S-nitrosoglutathione prevents blood-brain barrier disruption associated with increased matrix metalloproteinase-9 activity in experimental diabetes

Journal of Neurochemistry

Volumn 132, Issue 5, 2015, Pages 595-608

  Aggarwal, Aanchal ^a   Khera, Alka ^a   Singh, Inderjit ^b   Sandhir, Rajat ^a  

^a PANJAB UNIVERSITY   (India)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

blood brain barrier; cognition; diabetes; GSNO; matrix metalloproteinases; tissue inhibitor of matrix metalloproteinases

Indexed keywords

GELATINASE A; GELATINASE B; GLUCOSE; MESSENGER RNA; S NITROSOGLUTATHIONE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; NEUROPROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CORTEX; BRAIN EDEMA; COGNITIVE DEFECT; CONTROLLED STUDY; DIABETES MELLITUS; DRUG EFFICACY; ELECTROLYTE DISTURBANCE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HIPPOCAMPUS; HISTOPATHOLOGY; LEARNING; MALE; MEMORY; MOLECULAR SIZE; MORRIS WATER MAZE TEST; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; SUPPLEMENTATION; TISSUE SECTION; TREATMENT DURATION; ANIMAL; COMPLICATION; DRUG EFFECTS; ENZYMOLOGY; EXPERIMENTAL DIABETES MELLITUS; MAZE TEST; METABOLISM; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALIA; MUS;

ANIMALS; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; DIABETES MELLITUS, EXPERIMENTAL; ENZYME ACTIVATION; MALE; MATRIX METALLOPROTEINASE 9; MAZE LEARNING; MICE; NEUROPROTECTIVE AGENTS; REAL-TIME POLYMERASE CHAIN REACTION; S-NITROSOGLUTATHIONE; TISSUE INHIBITOR OF METALLOPROTEINASE-1;

EID: 84938082843     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12939     Document Type: Article

References (73)

1. Abbott N. J., Patabendige A. A., Dolman D. E., Yusof S. R., and, Begley D. J., (2010) Structure and function of the blood-brain barrier. Neurobiol. Dis. 37, 13-25.
2. Barichello T., Generoso J. S., Michelon C. M., Simoes L. R., Elias S. G., Vuolo F., Comim C. M., Dal-Pizzol F., and, Quevedo J., (2014) Inhibition of matrix metalloproteinases-2 and -9 prevents cognitive impairment induced by pneumococcal meningitis in Wistar rats. Exp. Biol. Med. (Maywood) 239, 225-231.
3. Betz A. L., Keep R. F., Beer M. E., and, Ren X. D., (1994) Blood-brain barrier permeability and brain concentration of sodium, potassium, and chloride during focal ischemia. J. Cereb. Blood Flow Metab. 14, 29-37.
4. Brooks T. A., Hawkins B. T., Huber J. D., Egleton R. D., and, Davis T. P., (2005) Chronic inflammatory pain leads to increased blood-brain barrier permeability and tight junction protein alterations. Am. J. Physiol. Heart Circ. Physiol. 289, H738-H743.
5. Chaturvedi M., and, Kaczmarek L., (2014) Mmp-9 inhibition: a therapeutic strategy in ischemic stroke. Mol. Neurobiol. 49, 563-573.
6. Chen T., Wang J., Li C., Zhang W., Zhang L., An L., Pang T., Shi X., and, Liao H., (2014) Nafamostat mesilate attenuates neuronal damage in a rat model of transient focal cerebral ischemia through thrombin inhibition. Sci. Rep. 4, 5531.
7. Crocker S. J., Pagenstecher A., and, Campbell I. L., (2004) The TIMPs tango with MMPs and more in the central nervous system. J. Neurosci. Res. 75, 1-11.
8. Cui B., Sun J. H., Xiang F. F., Liu L., and, Li W. J., (2012) Aquaporin 4 knockdown exacerbates streptozotocin-induced diabetic retinopathy through aggravating inflammatory response. Exp. Eye Res. 98, 37-43.
9. Dai J., Vrensen G. F., and, Schlingemann R. O., (2002) Blood-brain barrier integrity is unaltered in human brain cortex with diabetes mellitus. Brain Res. 954, 311-316.
10. Dandona P., James I. M., Newbury P. A., Woollard M. L., and, Beckett A. G., (1978) Cerebral blood flow in diabetes mellitus: evidence of abnormal cerebrovascular reactivity. Br. Med. J. 2, 325-326.
11. Dias A. S., Porawski M., Alonso M., Marroni N., Collado P. S., and, Gonzalez-Gallego J., (2005) Quercetin decreases oxidative stress, NF-kappaB activation, and iNOS overexpression in liver of streptozotocin-induced diabetic rats. J. Nutr. 135, 2299-2304.
12. Dietrich W. D., Alonso O., and, Busto R., (1993) Moderate hyperglycemia worsens acute blood-brain barrier injury after forebrain ischemia in rats. Stroke 24, 111-116.
13. Frears E. R., Zhang Z., Blake D. R., O'Connell J. P., and, Winyard P. G., (1996) Inactivation of tissue inhibitor of metalloproteinase-1 by peroxynitrite. FEBS Lett. 381, 21-24.
14. Gasche Y., Copin J. C., Sugawara T., Fujimura M., and, Chan P. H., (2001) Matrix metalloproteinase inhibition prevents oxidative stress-associated blood-brain barrier disruption after transient focal cerebral ischemia. J. Cereb. Blood Flow Metab. 21, 1393-1400.
15. Giebel S. J., Menicucci G., McGuire P. G., and, Das A., (2005) Matrix metalloproteinases in early diabetic retinopathy and their role in alteration of the blood-retinal barrier. Lab. Invest. 85, 597-607.
16. Gomez D. E., Alonso D. F., Yoshiji H., and, Thorgeirsson U. P., (1997) Tissue inhibitors of metalloproteinases: structure, regulation and biological functions. Eur. J. Cell Biol. 74, 111-122.
17. Gulturk S., Demirkazik A., Kosar I., Cetin A., Dokmetas H. S., and, Demir T., (2010) Effect of exposure to 50 Hz magnetic field with or without insulin on blood-brain barrier permeability in streptozotocin-induced diabetic rats. Bioelectromagnetics 31, 262-269.
18. Hammes H. P., Lin J., Renner O., Shani M., Lundqvist A., Betsholtz C., Brownlee M., and, Deutsch U., (2002) Pericytes and the pathogenesis of diabetic retinopathy. Diabetes 51, 3107-3112.
19. Hawkins B. T., and, Davis T. P., (2005) The blood-brain barrier/neurovascular unit in health and disease. Pharmacol. Rev. 57, 173-185.
20. Hawkins B. T., Lundeen T. F., Norwood K. M., Brooks H. L., and, Egleton R. D., (2007) Increased blood-brain barrier permeability and altered tight junctions in experimental diabetes in the rat: contribution of hyperglycaemia and matrix metalloproteinases. Diabetologia 50, 202-211.
21. Hovsepyan M. R., Haas M. J., Boyajyan A. S., Guevorkyan A. A., Mamikonyan A. A., Myers S. E., and, Mooradian A. D., (2004) Astrocytic and neuronal biochemical markers in the sera of subjects with diabetes mellitus. Neurosci. Lett. 369, 224-227.
22. Huber J. D., (2008) Diabetes, cognitive function, and the blood-brain barrier. Curr. Pharm. Des. 14, 1594-1600.
23. Huber J. D., VanGilder R. L., and, Houser K. A., (2006) Streptozotocin-induced diabetes progressively increases blood-brain barrier permeability in specific brain regions in rats. Am. J. Physiol. Heart Circ. Physiol. 291, H2660-H2668.
24. Hultstrom D., Malmgren L., Gilstring D., and, Olsson Y., (1983) FITC-Dextrans as tracers for macromolecular movements in the nervous system. A freeze-drying method for dextrans of various molecular sizes injected into normal animals. Acta Neuropathol. 59, 53-62.
25. Hung Y. C., Chen T. Y., Lee E. J., Chen W. L., Huang S. Y., Lee W. T., Lee M. Y., Chen H. Y., and, Wu T. S., (2008) Melatonin decreases matrix metalloproteinase-9 activation and expression and attenuates reperfusion-induced hemorrhage following transient focal cerebral ischemia in rats. J. Pineal Res. 45, 459-467.
26. Iwata A., Koike F., Arasaki K., and, Tamaki M., (1999) Blood-brain barrier destruction in hyperglycemic chorea in a patient with poorly controlled diabetes. J. Neurol. Sci. 163, 90-93.
27. Kamada H., Yu F., Nito C., and, Chan P. H., (2007) Influence of hyperglycemia on oxidative stress and matrix metalloproteinase-9 activation after focal cerebral ischemia/reperfusion in rats: relation to blood-brain barrier dysfunction. Stroke 38, 1044-1049.
28. Kamboj S. S., Vasishta R. K., and, Sandhir R., (2010) N-acetylcysteine inhibits hyperglycemia-induced oxidative stress and apoptosis markers in diabetic neuropathy. J. Neurochem. 112, 77-91.
29. Kaposzta Z., Baskerville P. A., Madge D., Fraser S., Martin J. F., and, Markus H. S., (2001) L-arginine and S-nitrosoglutathione reduce embolization in humans. Circulation 103, 2371-2375.
30. Khan M., Sekhon B., Giri S., Jatana M., Gilg A. G., Ayasolla K., Elango C., Singh A. K., and, Singh I., (2005) S-Nitrosoglutathione reduces inflammation and protects brain against focal cerebral ischemia in a rat model of experimental stroke. J. Cereb. Blood Flow Metab. 25, 177-192.
31. Khan M., Im Y. B., Shunmugavel A., Gilg A. G., Dhindsa R. K., Singh A. K., and, Singh I., (2009) Administration of S-nitrosoglutathione after traumatic brain injury protects the neurovascular unit and reduces secondary injury in a rat model of controlled cortical impact. J. Neuroinflammation 6, 32.
32. Khan M., Sakakima H., Dhammu T. S., Shunmugavel A., Im Y. B., Gilg A. G., Singh A. K., and, Singh I., (2011) S-nitrosoglutathione reduces oxidative injury and promotes mechanisms of neurorepair following traumatic brain injury in rats. J. Neuroinflammation 8, 78.
33. Kumari R., Willing L. B., Patel S. D., Baskerville K. A., and, Simpson I. A., (2011) Increased cerebral matrix metalloprotease-9 activity is associated with compromised recovery in the diabetic db/db mouse following a stroke. J. Neurochem. 119, 1029-1040.
34. Kuo Y. R., Wang F. S., Jeng S. F., Lutz B. S., Huang H. C., and, Yang K. D., (2004) Nitrosoglutathione improves blood perfusion and flap survival by suppressing iNOS but protecting eNOS expression in the flap vessels after ischemia/reperfusion injury. Surgery 135, 437-446.
35. Lorenzi M., Healy D. P., Hawkins R., Printz J. M., and, Printz M. P., (1986) Studies on the permeability of the blood-brain barrier in experimental diabetes. Diabetologia 29, 58-62.
36. Lowry O. H., Rosebrough N. J., Farr A. L., and, Randall R. J., (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
37. Maxwell P. R., Timms P. M., Chandran S., and, Gordon D., (2001) Peripheral blood level alterations of TIMP-1, MMP-2 and MMP-9 in patients with type 1 diabetes. Diabet. Med. 18, 777-780.
38. McCall A. L., Gould J. B., and, Ruderman N. B., (1984) Diabetes-induced alterations of glucose metabolism in rat cerebral microvessels. Am. J. Physiol. 247, E462-E467.
39. Mogi M., and, Horiuchi M., (2011) Neurovascular coupling in cognitive impairment associated with diabetes mellitus. Circ. J. 75, 1042-1048.
40. Morrey J. D., Olsen A. L., Siddharthan V., Motter N. E., Wang H., Taro B. S., Chen D., Ruffner D., and, Hall J. O., (2008) Increased blood-brain barrier permeability is not a primary determinant for lethality of West Nile virus infection in rodents. J. Gen. Virol. 89, 467-473.
41. Morris R., (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11, 47-60.
42. Munaut C., Noel A., Hougrand O., Foidart J. M., Boniver J., and, Deprez M., (2003) Vascular endothelial growth factor expression correlates with matrix metalloproteinases MT1-MMP, MMP-2 and MMP-9 in human glioblastomas. Int. J. Cancer 106, 848-855.
43. Nagase H., Suzuki K., Morodomi T., Enghild J. J., and, Salvesen G., (1992) Activation mechanisms of the precursors of matrix metalloproteinases 1, 2 and 3. Matrix Suppl. 1, 237-244.
44. Oztas B., and, Kucuk M., (1995) Influence of acute arterial hypertension on blood-brain barrier permeability in streptozocin-induced diabetic rats. Neurosci. Lett. 188, 53-56.
45. Pelisch N., Hosomi N., Mori H., Masaki T., and, Nishiyama A., (2013) RAS inhibition attenuates cognitive impairment by reducing blood- brain barrier permeability in hypertensive subjects. Curr. Hypertens. Rev. 9, 93-98.
46. Pfaffl M. W., Horgan G. W., and, Dempfle L., (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36.
47. Phillips S. A., Sylvester F. A., and, Frisbee J. C., (2005) Oxidant stress and constrictor reactivity impair cerebral artery dilation in obese Zucker rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R522-R530.
48. Prasad R., Giri S., Nath N., Singh I., and, Singh A. K., (2007) GSNO attenuates EAE disease by S-nitrosylation-mediated modulation of endothelial-monocyte interactions. Glia 55, 65-77.
49. Rauhala P., Lin A. M., and, Chiueh C. C., (1998) Neuroprotection by S-nitrosoglutathione of brain dopamine neurons from oxidative stress. FASEB J. 12, 165-173.
50. Rauhala P., Andoh T., and, Chiueh C. C., (2005) Neuroprotective properties of nitric oxide and S-nitrosoglutathione. Toxicol. Appl. Pharmacol. 207, 91-95.
51. Rechthand E., Smith Q. R., Latker C. H., and, Rapoport S. I., (1987) Altered blood-nerve barrier permeability to small molecules in experimental diabetes mellitus. J. Neuropathol. Exp. Neurol. 46, 302-314.
52. Ries C., (2014) Cytokine functions of TIMP-1. Cell. Mol. Life Sci. 71, 659-672.
53. Romanic A. M., White R. F., Arleth A. J., Ohlstein E. H., and, Barone F. C., (1998) Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: inhibition of matrix metalloproteinase-9 reduces infarct size. Stroke 29, 1020-1030.
54. Rosenberg G. A., Estrada E. Y., and, Dencoff J. E., (1998) Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 29, 2189-2195.
55. Rosenberg G. A., Cunningham L. A., Wallace J., Alexander S., Estrada E. Y., Grossetete M., Razhagi A., Miller K., and, Gearing A., (2001) Immunohistochemistry of matrix metalloproteinases in reperfusion injury to rat brain: activation of MMP-9 linked to stromelysin-1 and microglia in cell cultures. Brain Res. 893, 104-112.
56. Schrammel A., Gorren A. C., Schmidt K., Pfeiffer S., and, Mayer B., (2003) S-nitrosation of glutathione by nitric oxide, peroxynitrite, and (∗)NO/O(2)(∗-). Free Radic. Biol. Med. 34, 1078-1088.
57. Starr J. M., Wardlaw J., Ferguson K., MacLullich A., Deary I. J., and, Marshall I., (2003) Increased blood-brain barrier permeability in type II diabetes demonstrated by gadolinium magnetic resonance imaging. J. Neurol. Neurosurg. Psychiatry 74, 70-76.
58. Stauber W. T., Ong S. H., and, McCuskey R. S., (1981) Selective extravascular escape of albumin into the cerebral cortex of the diabetic rat. Diabetes 30, 500-503.
59. Stawarski M., Stefaniuk M., and, Wlodarczyk J., (2014) Matrix metalloproteinase-9 involvement in the structural plasticity of dendritic spines. Front. Neuroanat. 8, 68.
60. Szkudelski T., (2001) The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol. Res. 50, 537-546.
61. Towbin H., Staehelin T., and, Gordon J., (1992) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. 1979. Biotechnology 24, 145-149.
62. Vandooren J., Geurts N., Martens E., Van den Steen P. E., Jonghe S. D., Herdewijn P., and, Opdenakker G., (2011) Gelatin degradation assay reveals MMP-9 inhibitors and function of O-glycosylated domain. World J. Biol. Chem. 2, 14-24.
63. VanGilder R. L., Kelly K. A., Chua M. D., Ptachcinski R. L., and, Huber J. D., (2009) Administration of sesamol improved blood-brain barrier function in streptozotocin-induced diabetic rats. Exp. Brain Res. 197, 23-34.
64. Viggars A. P., Wharton S. B., Simpson J. E., et al,. (2011) Alterations in the blood-brain barrier in ageing cerebral cortex in relationship to Alzheimer-type pathology: a study in the MRC-CFAS population neuropathology cohort. Neurosci. Lett. 505, 25-30.
65. Visse R., and, Nagase H., (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 92, 827-839.
66. Wautier J. L., Zoukourian C., Chappey O., Wautier M. P., Guillausseau P. J., Cao R., Hori O., Stern D., and, Schmidt A. M., (1996) Receptor-mediated endothelial cell dysfunction in diabetic vasculopathy. Soluble receptor for advanced glycation end products blocks hyperpermeability in diabetic rats. J. Clin. Invest. 97, 238-243.
67. Weissman D. E., and, Stewart C., (1988) Experimental drug therapy of peritumoral brain edema. J. Neurooncol. 6, 339-342.
68. Yan S. F., Ramasamy R., and, Schmidt A. M., (2008) Mechanisms of disease: advanced glycation end-products and their receptor in inflammation and diabetes complications. Nat. Clin. Pract. Endocrinol. Metab. 4, 285-293.
69. Young W., Rappaport Z. H., Chalif D. J., and, Flamm E. S., (1987) Regional brain sodium, potassium, and water changes in the rat middle cerebral artery occlusion model of ischemia. Stroke 18, 751-759.
70. Zampolli A., Basta G., Lazzerini G., Feelisch M., and, De Caterina R., (2000) Inhibition of endothelial cell activation by nitric oxide donors. J. Pharmacol. Exp. Ther. 295, 818-823.
71. Zhang J. W., and, Gottschall P. E., (1997) Zymographic measurement of gelatinase activity in brain tissue after detergent extraction and affinity-support purification. J. Neurosci. Methods 76, 15-20.
72. Zlokovic B. V., (2008) The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57, 178-201.
73. del Zoppo G. J., (2010) The neurovascular unit, matrix proteases, and innate inflammation. Ann. N. Y. Acad. Sci. 1207, 46-49.