Spranger M., Heumann R., Thoenen H. Regional and cellular co-distribution of interleukin-1β and nerve growth factor mRNA in the adult rat brain: possible relationship to the regulation of nerve growth factor synthesis. J Cell Biol 1990, 111:1701-1711.
13. Barber P.A., Rushforth D., Agrawal S., Tuor U.I. Infrared optical imaging of matrix metalloproteinases (MMPs) up regulation following ischemia reperfusion is ameliorated by hypothermia. BMC Neurosci 2012, 13:76.
14. Belayev L., Zhao W., Busto R., Ginsberg M.D. Transient middle cerebral occlusion by intraluminal suture: I. Three-dimensional autoradiographic image-analysis of local cerebral glucose metabolism-blood flow interrelationship during ischemia and early recirculation. J Cereb Blood Flow Metab 1997, 17:1266-1280.
15. Berta T., Liu T., Liu Y.C., Xu Z.Z., Ji R.R. Acute morphine activates satellite glial cells and up-regulates IL-1β in dorsal root ganglia in mice via matrix metalloprotease-9. Mol Pain 2012, 8:18.
16. Bonfil R.D., Dong Z., Trindade Filho J.C., Sabbota A., Osenkowski P., et al. Prostate cancer-associated membrane type 1-matrix metalloproteinase: a pivotal role in bone response and intraosseous tumor growth. Am J Pathol 2007, 170:2100-2111.
17. Buttini M., Sauter A., Boddeke H.W. Induction of interleukin-1 beta mRNA after focal cerebral ischaemia in the rat. Brain Res Mol Brain Res 1994, 23(1-2):126-134.
18. Celenza G., Villegas-Estrada A., Lee M., Boggess B., Forbes C., et al. Metabolism of (4-phenoxyphenylsulfonyl)methylthiirane, a selective gelatinase inhibitor. Chem Biol Drug Des 2008, 71:187-196.
19. Chang D.I., Hosomi N., Lucero J., Heo J.H., Abumiya T., et al. Activation systems for latent matrix metalloproteinase-2 are upregulated immediately after focal cerebral ischemia. J Cereb Blood Flow Metab 2003, 23:1408-1419.
20. Clausen B.H., Lambertsen K.L., Meldgaard M., Finsen B. A quantitative in situ hybridization and polymerase chain reaction study of microglial-macrophage expression of interleukin-1beta mRNA following permanent middle cerebral artery occlusion in mice. Neuroscience. 2005, 132:879-892.
21. Coeshott C., Ohnemus C., Pilyavskaya A., Ross S., Wieczorek M., et al. Converting enzyme-independent release of tumor necrosis factor alpha and IL-1beta from a stimulated human monocytic cell line in the presence of activated neutrophils or purified proteinase 3. Proc Natl Acad Sci USA 1999, 96:6261-6266.
22. Copin J.C., Goodyear M.C., Gidday J.M., Shah A.R., Gascon E., et al. Role of matrix metalloproteinases in apoptosis after transient focal cerebral ischemia in rats and mice. Eur J Neurosci 2005, 22:1597-1608.
23. Corasaniti M.T., Turano P., Bilotta A., Malorni W., Stringaro A.R., et al. Evidence that increases of mitochondrial immunoreactive IL-1beta by HIV-1 gp120 implicate in situ cleavage of pro-IL-1beta in the neocortex of rat. J Neurochem 2001, 78(3):611-618.
24. Corasaniti M.T., Russo R., Amantea D., Gliozzi M., Siviglia E., et al. Neuroprotection by the caspase-1 inhibitor Ac-YVAD-(acyloxy)mk in experimental neuroAIDS is independent from IL-1beta generation. Cell Death Differ 2005, 12(Suppl. 1):999-1001.
25. Cui J., Chen S., Zhang C., Meng F., Wu W., et al. Inhibition of MMP-9 by a selective gelatinase inhibitor protects neurovasculature from embolic focal cerebral ischemia. Mol Neurodegener 2012, 7:21.
26. Del Zoppo G.J. The neurovascular unit, matrix proteases, and innate inflammation. Ann N Y Acad Sci 2010, 1207:46-49.
27. Denes A., Pinteaux E., Rothwell N.J., Allan S.M. Interleukin-1 and stroke: biomarker, harbinger of damage, and therapeutic target. Cerebrovasc Dis 2011, 32(6):517-527.
28. Denes A., Wilkinson F., Bigger B., Chu M., Rothwell N.J., Allan S.M. Central and haematopoietic interleukin-1 both contribute to ischaemic brain injury in mice. Dis Model Mech 2013, 6(4):1043-1048.
29. Dinarello C.A. Biologic basis for interleukin-1 in disease. Blood 1996, 87:2095-2147.
30. Dinarello C.A. Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol 2009, 27:519-550.
31. Dinarello C.A. A clinical perspective of IL-1β as the gatekeeper of inflammation. Eur J Immunol 2011, 41(5):1203-1217.
32. Enzmann G., Mysiorek C., Gorina R., Cheng Y.J., Ghavampour S., et al. The neurovascular unit as a selective barrier to polymorphonuclear granulocyte (PMN) infiltration into the brain after ischemic injury. Acta Neuropathol 2013, 125:395-412.
33. Fann D.Y.W., Lee S.Y., Manzanero S., Chunduri P., Sobey C.G., Arumugam T.V. Pathogenesis of acute stroke and the role of inflammasomes. Ageing Res Rev 2013, 12:941-966.
34. Galea J., Ogungbenro K., Hulme S., Greenhalgh A., Aarons L., et al. Intravenous anakinra can achieve experimentally effective concentrations in the central nervous system within a therapeutic time window: results of a dose-ranging study. J Cereb Blood Flow Metab 2011, 31:439-447.
35. Gasche Y., Copin J.C., Sugawara T., Fujimura M., Chan P.H. Matrix metalloproteinase inhibition prevents oxidative stress associated blood-brain barrier disruption after transient focal cerebral ischemia. J Cereb Blood Flow Metab 2001, 21:1393-1400.
36. Greco R., Mangione A.S., Amantea D., Bagetta G., Nappi G., Tassorelli C. IkappaB-alpha expression following transient focal cerebral ischemia is modulated by nitric oxide. Brain Res 2011, 1372:145-151.
37. Greenhalgh A.D., Galea J., Denes A., Tyrrell P.J., Rothwell N.J. Rapid brain penetration of interleukin-1 receptor antagonist in rat cerebral ischaemia: pharmacokinetics, distribution, protection. Br J Pharmacol 2010, 160:153-159.
38. Greten F.R., Arkan M.C., Bollrath J., Hsu L.C., Goode J., et al. NF-kappaB is a negative regulator of IL-1beta secretion as revealed by genetic and pharmacological inhibition of IKKbeta. Cell 2007, 130:918-931.
39. Gu Z.Z., Cui J., Brown S., Fridman R., Mobashery S., et al. A highly specific inhibitor of matrix metalloproteinase-9 rescues laminin from proteolysis and neurons from apoptosis in transient focal cerebral ischemia. J Neurosci 2005, 25:6401-6408.
40. Hill J.W., Poddar R., Thompson J.F., Rosenberg G.A., Yang Y. Intranuclear matrix metalloproteinases promote DNA damage and apoptosis induced by oxygen-glucose deprivation in neurons. Neuroscience 2012, 220:277-290.
41. Horstmann S., Kalb P., Koziol J., Gardner H., Wagner S. Profiles of matrix metalloproteinases, their inhibitors, and laminin in stroke patients: influence of different therapies. Stroke 2003, 34:2165-2170.
42. Ikejiri M., Bernardo M.M., Bonfil R.D., Toth M., Chang M., et al. Potent mechanism-based inhibitors for matrix metalloproteinases. J Biol Chem 2005, 280(40):33992-34002.
43. Jalal F.Y., Yang Y., Thompson J., Lopez A.C., Rosenberg G.A. Myelin loss associated with neuroinflammation in hypertensive rats. Stroke 2012, 43(4):1115-1122.
44. Joosten L.A., Netea M.G., Fantuzzi G., Koenders M.I., Helsen M.M., et al. Inflammatory arthritis in caspase 1 gene-deficient mice: contribution of proteinase 3 to caspase 1-independent production of bioactive interleukin-1beta. Arthritis Rheum 2009, 60(12):3651-3662.
45. Kaczmarek L. Mmp-9 inhibitors in the brain: can old bullets shoot new targets?. Curr Pharm Des 2013, 19(6):1085-1089.
46. Kilkenny C., Browne W.J., Cuthill I.C., Emerson M., Altman D.G. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 2010, 8(6):e1000412.
47. Kontogiorgis C.A., Papaioannou P., Hadjipavlou-Litina D.J. Matrix metalloproteinase inhibitors: a review on pharmacophore mapping and (Q)SARs results. Curr Med Chem 2005, 12(3):339-355.
48. Lakhan S.E., Kirchgessner A., Tepper D., Leonard A. Matrix metalloproteinases and blood-brain barrier disruption in acute ischemic stroke. Front Neurol 2013, 4:32.
49. Lambertsen K.L., Biber K., Finsen B. Inflammatory cytokines in experimental and human stroke. J Cereb Blood Flow Metab 2012, 32(9):1677-1698.
50. Lechan R.M., Toni R., Clark B.D., Cannon J.G., Shaw A.R., et al. Immunoreactive interleukin-1β localization in the rat forebrain. Brain Res 1990, 514:135-140.
51. Lee M., Villegas-Estrada A., Celenza G., Boggess B., Toth M., et al. Metabolism of a highly selective gelatinase inhibitor generates active metabolite. Chem Biol Drug Des 2007, 70:371-382.
52. Lee M., Ikejiri M., Klimpel D., Toth M., Espahbodi M., et al. Structure-activity relationship for thiirane-based gelatinase inhibitors. ACS Med Chem Lett 2012, 3(6):490-495.
53. Lu A., Suofu Y., Guan F., Broderick J.P., Wagner K.R., Clark J.F. Matrix metalloproteinase-2 deletions protect against hemorrhagic transformation after 1h of cerebral ischemia and 23h of reperfusion. Neuroscience 2013, 253:361-367.
54. Luheshi N.M., Kovács K.J., Lopez-Castejon G., Brough D., Denes A. Interleukin-1α expression precedes IL-1β after ischemic brain injury and is localised to areas of focal neuronal loss and penumbral tissues. J Neuroinflamm 2011, 8:186.
55. Mannello F., Medda V. Nuclear localization of matrix metalloproteinases. Prog Histochem Cytochem 2012, 47(1):27-58.
56. Martinon F., Burns K., Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-β. Mol Cell 2002, 10:417-426.
57. Memezawa H., Minamisawa H., Smith M.L., Siesjo B.K. Ischemic penumbra in a model of reversible middle cerebral artery occlusion in the rat. Exp Brain Res 1992, 89:67-78.
58. Murata Y., Fujiwara N., Seo J.H., Yan F., Liu X., et al. Delayed inhibition of c-Jun N-terminal kinase worsens outcomes after focal cerebral ischemia. J Neurosci 2012, 32(24):8112-8115.
59. Nagel S., Su Y., Horstmann S., Heiland S., Gardner H., et al. Minocycline and hypothermia for reperfusion injury after focal cerebral ischemia in the rat: effects on BBB breakdown and MMP expression in the acute and subacute phase. Brain Res 2008, 1188:198-206.
60. Navaratna D., Fan X., Leung W., Lok J., Guo S., et al. Cerebrovascular degradation of TRKB by MMP9 in the diabetic brain. J Clin Invest 2013, 123(8):3373-3377.
61. Netea M.G., Simon A., van de Veerdonk F., Kullberg B.J., Van der Meer J.W., Joosten L.A. IL-1beta processing in host defense: beyond the inflammasomes. PLoS Pathog 2010, 6(2):e1000661.
62. Planas A.M., Sole S., Justicia C. Expression and activation of matrix metalloproteinase-2 and -9 in rat brain after transient focal cerebral ischemia. Neurobiol Dis 2001, 8:834-846.
63. Pradillo J.M., Denes A., Greenhalgh A.D., Boutin H., Drake C. Delayed administration of interleukin-1 receptor antagonist reduces ischemic brain damage and inflammation in comorbid rats. J Cereb Blood Flow Metab 2012, 32(9):1810-1819.
64. Relton J.K., Rothwell N.J. Interleukin-1 receptor antagonist inhibits ischaemic and excitotoxic neuronal damage in the rat. Brain Res Bull 1992, 29:243-246.
65. Romanic A.M., White R.F., Arleth A.J., Ohlstein E.H., Barone F.C. Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: inhibition of matrix metalloproteinase-9 reduces infarct size. Stroke 1998, 29:1020-1030.
66. Rosell A., Lo E.H. Multiphasic roles for matrix metalloproteinases after stroke. Curr Opin Pharmacol 2008, 8(1):82-89.
67. Rosenberg G.A., Estrada E.Y., Dencoff J.E. Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 1998, 29:2189-2195.
68. Rosenberg G.A., Cunningham L.A., Wallace J., Alexander S., Estrada E.Y., et al. Immunohistochemistry of matrix metalloproteinases in reperfusion injury in rat brain: activation of MMP-9 linked to stromelysin-1 and microglia in cell cultures. Brain Res 2001, 893:104-112.
69. Russo R., Siviglia E., Gliozzi M., Amantea D., Paoletti A., et al. Evidence implicating matrix metalloproteinases in the mechanism underlying accumulation of IL-1beta and neuronal apoptosis in the neocortex of HIV/gp120-exposed rats. Int Rev Neurobiol 2007, 82:407-421.
70. Sato H., Kinoshita T., Takino T., Nakayama K., Seiki M. Activation of a recombinant membrane type 1-matrix metalloproteinase (MT1-MMP) by furin and its interaction with tissue inhibitor of metalloproteinases (TIMP)-2. FEBS Lett 1996, 393:101-104.
71. Savage C.D., Lopez-Castejon G., Denes A., Brough D. NLRP3-inflammasome activating DAMPs stimulate an inflammatory response in glia in the absence of priming which contributes to brain inflammation after injury. Front Immunol 2012, 3:288.
72. Schönbeck U., Mach F., 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 1998, 161(7):3340-3346.
73. Seo J.H., Guo S., Lok J., Navaratna D., Whalen M.J., et al. Neurovascular matrix metalloproteinases and the blood-brain barrier. Curr Pharm Des 2012, 18(25):3645-3648.
74. Skiles J.W., Gonnella N.C., Jeng A.Y. The design, structure, and clinical update of small molecular weight matrix metalloproteinase inhibitors. Curr Med Chem 2004, 11(22):2911-2977.
75. Strongin A.Y., Collier I., Bannikov G., Marmer B.L., Grant G.A., Goldberg G.I. Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J Biol Chem 1995, 270:5331-5338.
76. Testero S.A., Lee M., Staran R.T., Espahbodi M., Llarrull L.I., et al. Sulfonate-containing thiiranes as selective gelatinase inhibitors. ACS Med Chem Lett 2011, 2:177-181.
77. Tu G., Xu W., Huang H., Li S. Progress in the development of matrix metalloproteinase inhibitors. Curr Med Chem 2008, 15(14):1388-1395.
78. van de Veerdonk F.L., Netea M.G., Dinarello C.A., Joosten L.A. Inflammasome activation and IL-1β and IL-18 processing during infection. Trends Immunol 2011, 32(3):110-116.
79. Vila N., Castillo J., Davalos A., Chamorro A. Proinflammatory cytokines and early neurological worsening in ischemic stroke. Stroke 2000, 31:2325-2329.
80. Watt J.A., Hobbs N.K. Interleukin-1β immunoreactivity in identified neurons of the rat magnocellular neurosecretory system: evidence for activity-dependent release. J Neurosci Res 2000, 60:478-489.
81. Whittaker M., Floyd C.D., Brown P., Gearing A.J. Design and therapeutic application of matrix metalloproteinase inhibitors. Chem Rev 1999, 99(9):2735-2776.
82. Yamasaki Y., Matsuura N., Shozuhara H., Onodera H., Itoyama Y., Kogure K. Interleukin-1 as a pathogenetic mediator of ischemic brain damage in rats. Stroke 1995, 26:676-680. [discussion 681].
83. Yang Y., Estrada E., Thompson J., Liu W., Rosenberg G. Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J Cereb Blood Flow Metab 2007, 27:697-709.
84. Yang Y., Candelario-Jalil E., Thompson J.F., Cuadrado E., Estrada E.Y., et al. Increased intranuclear matrix metalloproteinase activity in neurons interferes with oxidative DNA repair in focal cerebral ischemia. J Neurochem 2010, 112(1):134-149.
85. Yang Y., Thompson J.F., Taheri S., Salayandia V.M., McAvoy T.A., et al. Early inhibition of MMP activity in ischemic rat brain promotes expression of tight junction proteins and angiogenesis during recovery. J Cereb Blood Flow Metab 2013, 33(7):1104-1114.
86. Yilmaz G., Granger D.N. Cell adhesion molecules and ischemic stroke. Neurol Res 2008, 30:783-793.
87. Yong V.W. Metalloproteinases: mediators of pathology and regeneration in the CNS. Nature Rev Neurosci 2005, 6:931-944.
88. Zhao B.Q., Wang S., Kim H.Y., Storrie H., Rosen B.R., et al. Role of matrix metalloproteinases in delayed cortical responses after stroke. Nat Med 2006, 12:441-445.