Minocycline protects against permanent cerebral ischemia in wild type but not in matrix metalloprotease-9-deficient mice

Journal of Cerebral Blood Flow and Metabolism

Volumn 25, Issue 4, 2005, Pages 460-467

  Koistinaho, Milla ^a   Malm, Tarja M ^a   Kettunen, Mikko I ^a   Goldsteins, Gundars ^a   Starckx, Sofie ^b   Kauppinen, Risto A ^a   Opdenakker, Ghislain ^b   Koistinaho, Jari ^a,c  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^c KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

Gene knockout; Mice; Minocycline; Neuroprotection; Stroke

Indexed keywords

DOXYCYCLINE; GELATINASE A; GELATINASE B; MINOCYCLINE; SODIUM CHLORIDE; TETRACYCLINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; DRUG MECHANISM; KNOCKOUT MOUSE; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; WILD TYPE;

ANIMALS; ANTI-BACTERIAL AGENTS; BRAIN ISCHEMIA; CEREBRAL CORTEX; DOWN-REGULATION; DOXYCYCLINE; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MINOCYCLINE;

EID: 17044364404     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.jcbfm.9600040     Document Type: Article

References (38)

1. Asahi M, Asahi K, Jung JC, del Zoppo GJ, Fini ME, Lo EH (2000) Role for matrix metalloproteinase 9 after focal cerebral ischemia: effects of gene knockout and enzyme inhibition with BB-94. J Cereb Blood Flow Metab 20:1681-9
2. Asahi M, Sumii T, Fini ME, Itohara S, Lo EH (2001) Matrix metalloproteinase 2 gene knockout has no effect on acute brain injury after focal ischemia. Neuroreport 12:3003-7
3. Barone FC, Feuerstein GZ (1999) Inflammatory mediators and stroke: new opportunities for novel therapeutics. J Cereb Blood Flow Metab 19:819-34
4. Brundula V, Rewcastle NB, Metz LM, Bernard CC, Yong VW (2002) Targeting leukocyte MMPs and transmigration: minocycline asa potential therapy for multiple sclerosis. Brain 125:1297-308
5. Chang DI, Hosomi N, Lucero J, Heo JH, Abumiya T, Mazar AP, del Zoppo GJ (2003) Activation systems for latent matrix metalloproteinase-2 are upregulated immediately after focal cerebral ischemia. J Cereb Blood Flow Metab 23:1408-19
6. Chen M, Ona VO, Li M, Ferrante RJ, Fink KB, Zhu S, Bian J, Guo L, Farrell LA, Hersch SM, Hobbs W, Vonsattel JP, Cha JH, Friedlander RM (2000) Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat Med 6:797-801
7. Clark AW, Krekoski CA, Bou SS, Chapman KR, Edwards DR (1997) Increased gelatinase A (MMP-2) and gelatinase B (MMP-9) activities in human brain after focal ischemia. Neurosci Lett 238:53-6
8. del Zoppo GJ, Mabuchi T (2003) Cerebral microvessel responses to focal ischemia. J Cereb Blood Flow Metab 23:879-94
9. Du Y, Ma Z, Lin S, Dodel RC, Gao F, Bales KR, Triarhou LC, Chernet E, Perry KW, Nelson DL, Luecke S, Phebus LA, Bymaster FP, Paul SM (2001) Minocycline prevents nigrostriatal dopaminergic neurodegeneration in the MPTP model of Parkinson's disease. Proc Natl Acad Sci USA 98:14669-74
10. Dubois B, Masure S, Hurtenbach U, Paemen L, Heremans H, van den Oord J, Sciot R, Meinhardt T, Hammerling G, Opdenakker G, Arnold B (1999) Resistance of young gelatinase B-deficient mice to experimental autoimmune encephalomyelitis and necrotizing tail lesions. J Clin Invest 104:1507-15
11. Ducharme A, Frantz S, Aikawa M, Rabkin E, Lindsey M, Rohde LE, Schoen FJ, Kelly RA, Werb Z, Libby P, Lee RT (2000) Targeted deletion of matrix metalloproteinase-9 attenuates left ventricular enlargement and collagen accumulation after experimental myocardial infarction. J Clin Invest 106:55-62
12. Fujimura M, Gasche Y, Morita-Fujimura Y, Massengale J, Kawase M, Chan PH (1999) Early appearance of activated matrix metalloproteinase-9 and blood-brain barrier disruption in mice after focal cerebral ischemia and reperfusion. Brain Res 842:92-100
13. Fukuda S, Fini CA, Mabuchi T, Koziol JA, Eggleston Jr LL, del Zoppo GJ (2004) Focal cerebral ischemia induces active proteases that degrade microvascular matrix. Stroke 35:998-1004
14. Gasche Y, Fujimura M, Morita-Fujimura Y, Copin JC, Kawase M, Massengale J, Chan PH (1999) Early appearance of activated matrix metalloproteinase-9 after focal cerebral ischemia in mice: a possible role in blood-brain barrier dysfunction. J Cereb Blood Flow Metab 19:1020-8
15. Golub LM, Lee HM, Ryan ME, Giannobile WV, Payne J, Sorsa T (1998) Tetracyclines inhibit connective tissue breakdown by multiple non-antimicrobial mechanisms. Adv Dent Res 12:12-26
16. Hibbs MS, Hasty KA, Seyer JM, Kang AH, Mainardi CL (1985) Biochemical and immunological characterization of the secreted forms of human neutrophil gelatinase. J Biol Chem 260:2493-500
17. Koistinaho M, Kettunen MI, Goldsteins G, Keinanen R, Salminen A, Ort M, Bures J, Liu D, Kauppinen RA, Higgins LS, Koistinaho J (2002) Beta-amyloid precursor protein transgenic mice that harbor diffuse A beta deposits but do not form plaques show increased ischemic vulnerability: role of inflammation. Proc Natl Acad Sci USA 99:1610-5
18. Lin T-N, He YY, Wu G, Khan M, Hsu CY (1993) Effect of brain edema on infarct volume in focal ischemia model of stroke in rats. Stroke 24:117-21
19. Majid A, He YY, Gidday JM, Kaplan SS, Gonzales ER, Park TS, Fenstermacher JD, Wei L, Choi DW, Hsu CY (2003) Differences in vulnerability to permanent focal cerebral ischemia among 3 common mouse strains. Stroke 31:2707-14
20. Opdenakker G, Van den Steen PE, Laureys G, Hunninck K, Arnold B (2003) Neutralizing antibodies in gene-defective hosts. Trends Immunol 24:94-100
21. Paemen L, Martens E, Norga K, Masure S, Roets E, Hoogmartens J, Opdenakker G (1996) The gelatinase inhibitory activity of tetracyclines and chemically modified tetracycline analogues as measured by a novel microtiter assay for inhibitors. Biochem Pharmacol 52:105-11
22. Park MJ, Park IC, Hur JH, Kim MS, Lee HC, Woo SH, Lee KH, Rhee CH, Hong SI, Lee SH (2002) Modulation of phorbol ester-induced regulation of matrix metalloproteinases and tissue inhibitors of metalloproteinases by SB203580, a specific inhibitor of p38 mitogen-activated protein kinase. J Neurosurg 97:112-8
23. Romanic AM, White RF, Arleth AJ, Ohlstein EH, Barone FC (1998) Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: inhibition of matrix metalloproteinase-9 reduces infarct size. Stroke 29:1020-30
24. Rosenberg GA, Estrada EY, Dencoff JE (1998) Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 29:2189-95
25. Rosenberg GA, Navratil M, Barone F, Feuerstein G (1996) Proteolytic cascade enzymes increase in focal cerebral ischemia in rat. J Cereb Blood Flow Metab 16:360-6
26. Sorsa T, Ramamurthy NS, Vernillo AT, Zhang X, Konttinen YT, Rifkin BR, Golub LM (1998) Functional sites of chemically modified tetracyclines: inhibition of the oxidative activation of human neutrophil and chicken osteoclast pro-matrix metalloproteinases. J Rheumatol 25:975-82
27. Tikka T, Koistinaho J (2001) Minocycline provides neuroprotection against N-methyl-D-aspartate neurotoxicity by inhibiting microglia. J Immunol 166:7527-33
28. Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J (2001) Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 21:2580-8
29. Tikka T, Vartiainen N, Goldsteins G, Oja SS, Andersen PM, Marklund SL, Koistinaho J (2002) Minocycline prevents neurotoxicity induced by cerebrospinal fluid from patients with motor neurone disease. Brain 125:722-31
30. Van den Steen PE, Dubois B, Nelissen I, Rudd PM, Dwek RA, Opdenakker G (2002) Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Crit Rev Biochem Mol Biol 37:375-536
31. Vayalil PK, Katiyar SK (2004) Treatment of epigallocatechin-3-gallate inhibits matrix metalloproteinases-2 and -9 via inhibition of activation of mitogen-activated protein kinases, c-jun and NF-kappaB in human prostate carcinoma DU-145 cells. Prostate 59:33-42
32. Vitale S, Schmid-Alliana A, Breuil V, Pomeranz M, Millet MA, Rossi B, Schmid-Antomarchi H (2004) Soluble fractalkine prevents monocyte chemoattractant protein-1-induced monocyte migration via inhibition of stress-activated protein kinase 2/p38 and matrix metalloproteinase activities. J Immunol 172:585-92
33. Wang CX, Yang T, Shuaib A (2003) Effects of minocycline alone and in combination with mild hypothermia in embolic stroke. Brain Res 963:239-327
34. Xu L, Fagan SC, Waller JL, Edwards D, Borlongan CV, Zheng J, Hill WD, Feuerstein G, Hess DC (2004) Low dose intravenous minocycline is neuroprotective after middle cerebral artery occlusion-reperfusion in rats. BMC Neurol 4:7
35. Yrjänheikki J, Keinänen R, Pellikka M, Hökfelt T, Koistinaho J (1998) Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci USA 95:15769-74
36. Yrjänheikki J, Tikka T, Keinänen R, Goldsteins G, Chan PH, Koistinaho J (1999) A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci USA 96:13496-500
37. Zhang F, Iadecola C (1998) Temporal characteristics of the protective effect of aminoguanidine on cerebral ischemic damage. Brain Res 802:104-10
38. Zhu S, Stavrovskaya IG, Drozda M, Kim BY, Ona V, Li M, Sarang S, Liu AS, Hartley DM, Wu du C, Gullans S, Ferrante RJ, Przedborski S, Kristal BS, Friedlander RM (2002) Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 417:74-8