Caspase-3 contributes to ZO-1 and Cl-5 Tight-junction disruption in rapid anoxic neurovascular unit damage

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Zehendner, Christoph M ^a   Librizzi, Laura ^b   de Curtis, Marco ^b   Kuhlmann, Christoph R W ^a   Luhmann, Heiko J ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b DEPARTMENT OF NEUROSURGERY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLASPARTYLGLUTAMYLVALYLASPARTYL FLUOROMETHYL KETONE; CASPASE 3; CASPASE 3 INHIBITOR; GLUCOSE; MEMBRANE PROTEIN; OXYGEN; PROTEIN CL5; PROTEIN ZO1; UNCLASSIFIED DRUG; CLAUDIN; PHOSPHOPROTEIN; ZONULA OCCLUDENS-1 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ANOXIA; ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; BRAIN ISCHEMIA; CONTROLLED STUDY; DNA FRAGMENTATION; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; ENZYME ACTIVATION; GUINEA PIG; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; METHODOLOGY; MIDDLE CEREBRAL ARTERY OCCLUSION; NICK END LABELING; NONHUMAN; PROTEIN DEGRADATION; TIGHT JUNCTION; ANIMAL; BRAIN HYPOXIA; CAPILLARY PERMEABILITY; CELL CULTURE; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; PROTEIN TRANSPORT; TIME;

CAVIA;

ANIMALS; BLOOD-BRAIN BARRIER; CAPILLARY PERMEABILITY; CASPASE 3; CELLS, CULTURED; CLAUDINS; ENDOTHELIAL CELLS; GUINEA PIGS; HYPOXIA, BRAIN; MEMBRANE PROTEINS; MICE; PHOSPHOPROTEINS; PROTEIN TRANSPORT; TIGHT JUNCTIONS; TIME FACTORS;

EID: 79952056317     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016760     Document Type: Article

References (47)

1. Zlokovic BV, (2008) The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57: 178-201.
2. Ballabh P, Braun A, Nedergaard M, (2004) The blood-brain barrier: an overview- Structure, regulation, and clinical implications. Neurobiology of Disease 16: 1-13.
3. Rosenberg GA, Yang Y, (2007) Vasogenic edema due to tight junction disruption by matrix metalloproteinases in cerebral ischemia. Neurosurg Focus 22: E4.
4. Shichita T, Sugiyama Y, Ooboshi H, Sugimori H, Nakagawa R, et al. (2009) Pivotal role of cerebral interleukin-17-producing gamma delta T cells in the delayed phase of ischemic brain injury. Nature Medicine 15: 946-950.
5. Koto T, Takubo K, Ishida S, Shinoda H, Inoue M, et al. (2007) Hypoxia disrupts the barrier function of neural blood vessels through changes in the expression of claudin-5 in endothelial cells. American Journal of Pathology 170: 1389-1397.
6. Yang Y, Estrada EY, Thompson JF, Liu W, Rosenberg GA, (2007) 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 27: 697-709.
7. Chen J, Nagayama T, Jin KL, Stetler RA, Zhu RL, et al. (1998) Induction of caspase-3-like protease may mediate delayed neuronal death in the hippocampus after transient cerebral ischemia. Journal of Neuroscience 18: 4914-4928.
8. Hara H, Friedlander RM, Gagliardini V, Ayata C, Fink K, et al. (1997) Inhibition of interleukin 1 beta converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage. Proceedings of the National Academy of Sciences of the United States of America 94: 2007-2012.
9. Karatas H, Aktas Y, Gursoy-Ozdemir Y, Bodur E, Yemisci M, et al. (2009) A Nanomedicine Transports a Peptide Caspase-3 Inhibitor across the Blood-Brain Barrier and Provides Neuroprotection. Journal of Neuroscience 29: 13761-13769.
10. Li H, Colbourne F, Sun P, Zhao ZH, Buchan AM, (2000) Caspase inhibitors reduce neuronal injury after focal but not global cerebral ischemia in rats. Stroke 31: 176-181.
11. Lee SR, Lo EH, (2004) Induction of caspase-mediated cell death by matrix metalloproteinases in cerebral endothelial cells after hypoxia-reoxygenation. J Cereb Blood Flow Metab 24: 720-727.
12. Rosell A, Cuadrado E, Alvarez-Sabin J, Hernandez-Guillamon M, Delgado P, et al. (2008) Caspase-3 is related to infarct growth after human ischemic stroke. Neuroscience Letters 430: 1-6.
13. Lampl Y, Boaz M, Gilad R, Lorberboym M, Dabby R, et al. (2007) Minocycline treatment in acute stroke: an open-label, evaluator-blinded study. Neurology 69: 1404-1410.
14. Chen M, Ona VO, Li MW, Ferrante RJ, Fink KB, et al. (2000) Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nature Medicine 6: 797-801.
15. Zehendner CM, Luhmann HJ, Kuhlmann CR, (2009) Studying the neurovascular unit: an improved blood-brain barrier model. J Cereb Blood Flow Metab 29: 1879-1884.
16. Mark KS, Davis TP, (2002) Cerebral microvascular changes in permeability and tight junctions induced by hypoxia-reoxygenation. Am J Physiol Heart Circ Physiol 282: H1485-H1494.
17. Simard JM, Kent TA, Chen M, Tarasov KV, Gerzanich V, (2007) Brain oedema in focal ischaemia: molecular pathophysiology and theoretical implications. Lancet Neurol 6: 258-268.
18. Muhlethaler M, de Curtis M, Walton K, Llinas R, (1993) The isolated and perfused brain of the guinea-pig in vitro. Eur J Neurosci 5: 915-926.
19. Deli MA, Abraham CS, Kataoka Y, Niwa M, (2005) Permeability studies on in vitro blood-brain barrier models: physiology, pathology, and pharmacology. Cell Mol Neurobiol 25: 59-127.
20. Brillault J, Berezowski V, Cecchelli R, Dehouck MP, (2002) Intercommunications between brain capillary endothelial cells and glial cells increase the transcellular permeability of the blood-brain barrier during ischaemia. J Neurochem 83: 807-817.
21. de Curtis M, Biella G, Buccellati C, Folco G, (1998) Simultaneous investigation of the neuronal and vascular compartments in the guinea pig brain isolated in vitro. Brain Res Brain Res Protoc 3: 221-228.
22. Llinas R, Yarom Y, Sugimori M, (1981) Isolated Mammalian Brain Invitro- New Technique for Analysis of Electrical-Activity of Neuronal Circuit Function. Federation Proceedings 40: 2240-2245.
23. Marin-Teva JL, Dusart I, Colin C, Gervais A, van Rooijen N, et al. (2004) Microglia promote the death of developing Purkinje cells. Neuron 41: 535-547.
24. Wang ZY, Shen LJ, Tu L, Hu DN, Liu GY, et al. (2009) Erythropoietin protects retinal pigment epithelial cells from oxidative damage. Free Radic Biol Med 46: 1032-1041.
25. Bauer AT, Burgers HF, Rabie T, Marti HH, (2009) Matrix metalloproteinase-9 mediates hypoxia-induced vascular leakage in the brain via tight junction rearrangement. J Cereb Blood Flow Metab 30: 837-848.
26. Brown RC, Morris AP, O'Neil RG, (2007) Tight junction protein expression and barrier properties of immortalized mouse brain microvessel endothelial cells. Brain Research 1130: 17-30.
27. Bendfeldt K, Radojevic V, Kapfhammer J, Nitsch C, (2007) Basic fibroblast growth factor modulates density of blood vessels and preserves tight junctions in organotypic cortical cultures of mice: a new in vitro model of the blood-brain barrier. J Neurosci 27: 3260-3267.
28. Springer JE, Azbill RD, Knapp PE, (1999) Activation of the caspase-3 apoptotic cascade in traumatic spinal cord injury. Nat Med 5: 943-946.
29. Jin R, Yang G, Li G, (2010) Molecular insights and therapeutic targets for blood-brain barrier disruption in ischemic stroke: critical role of matrix metalloproteinases and tissue-type plasminogen activator. Neurobiol Dis 38: 376-385.
30. Kitagawa K, Matsumoto M, Niinobe M, Mikoshiba K, Hata R, et al. (1989) Microtubule-associated protein 2 as a sensitive marker for cerebral ischemic damage-immunohistochemical investigation of dendritic damage. Neuroscience 31: 401-411.
31. Pastori C, Regondi MC, Librizzi L, de Curtis M, (2007) Early excitability changes in a novel acute model of transient focal ischemia and reperfusion in the in vitro isolated guinea pig brain. Experimental Neurology 204: 95-105.
32. Hotchkiss RS, Strasser A, McDunn JE, Swanson PE, (2009) Cell death. N Engl J Med 361: 1570-1583.
33. Rosenberg GA, (1999) Ischemic brain edema. Prog Cardiovasc Dis 42: 209-216.
34. Sandoval KE, Witt KA, (2008) Blood-brain barrier tight junction permeability and ischemic stroke. Neurobiol Dis 32: 200-219.
35. Fischer S, Wobben M, Marti HH, Renz D, Schaper W, (2002) Hypoxia-induced hyperpermeability in brain microvessel endothelial cells involves VEGF-mediated changes in the expression of zonula occludens-1. Microvascular Research 63: 70-80.
36. Girouard H, Iadecola C, (2006) Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. Journal of Applied Physiology 100: 328-335.
37. Yenari MA, Xu LJ, Tang XN, Qiao YL, Giffard RG, (2006) Microglia potentiate damage to blood-brain barrier constituents- Improvement by minocycline in vivo and in vitro. Stroke 37: 1087-1093.
38. Gursoy-Ozdemir Y, Qiu JH, Matsuoka N, Bolay H, Bermpohl D, et al. (2004) Cortical spreading depression activates and upregulates MMP-9. Journal of Clinical Investigation 113: 1447-1455.
39. Gerriets T, Walberer M, Ritschel N, Tschernatsch M, Mueller C, et al. (2009) Edema formation in the hyperacute phase of ischemic stroke. Journal of Neurosurgery 111: 1036-1042.
40. Bojarski C, Weiske J, Schoneberg T, Schroder W, Mankertz J, et al. (2004) The specific fates of tight junction proteins in apoptotic epithelial cells. Journal of Cell Science 117: 2097-2107.
41. Kuhlmann CRW, Zehendner CM, Gerigk M, Closhen D, Bender B, et al. (2009) MK801 blocks hypoxic blood-brain-barrier disruption and leukocyte adhesion. Neuroscience Letters 449: 168-172.
42. Dimitrijevic OB, Stamatovic SM, Keep RF, Andjelkovic AV, (2006) Effects of the chemokine CCL2 on blood-brain barrier permeability during ischemia-reperfusion injury. J Cereb Blood Flow Metab 26: 797-810.
43. Kuhlmann CR, Tamaki R, Gamerdinger M, Lessmann V, Behl C, et al. (2007) Inhibition of the myosin light chain kinase prevents hypoxia-induced blood-brain barrier disruption. J Neurochem 102: 501-507.
44. Gavrieli Y, Sherman Y, Bensasson SA, (1992) Identification of Programmed Cell-Death Insitu Via Specific Labeling of Nuclear-Dna Fragmentation. Journal of Cell Biology 119: 493-501.
45. Ousman SS, Tomooka BH, van Noort JM, Wawrousek EF, O'Connor KC, et al. (2007) Protective and therapeutic role for alphaB-crystallin in autoimmune demyelination. Nature 448: 474-479.
46. Garnier P, Prigent-Tessier A, Van Hoecke M, Bertrand N, Demougeot C, et al. (2004) Hypoxia induces caspase-9 and caspase-3 activation without neuronal death in gerbil brains. European Journal of Neuroscience 20: 937-946.
47. D'Amelio M, Cavallucci V, Middei S, Marchetti C, Pacioni S, et al. (2011) Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer's disease. Nature Neuroscience 14: 69-76.