Blood-brain barrier disruption induced by hemoglobin in vivo: Involvement of up-regulation of nitric oxide synthase and peroxynitrite formation

Brain Research

Volumn 1571, Issue , 2014, Pages 25-38

  Ding, Rui ^a   Chen, Yizhao ^a   Yang, Shuo ^b   Deng, Xinqing ^c   Fu, Zhenghao ^a   Feng, Liang ^a   Cai, Yingqian ^a   Du, Mouxuan ^a   Zhou, Yuxi ^a   Tang, Yanping ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b Gaoqing County People's Hospital of Shandong Province   (China)

^c JINAN UNIVERSITY   (China)

Author keywords

Blood brain barrier; Brain edema; Hemoglobin; Intracerebral hemorrhage; Nitric oxide synthase; Peroxynitrite

Indexed keywords

3 NITROTYROSINE; BIOLOGICAL MARKER; CLAUDIN 5; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEMOGLOBIN; INDUCIBLE NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE; PEROXYNITRITE; PROTEIN ZO1; 3-NITROTYROSINE; CLDN5 PROTEIN, RAT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PEROXYNITROUS ACID; TJP1 PROTEIN, RAT; TYROSINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN EDEMA; BRAIN HEMORRHAGE; BRAIN INJURY; BRAIN TISSUE; CAUDATE NUCLEUS; CONTROLLED STUDY; ENZYME LOCALIZATION; EXPERIMENTAL STROKE; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; IN VIVO STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; RAT; UPREGULATION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANALYSIS OF VARIANCE; ANIMAL; BLOOD; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; METABOLISM; MOTOR ACTIVITY; PATHOLOGY; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT; TIME; TOXICITY;

ANALYSIS OF VARIANCE; ANIMALS; BLOOD-BRAIN BARRIER; BRAIN EDEMA; CEREBRAL HEMORRHAGE; CLAUDIN-5; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HEMOGLOBINS; MALE; MOTOR ACTIVITY; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PEROXYNITROUS ACID; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS; TYROSINE; UP-REGULATION; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84903200586     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2014.04.042     Document Type: Article

References (48)

1. N.J. Abbott, A.A. Patabendige, D.E. Dolman, S.R. Yusof, and D.J. Begley Structure and function of the blood-brain barrier Neurobiol. Dis. 37 2010 13 25
2. J. Aronowski, and X. Zhao Molecular pathophysiology of cerebral hemorrhage: secondary brain injury Stroke 42 2011 1781 1786
3. J.S. Balami, and A.M. Buchan Complications of intracerebral haemorrhage Lancet Neurol. 11 2012 101 118
4. T. Barichello, G.D. Fagundes, J.S. Generoso, S.G. Elias, L.R. Simoes, and A.L. Teixeira Pathophysiology of neonatal acute bacterial meningitis J. Med. Microbiol. 62 2013 1781 1789
5. R.R. Bhasin, G. Xi, Y. Hua, R.F. Keep, and J.T. Hoff Experimental intracerebral hemorrhage: effect of lysed erythrocytes on brain edema and blood-brain barrier permeability Acta Neurochir. Suppl. 81 2002 249 251
6. A. Cassina, and R. Radi Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport Arch. Biochem. Biophys. 328 1996 309 316
7. J. Chen, Y. Li, L. Wang, Z. Zhang, D. Lu, M. Lu, and M. Chopp Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats Stroke 32 2001 1005 1011
8. X.M. Chen, H.S. Chen, M.J. Xu, and J.G. Shen Targeting reactive nitrogen species: a promising therapeutic strategy for cerebral ischemia-reperfusion injury Acta Pharmacol. Sin. 34 2013 67 77
9. S. Danjo, Y. Ishihara, M. Watanabe, Y. Nakamura, and K. Itoh Pentylentetrazole-induced loss of blood-brain barrier integrity involves excess nitric oxide generation by neuronal nitric oxide synthase Brain Res. 1530 2013 44 53
10. Y. Deng-Bryant, I.N. Singh, K.M. Carrico, and E.D. Hall Neuroprotective effects of tempol, a catalytic scavenger of peroxynitrite-derived free radicals, in a mouse traumatic brain injury model J. Cereb. Blood Flow Metab. 28 2008 1114 1126
11. W.N. Duran, A.V. Beuve, and F.A. Sanchez Nitric oxide, S-nitrosation, and endothelial permeability IUBMB Life 65 2013 819 826
12. M. Endres, U. Laufs, Z. Huang, T. Nakamura, P. Huang, M.A. Moskowitz, and J.K. Liao Stroke protection by 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase inhibitors mediated by endothelial nitric oxide synthase Proc. Natl. Acad. Sci. USA 95 1998 8880 8885
13. D. Fan, Y.T. Gu, H. Lv, T. Tang, Z.H. Xu, Z.Q. Song, and X.J. Tong The protective mechanism for the blood-brain barrier induced by aminoguanidine in surgical brain injury in rats Cell Mol. Neurobiol. 31 2011 1213 1219
14. J.J. Gebel, E.C. Jauch, T.G. Brott, J. Khoury, L. Sauerbeck, S. Salisbury, J. Spilker, T.A. Tomsick, J. Duldner, and J.P. Broderick Relative edema volume is a predictor of outcome in patients with hyperacute spontaneous intracerebral hemorrhage Stroke 33 2002 2636 2641
15. Y. Gursoy-Ozdemir, A. Can, and T. Dalkara Reperfusion-induced oxidative/nitrative injury to neurovascular unit after focal cerebral ischemia Stroke 35 2004 1449 1453
16. F. Han, Y. Shirasaki, and K. Fukunaga Microsphere embolism-induced endothelial nitric oxide synthase expression mediates disruption of the blood-brain barrier in rat brain J. Neurochem. 99 2006 97 106
17. F. Han, and K. Fukunaga Brain embolism-induced injury of vascular endothelial cells and a novel vasoprotective drug Yakugaku Zasshi 127 2007 743 748
18. A.F. Huhmer, C.R. Nishida, D.M.P. Ortiz, and C. Schoneich Inactivation of the inducible nitric oxide synthase by peroxynitrite Chem. Res. Toxicol. 10 1997 618 626
19. S.W. Jeong, K. Chu, K.H. Jung, S.U. Kim, M. Kim, and J.K. Roh Human neural stem cell transplantation promotes functional recovery in rats with experimental intracerebral hemorrhage Stroke 34 2003 2258 2263
20. M. Katsu, K. Niizuma, H. Yoshioka, N. Okami, H. Sakata, and P.H. Chan Hemoglobin-induced oxidative stress contributes to matrix metalloproteinase activation and blood-brain barrier dysfunction in vivo J. Cereb. Blood Flow Metab. 30 2010 1939 1950
21. M. Khan, H. Sakakima, T.S. Dhammu, A. Shunmugavel, Y.B. Im, A.G. Gilg, A.K. Singh, and I. Singh S-nitrosoglutathione reduces oxidative injury and promotes mechanisms of neurorepair following traumatic brain injury in rats J Neuroinflamm. 8 2011 78
22. M. Khan, T.S. Dhammu, H. Sakakima, A. Shunmugavel, A.G. Gilg, A.K. Singh, and I. Singh The inhibitory effect of S-nitrosoglutathione on blood-brain barrier disruption and peroxynitrite formation in a rat model of experimental stroke J. Neurochem. 123 Suppl. 2 2012 S86 S97
23. M.D. Laird, C. Wakade, C.J. Alleyne, and K.M. Dhandapani Hemin-induced necroptosis involves glutathione depletion in mouse astrocytes Free Radic. Biol. Med. 45 2008 1103 1114
24. U. Laufs, K. Gertz, U. Dirnagl, M. Bohm, G. Nickenig, and M. Endres Rosuvastatin, a new HMG-CoA reductase inhibitor, upregulates endothelial nitric oxide synthase and protects from ischemic stroke in mice Brain Res. 942 2002 23 30
25. H.J. Luth, G. Munch, and T. Arendt Aberrant expression of NOS isoforms in Alzheimers disease is structurally related to nitrotyrosine formation Brain Res. 953 2002 135 143
26. R.B. Muijsers, G. Folkerts, P.A. Henricks, G. Sadeghi-Hashjin, and F.P. Nijkamp Peroxynitrite: a two-faced metabolite of nitric oxide Life Sci. 60 1997 1833 1845
27. +-ATPase inhibition by nitric oxide and peroxynitrite anion J. Appl. Toxicol. 23 2003 275 278
28. S. Nag, P. Picard, and D.J. Stewart Expression of nitric oxide synthases and nitrotyrosine during blood-brain barrier breakdown and repair after cold injury Lab Investig. 81 2001 41 49
29. G.H. Oliveira-Paula, R. Lacchini, and J.E. Tanus-Santos Inducible nitric oxide synthase as a possible target in hypertension Curr. Drug Targets. 15 2014 164 174
30. P. Pacher, J.S. Beckman, and L. Liaudet Nitric oxide and peroxynitrite in health and disease Physiol. Rev. 87 2007 315 424
31. L.L. Pearce, A.J. Kanai, M.W. Epperly, and J. Peterson Nitrosative stress results in irreversible inhibition of purified mitochondrial complexes I and III without modification of cofactors Nitric Oxide 13 2005 254 263
32. T.W. Phares, M.J. Fabis, C.M. Brimer, R.B. Kean, and D.C. Hooper A peroxynitrite-dependent pathway is responsible for blood-brain barrier permeability changes during a central nervous system inflammatory response: TNF-alpha is neither necessary nor sufficient J. Immunol. 178 2007 7334 7343
33. +-ATPase modification during hypoxia in the cerebral cortex of the guinea pig fetus Neurochem. Res. 26 2001 1163 1169
34. A.I. Qureshi, A.D. Mendelow, and D.F. Hanley Intracerebral haemorrhage Lancet 373 2009 1632 1644
35. V.K. Robinson, E. Sato, D.K. Nelson, S.L. Camhi, R.A. Robbins, and J.C. Hoyt Peroxynitrite inhibits inducible (type 2) nitric oxide synthase in murine lung epithelial cells in vitro Free Radic. Biol. Med. 30 2001 986 991
36. J.K. Ryu, and J.G. McLarnon Minocycline or iNOS inhibition block 3-nitrotyrosine increases and blood-brain barrier leakiness in amyloid beta-peptide-injected rat hippocampus Exp. Neurol. 198 2006 552 557
37. M. Sabri, J. Ai, B. Knight, A. Tariq, H. Jeon, X. Shang, P.A. Marsden, and M.R. Loch Uncoupling of endothelial nitric oxide synthase after experimental subarachnoid hemorrhage J. Cereb. Blood Flow Metab. 31 2011 190 199
38. G.S. Scott, S.R. Bowman, T. Smith, R.J. Flower, and C. Bolton Glutamate-stimulated peroxynitrite production in a brain-derived endothelial cell line is dependent on N-methyl-D-aspartate (NMDA) receptor activation Biochem. Pharmacol. 73 2007 228 236
39. Y. Suofu, J. Clark, J. Broderick, K.R. Wagner, T. Tomsick, Y. Sa, and A. Lu Peroxynitrite decomposition catalyst prevents matrix metalloproteinase activation and neurovascular injury after prolonged cerebral ischemia in rats J. Neurochem. 115 2010 1266 1276
40. K.H. Tan, S. Harrington, W.M. Purcell, and R.D. Hurst Peroxynitrite mediates nitric oxide-induced blood-brain barrier damage Neurochem. Res. 29 2004 579 587
41. M. Thiyagarajan, C.L. Kaul, and S.S. Sharma Neuroprotective efficacy and therapeutic time window of peroxynitrite decomposition catalysts in focal cerebral ischemia in rats Br. J. Pharmacol. 142 2004 899 911
42. E.B. Vitner, T. Farfel-Becker, R. Eilam, I. Biton, and A.H. Futerman Contribution of brain inflammation to neuronal cell death in neuronopathic forms of Gauchers disease Brain 135 2012 1724 1735
43. W. Wang, G. Sawicki, and R. Schulz Peroxynitrite-induced myocardial injury is mediated through matrix metalloproteinase-2 Cardiovasc. Res. 53 2002 165 174
44. M. Xu, X. Chen, Y. Gu, T. Peng, D. Yang, R.C. Chang, K.F. So, K. Liu, and J. Shen Baicalin can scavenge peroxynitrite and ameliorate endogenous peroxynitrite-mediated neurotoxicity in cerebral ischemia-reperfusion injury J. Ethnopharmacol. 150 2013 116 124
45. S. Yang, Y. Chen, X. Deng, W. Jiang, B. Li, Z. Fu, M. Du, and R. Ding Hemoglobin-induced nitric oxide synthase overexpression and nitric oxide production contribute to blood-brain barrier disruption in the rat J. Mol. Neurosci. 51 2013 352 363
46. H. Yokoo, S. Chiba, K. Tomita, M. Takashina, H. Sagara, S. Yagisita, Y. Takano, and Y. Hattori Neurodegenerative evidence in mice brains with cecal ligation and puncture-induced sepsis: preventive effect of the free radical scavenger edaravone PLoS One 7 2012 e51539
47. M.H. Zou, C. Shi, and R.A. Cohen Oxidation of the zinc-thiolate complex and uncoupling of endothelial nitric oxide synthase by peroxynitrite J. Clin. Investig. 109 2002 817 826
48. M.H. Zou, R. Cohen, and V. Ullrich Peroxynitrite and vascular endothelial dysfunction in diabetes mellitus Endothelium 11 2004 89 97