Skip to main content
SpringerLink
Log in

Matrix Metalloproteinases in Ischemia–Reperfusion Injury in Brain: Antioxidants as Rescuer

  • Chapter
  • First Online:
Role of Proteases in Cellular Dysfunction

Part of the book series: Advances in Biochemistry in Health and Disease ((ABHD,volume 8))

  • 1271 Accesses

Abstract

Cerebral ischemia–reperfusion (CIR) injury exerts a potential threat on neuronal cell survival. Cerebral ischemia, a type of stroke, ensues due to occlusion of oxygen in common carotid arteries and blockage of nutrients in brain tissues. It is the most common and lethal neurological disorder especially in the aged individuals. When neuronal cells become deprived of sufficient oxygen because of low blood flow rate following ischemic stroke, a cascade of events occurs, leading to cell death by toxicity and oxidative stress. Oxidative stress appears to be an important role in CIR injury wherein a large amount of reactive oxygen species generated by the mitochondria provokes the release of cytochrome c and other apoptotic proteins, leading to defective gene expression and subsequent cell death. Under CIR, natural defense mechanism fails to protect neurons from oxidative damage. Matrix metalloproteinases (MMPs), mainly MMP-2 and MMP-9, are elevated after cerebral ischemia which are involved in accelerating matrix degradation, disrupting the blood–brain barrier (BBB), and increasing the neuronal infarct size. Some compounds (flavonoids, antioxidants, MMP inhibitors) show the potency as neuroprotectant against CIR. Question arises how to reduce the cytotoxicity of the compounds and overcome the BBB permeability? Over the past few years, different vesicular formulations, especially liposome and nanocapsule, have received attention as effective modality in enhancing therapeutic concentration while rescuing CIR. This chapter is focused on the mechanism of MMPs’ action during CIR injury and to delineate the effect of MMP inhibitors and antioxidants with their different formulations in modulating MMP activity.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Soler EP & Ruiz VC (2010) Epidemiology and risk factors of cerebral ischemia and ischemic heart diseases: similarities and differences. Curr Cardiol Rev 6:138-149

    PubMed  Google Scholar 

  2. Donnan GA, Fisher M, Macleod M et al (2008) The secondary prevention of stroke. The Lancet 372:1036

    Google Scholar 

  3. Mathers CD, Boerma T, Ma Fat D (2009) Global and regional causes of death. Brit Med Bull 92:7-32

    PubMed  Google Scholar 

  4. Lakhan S, Kirchgessner A, Hofer M (2009) Inflammatory mechanisms in ischemic stroke: therapeutic approaches. J Transl Med 7:97

    PubMed  Google Scholar 

  5. Sims NR, Muyderman H (2010) Mitochondria, oxidative metabolism and cell death in stroke. BBA – Mol Basis Dis 1802:80-91

    Google Scholar 

  6. Khatri R, McKinney AM, Swenson B et al (2012) Blood–brain barrier, reperfusion injury, and hemorrhagic transformation in acute ischemic stroke. Neurology 79: S52-57

    PubMed  Google Scholar 

  7. Stanimirovic D , Satoh K (2000) Inflammatory mediators of cerebral endothelium: a role in ischemic brain inflammation. Brain Pathol 10:113-126

    PubMed  CAS  Google Scholar 

  8. Ritter LS, Orozco JA, Coull BM et al (2000) Leukocyte accumulation and hemodynamic changes in the Cerebral Microcirculation during early reperfusion after Stroke. Stroke 31:1153-1161

    PubMed  CAS  Google Scholar 

  9. Sugawara T, Fujimura M, Noshita N et al (2004) Neuronal death/survival signaling pathways in cerebral ischemia. Neurotherapeutics 1:17-25

    Google Scholar 

  10. Dale N, Frenguelli BG (2009) Release of adenosine and ATP during ischemia and epilepsy. Curr Neuropharmacology 7:160-179

    CAS  Google Scholar 

  11. Bora KS, Sharma A (2011) Evaluation of Antioxidant and Cerebroprotective Effect of Medicago sativa Linn. against Ischemia and Reperfusion Insult. J Evid Based Complementary Altern Med 2011:792167

    Google Scholar 

  12. Greve MW, Zink BJ (2009) Pathophysiology of traumatic brain injury. Mount Sinai Journal of Medicine: J Translat Personalized Med 76:97-104

    Google Scholar 

  13. Atlee JL (2007) ed. Complications in Anesthesia, 2nd ed. Philadelphia: Saunders Elsevier, 2007:508-4512

    Google Scholar 

  14. Siesjö BK (1992) Pathophysiology and treatment of focal cerebral ischemia. J Neurosurg 77:337-354

    PubMed  Google Scholar 

  15. Stamatovic SM, Keep RF, Andjelkovic AV (2008) Brain endothelial cell-cell junctions: how to “open” the blood brain barrier. Curr Neuropharmacol 6:179-192

    PubMed  CAS  Google Scholar 

  16. Kundu P, Mukhopadhyay AK, Patra R et al (2006) Cag Pathogenicity Island-independent Up-regulation of Matrix Metalloproteinases-9 and −2 Secretion and Expression in Mice by Helicobacter pylori Infection. J Biol Chem 281:34651-34662

    PubMed  CAS  Google Scholar 

  17. Hermann DM, Matter CM (2007) Tissue Plasminogen Activator–Induced Reperfusion Injury After Stroke Revisited. Circulation 116:363-365

    PubMed  Google Scholar 

  18. Ceulemans A-G, Zgavc T, Kooijman R et al (2010) The dual role of the neuroinflammatory response after ischemic stroke: modulatory effects of hypothermia. J. of Neuroinflam. 7:74

    Google Scholar 

  19. Cheng T, Petraglia AL, Li Z et al (2006) Activated protein C inhibits tissue plasminogen activator-induced brain hemorrhage. Nat Med 12:1278-1285

    PubMed  CAS  Google Scholar 

  20. Kilic E, Kilic Ü, Reiter RJ, Bassetti CL et al (2005) Tissue-plasminogen activator-induced ischemic brain injury is reversed by melatonin: role of iNOS and Akt. J Pineal Res 39:151-155

    PubMed  CAS  Google Scholar 

  21. Kilic E, Kilic U, Matter CM et al (2005) Aggravation of Focal Cerebral Ischemia by Tissue Plasminogen Activator Is Reversed by 3-Hydroxy-3-Methylglutaryl Coenzyme A Reductase Inhibitor but Does Not Depend on Endothelial NO Synthase. Stroke 36:332-336

    PubMed  CAS  Google Scholar 

  22. Zhang L, Zhang ZG, Ding GL et al (2005) Multitargeted Effects of Statin-Enhanced Thrombolytic Therapy for Stroke With Recombinant Human Tissue-Type Plasminogen Activator in the Rat. Circulation 112:3486-3494

    PubMed  CAS  Google Scholar 

  23. Liu D, Cheng T, Guo H et al (2004) Tissue plasminogen activator neurovascular toxicity is controlled by activated protein C. Nat Med 10:1379-1383

    PubMed  CAS  Google Scholar 

  24. Tsay HJ, Wang P, Wang SL et al (2000) Age-associated changes of superoxide dismutase and catalase activities in the rat brain. J Biomed Sci 7:466-474

    PubMed  CAS  Google Scholar 

  25. Amirkhizi F, Siassi F, Djalali M et al (2010) Assessment of antioxidant enzyme activities in erythrocytes of pre-hypertensive and hypertensive women. J Res Med Sci 15:270-278

    PubMed  Google Scholar 

  26. Verstraete M, Bounameaux H, de Cock F et al (1985) Pharmacokinetics and systemic fibrinogenolytic effects of recombinant human tissue-type plasminogen activator (rt-PA) in humans. J Pharm Exp Ther 235:506-512

    CAS  Google Scholar 

  27. Matsumiya N, Koehler RC, Kirsch JR et al (1991) Conjugated superoxide dismutase reduces extent of caudate injury after transient focal ischemia in cats. Stroke 22:1193-1200

    PubMed  CAS  Google Scholar 

  28. Michowiz SD, Melamed E, Pikarsky E et al (1990) Effect of ischemia induced by middle cerebral artery occlusion on superoxide dismutase activity in rat brain. Stroke 21:1613-1617

    PubMed  CAS  Google Scholar 

  29. Mahadik SP, Makar TK, Murthy JN et al (1993) Temporal changes in superoxide dismutase, glutathione peroxidase, and catalase levels in primary and peri-ischemic tissue. Monosialoganglioside (GM1) treatment effects. Mol Chem Neuropathol 18:1-14

    PubMed  CAS  Google Scholar 

  30. Tasdemiroglu E, Chistenberry PD, Ardell JL et al (1993) Effect of superoxide dismutase on acute reperfusion injury of the rabbit brain. Acta Neurochir (Wien) 120:180-186

    CAS  Google Scholar 

  31. Yamaguchi K, Uematsu D, Itoh Y et al (2002) In vivo measurement of superoxide in the cerebral cortex during anoxia-reoxygenation and ischemia-reperfusion. Keio J Med 51:201-207

    PubMed  CAS  Google Scholar 

  32. Chaudhary G, Sinha K, Gupta YK (2003) Protective effect of exogenous administration of α-tocopherol in middle cerebral artery occlusion model of cerebral ischemia in rats. Fundam Clin Pharm 17:703-707

    CAS  Google Scholar 

  33. Truelove D, Shuaib A, Ijaz S et al (1994) Superoxide dismutase, catalase, and U78517F attenuate neuronal damage in gerbils with repeated brief ischemic insults. Neurochem Res 19:665-671

    PubMed  CAS  Google Scholar 

  34. Maier CM, Ahern K, Cheng ML et al (2002) Effects of Mild Hypothermia on Superoxide Anion Production, Superoxide Dismutase Expression, and Activity Following Transient Focal Cerebral Ischemia. Neurobiol Dis 11:28-42

    PubMed  CAS  Google Scholar 

  35. Khaira HS, Maxwell SR, Thomason H et al (1996) Antioxidant depletion during aortic aneurysm repair. Brit J Surg 83:401-403

    PubMed  CAS  Google Scholar 

  36. Berman K, Brodaty H (2004) Tocopherol (vitamin E) in Alzheimer’s disease and other neurodegenerative disorders. CNS Drugs 18:807-825

    PubMed  CAS  Google Scholar 

  37. Sanossian N, Ovbiagele B (2009) Prevention and management of stroke in very elderly patients. The Lancet Neurology 8:1031-1041

    Google Scholar 

  38. Stam J (2005) Thrombosis of the Cerebral Veins and Sinuses. New Engl J Med 352:1791-1798

    PubMed  CAS  Google Scholar 

  39. Brunner LS, Smeltzer SCOC, Bare BG et al (2008) Brunner and Suddarth’s Textbook of Medical Surgical Nursing 11th ed. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins p.1527

    Google Scholar 

  40. Ellerbroek SM, Halbleib JM, Benavidez M et al (2001) Phosphatidylinositol 3-Kinase Activity in Epidermal Growth Factor-stimulated Matrix Metalloproteinase-9 Production and Cell Surface Association. Cancer Res. 61:1855-186

    PubMed  CAS  Google Scholar 

  41. Liu J-F, Crépin M, Liu J-M et al (2002) FGF-2 and TPA induce matrix metalloproteinase-9 secretion in MCF-7 cells through PKC activation of the Ras/ERK pathway. Biochem Bioph Res Co 293:1174-1182

    CAS  Google Scholar 

  42. Ruhul Amin ARM, Senga T, Oo ML et al (2003) Secretion of matrix metalloproteinase-9 by the proinflammatory cytokine, IL-1β: a role for the dual signalling pathways, Akt and Erk. Genes to Cells 8:515-523

    PubMed  CAS  Google Scholar 

  43. Suyama K, Shapiro I, Guttman M et al (2002) A signaling pathway leading to metastasis is controlled by N-cadherin and the FGF receptor. Cancer Cell 2:301-314

    PubMed  CAS  Google Scholar 

  44. Busti C, Falcinelli E, Momi S et al (2010) Matrix metalloproteinases and peripheral arterial disease. Intern Emerg Med 5:13-25

    PubMed  Google Scholar 

  45. Coussens LM, Tinkle CL, Hanahan D et al (2000) MMP-9 Supplied by Bone Marrow–Derived Cells Contributes to Skin Carcinogenesis. Cell 103:481-490

    PubMed  CAS  Google Scholar 

  46. Ho T-Y, Bagnell CA (2005) Relaxin Induces Matrix Metalloproteinase-9 through Activation of Nuclear Factor Kappa B in Human THP-1 Cells. Ann NY Acad Sci 1041:314-316

    PubMed  CAS  Google Scholar 

  47. Jintang S, Feng A, Zhang Y et al (2010) Fucoidan increases TNF-α-induced MMP-9 secretion in monocytic cell line U937. Inflamm Res 59:271-276

    Google Scholar 

  48. Chakraborti S, Mandal M, Das S et al (2003) Regulation of matrix metalloproteinases: an overview. Mol Cell Biochem 253:269-285

    PubMed  CAS  Google Scholar 

  49. Ma Z, Shah RC, Chang MJ et al (2004) Coordination of cell signaling, chromatin remodeling, histone modifications, and regulator recruitment in human matrix metalloproteinase 9 gene transcription. Mol Cell Biol 24:5496-5509

    PubMed  CAS  Google Scholar 

  50. Gidday JM, Gasche YG, Copin JC et al (2005) Leukocyte-derived matrix metalloproteinase-9 mediates blood–brain barrier breakdown and is proinflammatory after transient focal cerebral ischemia. Am J Physiol - Heart C 289:558-568

    Google Scholar 

  51. Wang G, Guo Q, Hossain M et al (2009) Bone marrow-derived cells are the major source of MMP-9 contributing to blood–brain barrier dysfunction and infarct formation after ischemic stroke in mice. Brain Res 1294:183-192

    PubMed  CAS  Google Scholar 

  52. Gasche Y, Fuzimura Y, Copin J et al (1999) Early appearance of activated matrix metalloproteinase-9 after focal cerebral ischemia in mice: a possible role in blood–brain barrier dysfunction. J Cerebr Blood F Met 19:1020-1028

    CAS  Google Scholar 

  53. Planas AM, Solé S, Justicia C (2001) Expression and Activation of Matrix Metalloproteinase-2 and −9 in Rat Brain after Transient Focal Cerebral Ischemia. Neurobiol Dis 8:834-846

    PubMed  CAS  Google Scholar 

  54. Romanic AM, White RF, Arleth AJ et al (1998) Matrix Metalloproteinase Expression Increases After Cerebral Focal Ischemia in Rats: Inhibition of Matrix Metalloproteinase-9 Reduces Infarct Size. Stroke 29:1020-1030

    PubMed  CAS  Google Scholar 

  55. Montaner J, Alvarez-Sabin J, Molina C et al (2001) Matrix Metalloproteinase Expression After Human Cardioembolic Stroke: Temporal Profile and Relation to Neurological Impairment. Stroke 32:1759-1766

    PubMed  CAS  Google Scholar 

  56. Rosell A, Ortega-Aznar A, Alvarez-Sabin-J et al (2006) Increased Brain Expression of Matrix Metalloproteinase-9 After Ischemic and Hemorrhagic Human Stroke. Stroke 37:1399-1406

    Google Scholar 

  57. Park K-P, Rossel A, Foerch C et al (2009) Plasma and Brain Matrix Metalloproteinase-9 after acute focal Cerebral Ischemia in rats. Stroke 40:2836-2842

    PubMed  CAS  Google Scholar 

  58. Horstmann S, Kalb P, Koziol J et al (2003) Profiles of Matrix Metalloproteinases, their Inhibitors, and Laminin in Stroke patients: Influence of different therapies. Stroke 34:2165-2170

    PubMed  Google Scholar 

  59. Montaner J, Rovira A, Molina CA et al (2003) Plasmatic level of neuroinflammatory markers predict the extent of diffusion-weighted image lesions in hyperacute stroke. J Cerebr Blood F Met 23:1403-1407

    CAS  Google Scholar 

  60. Castellanos M, Leira R, Serena J et al (2003) Plasma Metalloproteinase-9 concentration predicts hemorrhagic transformation in acute ischemic stroke. Stroke 34:40-46

    PubMed  CAS  Google Scholar 

  61. Montaner J, Alvarez-Sabin J, Molina CA et al (2001) Matrix Metalloproteinase expression is related to hemorrhagic transformation after Cardioembolic Stroke. Stroke 32:2762-2767

    PubMed  CAS  Google Scholar 

  62. Gurney KJ, Estrada EY, Rosenberg GA (2006) Blood–brain barrier disruption by stromelysin-1 facilitates neutrophil infiltration in neuroinflammation. Neurobiol Dis 23:87-96

    PubMed  CAS  Google Scholar 

  63. Sole S, Petegnief V, Gorina R, Chamorro A et al (2004) Activation of matrix metalloproteinase-3 and agrin cleavage in cerebral ischemia/reperfusion. J Neuropathol Exp Neur 63:338-349

    CAS  Google Scholar 

  64. Kontos HA (1985) George E. Brown memorial lecture. Oxygen radicals in cerebral vascular injury. Circul Res 57:508-516

    CAS  Google Scholar 

  65. Siesjo BK, Agardh CD, Bengtsson F (1989) Free radicals and brain damage. Cerebrovasc Brain Metab Rev 1:165-211

    PubMed  CAS  Google Scholar 

  66. Chan PH (1994) Oxygen radicals in focal cerebral ischemia. Brain Pathol 4(1):59-65

    PubMed  CAS  Google Scholar 

  67. Boveris A & Chance B (1973) The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J 134(3):707-716

    PubMed  CAS  Google Scholar 

  68. Koh J, Choi D (1988) Vulnerability of cultured cortical neurons to damage by excitotoxins: differential susceptibility of neurons containing NADPH-diaphorase. J Neurosci 8:2153-2163

    PubMed  CAS  Google Scholar 

  69. Iadecola C (1997) Bright and dark sides of nitric oxide in ischemic brain injury. Trends Neurosci 20:132-139

    PubMed  CAS  Google Scholar 

  70. Zhang ZG, Chopp M, Zaloga C et al (1993) Cerebral endothelial nitric oxide synthase expression after focal cerebral ischemia in rats. Stroke 24:2016-2021

    PubMed  CAS  Google Scholar 

  71. Beasley TC, Bari F, Thore C et al (1998) Cerebral ischemia/reperfusion increases endothelial nitric oxide synthase levels by an indomethacin-sensitive mechanism. J Cerebr Blood F Met 18:88-96

    CAS  Google Scholar 

  72. Xu J, HE L, Ahmed S H et al (2000) Oxygen-Glucose Deprivation Induces Inducible Nitric Oxide Synthase and Nitrotyrosine Expression in Cerebral Endothelial Cells. Stroke 31:1744-1751

    Google Scholar 

  73. Nogawa S, Forster C, Zhang F et al (1998) Interaction between inducible nitric oxide synthase and cyclooxygenase-2 after cerebral ischemia. Proc Natl Acad Sci 95:10966-10971

    PubMed  CAS  Google Scholar 

  74. Chan PH (2001) Reactive oxygen radicals in signaling and damage in the ischemic brain. J Cerebr Blood F Met 21:2-14

    CAS  Google Scholar 

  75. Noshita N, Sugawara T, Fujimura M et al (2001) Manganese Superoxide Dismutase Affects Cytochrome c Release and Caspase-9 Activation After Transient Focal Cerebral Ischemia in Mice. J Cerebr Blood F Met 21:557-567

    CAS  Google Scholar 

  76. Xanthoudakis S, Miao G, Wang F et al (1992) Redox activation of Fos-Jun DNA binding activity is mediated by a DNA repair enzyme. Embo J 11:3323-3335

    PubMed  CAS  Google Scholar 

  77. Bennett RAO, Wilson DM, Wong D et al (1997) Interaction of human apurinic endonuclease and DNA polymerase β in the base excision repair pathway. Proc Natl Acad Sci 94:7166-7169

    PubMed  CAS  Google Scholar 

  78. Robertson KA, Hill DP , Xu Y et al (1997) Down-regulation of apurinic/apyrimidinic endonuclease expression is associated with the induction of apoptosis in differentiating myeloid leukemia cells. Cell Growth Differ 8:443-449

    PubMed  CAS  Google Scholar 

  79. Edwards M, Kent TA, Rea HC et al (1998) APE/Ref-1 responses to ischemia in rat brain. Neuroreport 9:4015-4018

    PubMed  CAS  Google Scholar 

  80. Kawase M, Fujimura M, Morita-Fujimura Y et al (1999) Reduction of Apurinic/Apyrimidinic Endonuclease Expression After Transient Global Cerebral Ischemia in Rats: Implication of the Failure of DNA Repair in Neuronal Apoptosis. Stroke 30:441-449

    PubMed  CAS  Google Scholar 

  81. Fujimura M, Morita-Fuzimura Y, Narasimhan P et al (1999) Copper-Zinc Superoxide Dismutase Prevents the Early Decrease of Apurinic/Apyrimidinic Endonuclease and Subsequent DNA Fragmentation After Transient Focal Cerebral Ischemia in Mice. Stroke 30:2408-2415

    PubMed  CAS  Google Scholar 

  82. Sen CK (1998) Redox Signaling and the Emerging Therapeutic Potential of Thiol Antioxidants. Biochem Pharmacol 55:1747-1758

    PubMed  CAS  Google Scholar 

  83. Dalton TP, Shertzer HG, Puga A (1999) Regulation of gene expression by reactive oxygen. Annu Rev Pharmacol 39:67-101

    CAS  Google Scholar 

  84. Yu Z, Zhou D, Bruce-Keller AJ, Kindy MS et al (1999) Lack of the p50 Subunit of Nuclear Factor-κB Increases the Vulnerability of Hippocampal Neurons to Excitotoxic Injury. J Neurosci 19:8856-8865

    PubMed  CAS  Google Scholar 

  85. Kuo PC, Abe K, Schroeder RA (2000) Superoxide enhances interleukin 1beta-mediated transcription of the hepatocyte-inducible nitric oxide synthase gene. Gastroenterol Jpn 118:608-618

    CAS  Google Scholar 

  86. Morita-Fujimura Y, Fujimura M, Kawase M et al (1999) Early decrease in apurinic/apyrimidinic endonuclease is followed by DNA fragmentation after cold injury-induced brain trauma in mice. J Neurosci 93:1465-1473

    CAS  Google Scholar 

  87. Morita-Fujimura Y, Fujimura M, Gasche Y et al (2000) Overexpression of copper and zinc superoxide dismutase in transgenic mice prevents the induction and activation of matrix metalloproteinases after cold injury-induced brain trauma. J Cerebr Blood F Met 20:130-138

    CAS  Google Scholar 

  88. Yrjanheikki J, Chan PH (2000) Spreading depression-induced expression of c-fos and cyclooxygenase-2 in transgenic mice that overexpress human copper/zinc-superoxide dismutase. J Neurotraum 17:713-718

    CAS  Google Scholar 

  89. Carden DL, Granger DN (2000) Pathophysiology of ischaemia–reperfusion injury. J Pathol 190:255-266

    PubMed  CAS  Google Scholar 

  90. Bolli R, Jeroudi MO, Patel B S et al (1989) Direct evidence that oxygen-derived free radicals contribute to postischemic myocardial dysfunction in the intact dog. Proc Natl Acad Sci 86:4695-4699

    PubMed  CAS  Google Scholar 

  91. Marklund SL (1982) Human copper-containing superoxide dismutase of high molecular weight. Proc Natl Acad Sci 79:7634-7638

    PubMed  CAS  Google Scholar 

  92. He YY, Hsu CY, Ezrin AM et al (1993) Polyethylene glycol-conjugated superoxide dismutase in focal cerebral ischemia-reperfusion. Am J Physiol. 265:252-256

    Google Scholar 

  93. Chan PH, Epstein CJ, Li Y et al (1994) SOD-1 Transgenic Mice as a Model for Studies of Neuroprotection in Stroke and Brain Trauma. Ann N Y Acad Sci 738:93-103

    PubMed  CAS  Google Scholar 

  94. Imaizumi S, Woolworth V, Fishman RA et al (1990) Liposome-entrapped superoxide dismutase reduces cerebral infarction in cerebral ischemia in rats. Stroke 21:1312-1317

    PubMed  CAS  Google Scholar 

  95. Chan PH, Longar S, Fishman RA (1987) Protective effects of liposome-entrapped superoxide dismutase on posttraumatic brain edema. Ann Neurol 21:540-547

    PubMed  CAS  Google Scholar 

  96. Epstein CJ, Avraham KV, Lovett M et al (1987) Transgenic mice with increased Cu/Zn-superoxide dismutase activity: animal model of dosage effects in Down syndrome. Proc Natl Acad Sci 84:8044-8048

    PubMed  CAS  Google Scholar 

  97. Havsteen B (1983) Flavonoids, a class of natural products of high pharmacological potency. Biochem Pharmacol 32:1141-1148

    PubMed  CAS  Google Scholar 

  98. Geetha T, Malhotra V, Chopra K et al (2005) Antimutagenic and antioxidant/prooxidant activity of quercetin. Ind J Exp Biol 43:61-67

    CAS  Google Scholar 

  99. Coleridge Smith PD, Thomas P et al (1988) Causes of venous ulceration: a new hypothesis. Br Med J (Clin Res Ed) 296:1726-1727

    CAS  Google Scholar 

  100. Chakraborty S, Sami S, Das N et al (2012) The use of nano-quercetin to arrest mitochondrial damage and MMP-9 upregulation during prevention of gastric inflammation induced by ethanol in rat. Biomaterials 33:2991-3001

    PubMed  CAS  Google Scholar 

  101. Heo HJ, Lee CY (2004) Protective Effects of Quercetin and Vitamin C against Oxidative Stress-Induced Neurodegeneration. J Agric Food Chem 52:7514-7517

    PubMed  CAS  Google Scholar 

  102. Pace-Asciak CR, Hahn S, Diamandis EP et al (1995) The red wine phenolics trans-resveratrol and quercetin block human platelet aggregation and eicosanoid synthesis: Implications for protection against coronary heart disease. Clin Chim Acta 235:207-219

    PubMed  CAS  Google Scholar 

  103. Huk I, Brokovich V, Villi J N et al (1998) Bioflavonoid quercetin scavenges superoxide and increases nitric oxide concentration in ischaemia–reperfusion injury: an experimental study. Br J Surg 85:1080-1085

    PubMed  CAS  Google Scholar 

  104. Ahlemeyer B, Krieglstein J (2003) Pharmacological studies supporting the therapeutic use of Ginkgo biloba extract for Alzheimer’s disease. Pharmacopsychiatry 36:8-14

    Google Scholar 

  105. Chandrasekaran K, Mehrabian Z, Spinnewyn B et al (2003) Neuroprotective effects of bilobalide, a component of Ginkgo biloba extract (EGb 761) in global brain ischemia and in excitotoxicity-induced neuronal death. Pharmacopsychiat. 36:89-94

    Google Scholar 

  106. Chung SY, Wang MF, Lin JY et al (2003) Effect of one week treatment with Ginkgo biloba extract (EGb761) on ischemia-induced infarct volume in gerbils. Am J Chin Med 31:533-542

    PubMed  CAS  Google Scholar 

  107. Donato G, Volpentesta G, Lavano A et al (2003) Effects of Ginko Biloba and caspase inhibitors on brain ischemia in the Mongolian Gerbil. J Neurosurg Sci 47:149-155

    PubMed  CAS  Google Scholar 

  108. Ovbiagele B, Kidwell CS, Starkman S et al (2003) Potential Role of Neuroprotective Agents in the Treatment of Patients with Acute Ischemic Stroke. Curr Treat Options Cardiovasc Med 5:441-449

    PubMed  Google Scholar 

  109. Hatcher JF, Dempsey RJ (2002) Citicoline: neuroprotective mechanisms in cerebral ischemia. J Neurochem 80:12-23

    PubMed  Google Scholar 

  110. Secades JJ, Lorenzo JL (2006) Citicoline: pharmacological and clinical review, 2006 update. Methods Find Exp Clin Pharmacol 28 :1-56

    PubMed  CAS  Google Scholar 

  111. Mandal AK, Das S, Basu MK et al (2007) Hepatoprotective Activity of Liposomal Flavonoid against Arsenite-Induced Liver Fibrosis. J Pharmacol Exp Ther 320:994-1001

    PubMed  CAS  Google Scholar 

  112. Forsman M, Fleischer JE, Milde JH et al (1988) Superoxide dismutase and catalase failed to improve neurologic outcome after complete cerebral ischemia in the dog. Acta Anaesthesiol Scand 32:152-155

    PubMed  CAS  Google Scholar 

  113. Fresta M, Puglisi G (1997) Survivalrate improvement in a rat ischemia model by long circulating liposomes containing cytidine-5′-diphosphate choline. Life Sci 61:1227-1235

    PubMed  CAS  Google Scholar 

  114. Regnier-Vigouroux A (2003) The mannose receptor in the brain. Int Rev Cytol 226:321-342

    PubMed  CAS  Google Scholar 

  115. Galea I, Palin K, Newman TA et al (2005) Mannose receptor expression specifically reveals perivascular macrophages in normal, injured, and diseased mouse brain. Glia 49:375-384

    PubMed  Google Scholar 

  116. Irache JM, Salman HH, Gamazo C et al (2008) Mannose-targeted systems for the delivery of therapeutics. Expert Opin Drug Deliv 5:703-724

    PubMed  CAS  Google Scholar 

  117. Umezawa F, Eto Y (1988) Liposome targeting to mouse brain: Mannose as a recognition marker. Biochem Biophys Res Commun 153:1038-1044

    PubMed  CAS  Google Scholar 

  118. Fresta M, Puglisi G (1999) Reduction of maturation phenomenon in cerebral ischemia with CDP-choline-loaded liposomes. Pharm Res 16:1843-1849

    PubMed  CAS  Google Scholar 

  119. Das S , Mandal AK, Ghosh A et al (2008) Nanoparticulated quercetin in combating age related cerebral oxidative injury. Curr Aging Sci 1:169-174

    PubMed  CAS  Google Scholar 

  120. Stamenkovic I (2003) Extracellular matrix remodelling: the role of matrix metalloproteinases. J Pathol 200:448-464

    PubMed  CAS  Google Scholar 

  121. Lu P, Weaver VM, Werb Z (2012) The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol 196:395-406

    PubMed  CAS  Google Scholar 

  122. Whittaker CA, Bergeron KF, Whittle J et al (2006) The echinoderm adhesome. Dev Biol 300:252-266

    PubMed  CAS  Google Scholar 

  123. Özbek S, Balasubramanian PG, Chiquet-Ehrismann R et al (2010) The Evolution of Extracellular Matrix. Mol Biol Cell 21:4300-4305

    PubMed  Google Scholar 

  124. Rohrbach DH, Timpl R (eds) (1993) Molecular and cellular aspects of basement membranes (Academic Press) San Diego, CA, 49–66

    Google Scholar 

  125. Egeblad M, Rasch MG, Weaver VM (2010) Dynamic interplay between the collagen scaffold and tumor evolution. Curr Opin Cell Biol 22:697-7

    PubMed  CAS  Google Scholar 

  126. Godenschwege TA, Pohar N, Buchner S et al (2000) Inflated wings, tissue autolysis and early death in tissue inhibitor of metalloproteinases mutants of Drosophila. Eur J Cell Biol 79:495-501

    PubMed  CAS  Google Scholar 

  127. Jones FS, Jones PL (2000) The tenascin family of ECM glycoproteins: Structure, function, and regulation during embryonic development and tissue remodeling. Dev Dyn 218:235-259

    PubMed  CAS  Google Scholar 

  128. Rauch U, Feng K, Zhou XH (2001) Neurocan: a brain chondroitin sulfate proteoglycan. Cell Mol Life Sci 58:1842-1856

    PubMed  CAS  Google Scholar 

  129. McDonald J, Hascall VC (2002) Hyaluronan Minireview Series. J Biol Chem 277:4575-4579

    PubMed  CAS  Google Scholar 

  130. Knudson W (1996) Tumor-associated hyaluronan. Providing an extracellular matrix that facilitates invasion. Am J Pathol 148:1721-1726

    PubMed  CAS  Google Scholar 

  131. Termeer C, Sleeman JP, Simon JC (2003) Hyaluronan – magic glue for the regulation of the immune response? Trends Immunol 24:112-114

    PubMed  CAS  Google Scholar 

  132. Fitch MT, Silver J (1997) Activated Macrophages and the Blood–Brain Barrier: Inflammation after CNS Injury Leads to Increases in Putative Inhibitory Molecules. Exp Neurol 148:587-603

    PubMed  CAS  Google Scholar 

  133. Davies SJ, Fitch MT, Memberg SP et al (1997) Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390:680-683

    PubMed  CAS  Google Scholar 

  134. Hirakawa S, Oohashi T, Su W-D et al (2000) The Brain Link Protein-1 (BRAL1): cDNA Cloning, Genomic Structure, and Characterization as a Novel Link Protein Expressed in Adult Brain. Biochem Biophys Res Commun 276:982-989

    PubMed  CAS  Google Scholar 

  135. Milev P, Maurel P, Chiba A et al (1998) Differential Regulation of Expression of Hyaluronan-Binding Proteoglycans in Developing Brain: Aggrecan, Versican, Neurocan, and Brevican. Biochem Biophys Res Commun 247:207-212

    PubMed  CAS  Google Scholar 

  136. Margolis RU, Margolis RK, Chang LB et al (1975) Glycosaminoglycans of brain during development. Biochemistry 14:85-88

    PubMed  CAS  Google Scholar 

  137. Yamaguchi Y (1996) Brevican: a major proteoglycan in adult brain. Perspect Dev Neurobiol 3:307-317

    PubMed  CAS  Google Scholar 

  138. Schmalfeldt M, Dours-Zimmermann MaT, Winterhalter KH et al (1998) Versican V2 Is a Major Extracellular Matrix Component of the Mature Bovine Brain. J Biol Chem 273:15758-15764

    Google Scholar 

  139. Pesheva P, Spiess E, Schachner M (1989) J1-160 and J1-180 are oligodendrocyte-secreted nonpermissive substrates for cell adhesion. J Cell Biol 109:1765-1778

    PubMed  CAS  Google Scholar 

  140. Rauch U, Gao P, Janetzko A et al (1991) Isolation and characterization of developmentally regulated chondroitin sulfate and chondroitin/keratan sulfate proteoglycans of brain identified with monoclonal antibodies. J Biol Chem 266:14785-14801

    PubMed  CAS  Google Scholar 

  141. Dörries U, Schachner M (1994) Tenascin mRNA isoforms in the developing mouse brain. J Neurosci Res 37:336-347

    PubMed  Google Scholar 

  142. Tomimatsu Y, Idemoto S, Moriguchi S et al (2002) Proteases involved in long-term potentiation. Life Sci 72:355-361

    PubMed  CAS  Google Scholar 

  143. Indyk JA, Chen ZL, Tsirka SE et al (2003) Laminin chain expression suggests that laminin-10 is a major isoform in the mouse hippocampus and is degraded by the tissue plasminogen activator/plasmin protease cascade during excitotoxic injury. Neurosci 116:359-371

    CAS  Google Scholar 

  144. Matthews RT, Gary SC, Zerillo C et al (2000) Brain-enriched Hyaluronan Binding (BEHAB)/Brevican Cleavage in a Glioma Cell Line Is Mediated by a Disintegrin and Metalloproteinase with Thrombospondin Motifs (ADAMTS) Family Member. J Biol Chem 275:22695-22703

    PubMed  CAS  Google Scholar 

  145. Westling J, Gottschall PE, Thompson V P et al (2004) ADAMTS4 (aggrecanase-1) cleaves human brain versican V2 at Glu405-Gln406 to generate glial hyaluronate binding protein. Biochem J 377:787-795

    PubMed  CAS  Google Scholar 

  146. Satoh K, Suzuki N, Yokota H (2000) ADAMTS-4 (a disintegrin and metalloproteinase with thrombospondin motifs) is transcriptionally induced in beta-amyloid treated rat astrocytes. Neurosci Lett 289:177-180

    PubMed  CAS  Google Scholar 

  147. Sandy JD, Westling J, Kenagy RD et al (2001) Versican V1 Proteolysis in Human Aorta in Vivo Occurs at the Glu441-Ala442 Bond, a Site That Is Cleaved by Recombinant ADAMTS-1 and ADAMTS-4. J Biol Chem 276:13372-13378

    PubMed  CAS  Google Scholar 

  148. Lee S-R, Tsuji K, Lee S-R et al (2004) Role of Matrix Metalloproteinases in delayed neuronal damage after transient global cerebral ischemia. J Neurosci 24:671-678

    PubMed  CAS  Google Scholar 

  149. Lu A, Tang Y, Ran R et al (2003) Genomics of the periinfarction cortex after focal cerebral ischemia. J Cereb Blood Flow Metab 23:786-810

    PubMed  CAS  Google Scholar 

  150. Nicholson C, Syková E (1998) Extracellular space structure revealed by diffusion analysis. Trends Neurosci 21:207-215

    PubMed  CAS  Google Scholar 

  151. Novak U, Kaye AH (2000) Extracellular matrix and the brain: components and function. J Clin Neurosci 7:280-290

    PubMed  CAS  Google Scholar 

  152. Mörgelin M, Heinegård D, Engel J et al (1994) The cartilage proteoglycan aggregate: assembly through combined protein—carbohydrate and protein—protein interactions. Biophys Chem 50:113-128

    PubMed  Google Scholar 

  153. Yamaguchi Y (2000) Lecticans: organizers of the brain extracellular matrix. Cell Mol Life Sci 57:276-289

    PubMed  CAS  Google Scholar 

  154. Bandtlow CE, Zimmermann DR (2000) Proteoglycans in the Developing Brain: New Conceptual Insights for Old Proteins. Physiol Rev 80:1267-1290

    PubMed  CAS  Google Scholar 

  155. Miura R, Aspberg A, Ethell IM et al (1999) The Proteoglycan Lectin Domain Binds Sulfated Cell Surface Glycolipids and Promotes Cell Adhesion. J Biol Chem 274:11431-11438

    PubMed  CAS  Google Scholar 

  156. Olin AI, Morgelin M, Sasaki T et al (2001) The Proteoglycans Aggrecan and Versican Form Networks with Fibulin-2 through Their Lectin Domain Binding. J Biol Chem 276:1253-1261

    PubMed  CAS  Google Scholar 

  157. Rauch U, Clement A, Retzler C et al (1997) Mapping of a Defined Neurocan Binding Site to Distinct Domains of Tenascin-C. J Biol Chem 272:26905-26912

    PubMed  CAS  Google Scholar 

  158. Aspberg A, Miura R, Bourdoulous S et al (1997) The C-type lectin domains of lecticans, a family of aggregating chondroitin sulfate proteoglycans, bind tenascin-R by protein– protein interactions independent of carbohydrate moiety. Proc Natl Acad Sci 94:10116-10121

    PubMed  CAS  Google Scholar 

  159. Day JM, Olin AI, Murdoch AD et al (2004) Alternative Splicing in the Aggrecan G3 Domain Influences Binding Interactions with Tenascin-C and Other Extracellular Matrix Proteins. J Biol Chem 279:12511-12518

    PubMed  CAS  Google Scholar 

  160. Chodobsky A, Zink B J, Chodobska J S (2011) Blood–brain barrier pathophysiology in traumatic brain injury. Transl Stroke Res 2: 492-516

    Google Scholar 

  161. Löffek S, Schilling O, Franzke C-W (2011) Biological role of matrix metalloproteinases: a critical balance. Eur Resp J 38:191-208

    Google Scholar 

  162. Jana S, Rudra DS, Paul S et al (2012) Curcumin delays endometriosis development by inhibiting MMP-2 activity. Indian J Biochem Biophys 49:342-348

    PubMed  CAS  Google Scholar 

  163. Ganguly K, Kundu P, Banerjee A et al (2006) Hydrogen peroxide-mediated downregulation of matrix metalloprotease-2 in indomethacin-induced acute gastric ulceration is blocked by melatonin and other antioxidants. Free Radic Biol Med 41:911-925

    PubMed  CAS  Google Scholar 

  164. Rosenberg GA, Estrada EY, Dencoff JE (1998) Matrix Metalloproteinases and TIMPs Are Associated With Blood–brain Barrier Opening After Reperfusion in Rat Brain. Stroke 29:2189-2195

    PubMed  CAS  Google Scholar 

  165. Visse R, Nagase H (2003) Matrix Metalloproteinases and Tissue Inhibitors of Metalloproteinases: Structure, Function, and Biochemistry. Circ Res 92:827-839

    PubMed  CAS  Google Scholar 

  166. Swarnakar S, Mishra A, Chaudhuri SR (2012) The gelatinases and their inhibitors: the structure-activity relationships. EXS 103:57-82

    PubMed  CAS  Google Scholar 

  167. Axisa B, Loftus I M, Naylor AR et al (2002) Prospective, Randomized, Double-Blind Trial Investigating the Effect of Doxycycline on Matrix Metalloproteinase Expression Within Atherosclerotic Carotid Plaques. Stroke 33:2858-2864

    PubMed  CAS  Google Scholar 

  168. Morgan AR, Rerkasem K, Gallagher PJ et al (2004) Differences in Matrix Metalloproteinase-1 and Matrix Metalloproteinase-12 Transcript Levels Among Carotid Atherosclerotic Plaques With Different Histopathological Characteristics. Stroke 35:1310-1315

    PubMed  CAS  Google Scholar 

  169. Mun-Bryce S, Rosenberg GA (1998) Matrix metalloproteinases in cerebrovascular disease. J Cereb Blood Flow Metab 18:1163-1172

    PubMed  CAS  Google Scholar 

  170. Molloy KJ, Thompson MM, Jones JL et al (2004) Unstable Carotid Plaques Exhibit Raised Matrix Metalloproteinase-8 Activity. Circulation 110:337-343

    PubMed  CAS  Google Scholar 

  171. Heo JH, Kim SH, Lee KY et al (2003) Increase in Plasma Matrix Metalloproteinase-9 in Acute Stroke Patients With Thrombolysis Failure. Stroke 34:48-e50

    Google Scholar 

  172. Cuzner ML, Gveric D, Strand C et al (1996) The expression of tissue-type plasminogen activator, matrix metalloproteases and endogenous inhibitors in the central nervous system in multiple sclerosis: comparison of stages in lesion evolution. J Neuropathol Exp Neurol 55:1194-1204

    PubMed  CAS  Google Scholar 

  173. Fukuda S, Fini CA, Mabuchi T et al (2004) Focal Cerebral Ischemia Induces Active Proteases That Degrade Microvascular Matrix. Stroke 35:998-1004

    PubMed  CAS  Google Scholar 

  174. Pfefferkorn T, Rosenberg GA (2003) Closure of the Blood–brain Barrier by Matrix Metalloproteinase Inhibition Reduces rtPA-Mediated Mortality in Cerebral Ischemia With Delayed Reperfusion. Stroke 34:2025-2030

    PubMed  Google Scholar 

  175. Eldrup N, Grønholdt M-LM, Sillesen H et al (2006) Elevated Matrix Metalloproteinase-9 Associated With Stroke or Cardiovascular Death in Patients With Carotid Stenosis. Circulation 114:1847-1854

    PubMed  CAS  Google Scholar 

  176. Zalewska T, Ziemka-Nalecz M, Sarnowska A et al (2002) Involvement of MMPs in delayed neuronal death after global ischemia. Acta Neurobiol Exp (Wars) 62(2):53-61

    Google Scholar 

  177. Hashimoto T, Wen G, Lawton MT et al (2003) Abnormal Expression of Matrix Metalloproteinases and Tissue Inhibitors of Metalloproteinases in Brain Arteriovenous Malformations. Stroke 34:925-931

    PubMed  CAS  Google Scholar 

  178. Lapchak PA, Chapman DF, Zivin JA (2000) Metalloproteinase Inhibition Reduces Thrombolytic (Tissue Plasminogen Activator)–Induced Hemorrhage After Thromboembolic Stroke. Stroke 31:3034-3040

    PubMed  CAS  Google Scholar 

  179. Montaner J, Molina CA, Monasterio J et al (2003) Matrix Metalloproteinase-9 Pretreatment Level Predicts Intracranial Hemorrhagic Complications After Thrombolysis in Human Stroke. Circulation 107:598-603

    PubMed  CAS  Google Scholar 

  180. Singh LP, Mishra A, Saha D et al (2011) Doxycycline blocks gastric ulcer by regulating matrix metalloproteinase-2 activity and oxidative stress. World J Gastroenterol 17:3310-3321

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Sibani Sarkar and Somnath Chatterjee contributed equally to the manuscript. Sibani Sarkar is the recipient of woman scientist award from DST, India. Prof. Siddhartha Roy, the Director of the CSIR-IICB, Kolkata, is acknowledged for providing all the supports. Authors are also thankful to Mr. Sayantan Jana for his unconditional help in the preparation of the figures.

Author information

Authors and Affiliations

  1. Drug Development Diagnostics and Biotechnology Division, CSIR – Indian Institute of Chemical Biology, 4, Raja S.C. Mullick Road, Jadavpur, Kolkata, 700032, West Bengal, India

    Sibani Sarkar, Somnath Chatterjee & Snehasikta Swarnakar

Authors
  1. Sibani Sarkar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Somnath Chatterjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Snehasikta Swarnakar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Snehasikta Swarnakar .

Editor information

Editors and Affiliations

  1. St. Boniface Hosp. Research, Univ. of Ma Institute of Cardiovascular Sciences, Winnipeg, Manitoba, Canada

    Naranjan S. Dhalla

  2. Dept of Biochemistry and Biophysics, University of Kalyani, Kalyani, West Bengal, India

    Sajal Chakraborti

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Sarkar, S., Chatterjee, S., Swarnakar, S. (2014). Matrix Metalloproteinases in Ischemia–Reperfusion Injury in Brain: Antioxidants as Rescuer. In: Dhalla, N., Chakraborti, S. (eds) Role of Proteases in Cellular Dysfunction. Advances in Biochemistry in Health and Disease, vol 8. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-9099-9_4

Download citation

Publish with us

Policies and ethics

Search

Navigation