Hydrogen sulfide attenuates neurodegeneration and neurovascular dysfunction induced by intracerebral-administered homocysteine in mice

Neuroscience

Volumn 252, Issue , 2013, Pages 302-319

  Kamat, P K ^a   Kalani, A ^a   Givvimani, S ^a   Sathnur, P B ^a   Tyagi, S C ^a   Tyagi, N ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

Cerebrovascular dysfunction; H2S; Neurodegeneration; Neuroinflammation

Indexed keywords

ACETYLCHOLINESTERASE; BISULFITE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GELATINASE A; GELATINASE B; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTATHIONE; HOMOCYSTEINE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; MALONALDEHYDE; NEURON SPECIFIC ENOLASE; NITRITE; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN S100B; PROTEIN ZO1; SYNAPTOSOME ASSOCIATED PROTEIN 97; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; CEREBROSPINAL FLUID; CEREBROVASCULAR DISEASE; CONTROLLED STUDY; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; MALE; MOUSE; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

5,5′-DITHIOBIS-(2-NITROBENZOIC ACID); ACETYLCHOLINESTERASE; ACHE; ACSF; AD; ALZHEIMER'S DISEASES; ARTIFICIAL CEREBROSPINAL FLUID; BBB; BLOOD-BRAIN BARRIER; CEREBROVASCULAR DYSFUNCTION; DI; DISCRIMINATION INDEX; DTNB; ECM; EDTA; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENOS; ETHYLENEDIAMINETETRAACETIC ACID; EXTRACELLULAR MATRIX; FJC; FLURO JADE-C; GFAP; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTATHIONE; GSH; H(2)S; HCY; HE; HEMATOXYLIN AND EOSIN; HOMOCYSTEINE; HORSERADISH PEROXIDASE; HRP; IC; IL; INDUCIBLE NITRIC OXIDE SYNTHASE; INOS; INTERLEUKIN; INTRACEREBRAL; MALONDIALDEHYDE; MATRIX METALLOPROTEINASES; MDA; MMP; NEURODEGENERATION; NEUROINFLAMMATION; NEURON-SPECIFIC ENOLASE; NSE; PARKINSON'S DISEASE; PBS; PD; PHENYLMETHYLSULFONYL FLUORIDE; PHOSPHATE-BUFFERED SALINE; PMSF; POLYVINYLIDENE DIFLUORIDE; POST-SYNAPTIC DENSITY-95; PSD95; PVDF; RADIO IMMUNOPRECIPITATION ASSAY; RECOGNITION INDEX; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RI; RIPA; RT-PCR; SAP97; SYNAPTOSOME ASSOCIATED PROTEIN-97; TBS-T; TCA; TERMINAL DEOXYNUCLEOTIDYL TRANSFERASE-MEDIATED, DUTP NICK-END LABELING; TIGHT JUNCTION PROTEINS; TIMP; TISSUE INHIBITOR OF METALLOPROTEINASES; TJPS; TNF; TRICHLOROACETIC ACID; TRIS-BUFFERED SALINE WITH TWEEN 20; TUMOR NECROSIS FACTOR; TUNEL; WILD TYPE; WT; ZO; ZONULA OCCULDENS;

ANIMALS; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; BRAIN; GASOTRANSMITTERS; HOMOCYSTEINE; HYDROGEN SULFIDE; INFLAMMATION; INJECTIONS, INTRAVENTRICULAR; MALE; MICE; NERVE DEGENERATION; OXIDATIVE STRESS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84884343024     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.07.051     Document Type: Article

References (73)

1. Abbott N.J., Rönnbäck L., Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006, 7:41-53.
2. Alvarez B., Ruiz C., Chacon P., Alvarez-Sabin J., Matas M. Serum values of metalloproteinase-2 and metalloproteinase-9 as related to unstable plaque and inflammatory cells in patients with greater than 70% carotid artery stenosis. J Vasc Surg 2004, 40:469-475.
3. Asahi M., Asahi K., Jung J.C., del Zoppo G.J., Fini M.E., Lo E.H. Role for matrix metalloproteinase 9 after focal cerebral ischemia: effects of gene knockout and enzyme inhibition with BB-94. J Cereb Blood Flow Metab 2000, 20:1681-1689.
4. Ataie A., Sabetkasaei M., Haghparast A., Moghaddam A.H., Ataee R., Moghaddam S.N. Curcumin exerts neuroprotective effects against homocysteine intracerebroventricular injection-induced cognitive impairment and oxidative stress in rat brain. J Med Food 2010, 13:821-826.
5. Calabrese V., Copani A., Testa D., Ravagna A., Spadaro F., Tendi E., Nicoletti V.G., Giuffrida Stella A.M. Nitric oxide synthase induction in astroglial cell cultures: effect on heat shock protein 70 synthesis and oxidant/antioxidant balance. J Neurosci Res 2000, 60:613-622.
6. Christie L.A., Riedel G., Algaidi S.A., Whalley L.J., Platt B. Enhanced hippocampal long-term potentiation in rats after chronic exposure to homocysteine. Neurosci Lett 2005, 373:119-124.
7. Colado M.I., O'Shea E., Granados R., Murray T.K., Green A.R. In vivo evidence for free radical involvement in the degeneration of rat brain 5-HT following administration of MDMA ('ecstasy') and p-chloroamphetamine but not the degeneration following fenfluramine. Br J Pharmacol 1997, 121:889-900.
8. da Cunha A.A., Ferreira A.G., Wyse A.T. Increased inflammatory markers in brain and blood of rats subjected to acute homocysteine administration. Metab Brain Dis 2010, 25:199-206.
9. D'Erasmo E., Acca M., Pisani D., Volpe M.S. Neurological state, infarct size and clinical outcome are related to early platelet count decrease in stroke. Gerontology 1993, 39:276-279.
10. Dollery C.M., Humphries S.E., McClelland A., Latchman D.S., McEwan J.R. Expression of tissue inhibitor of matrix metalloproteinases 1 by use of an adenoviral vector inhibits smooth muscle cell migration and reduces neointimal hyperplasia in the rat model of vascular balloon injury. Circulation 1999, 99:3199-3205.
11. Duffield J.S. The inflammatory macrophage: a story of Jekyll and Hyde. Clin Sci (Lond) 2003, 104:27-38.
12. Eikelboom J.W., Lonn E., Genest J., Hankey G., Yusuf S. Homocyst(e)ine and cardiovascular disease: a critical review of the epidemiologic evidence. Ann Intern Med 1999, 131:363-375.
13. El-Husseini A.E., Schnell E., Chetkovich D.M., Nicoll R.A., Bredt D.S. PSD-95 involvement in maturation of excitatory synapses. Science 2000, 290:1364-1368. (New York, NY).
14. Ellman G.L. Tissue sulfhydryl groups. Arch Biochem Biophys 1959, 82:70-77.
15. Fanning A.S., Little B.P., Rahner C., Utepbergenov D., Walther Z., Anderson J.M. The unique-5 and -6 motifs of ZO1 regulate tight junction strand localization and scaffold properties. Mol Biol Cell 2007, 18:721-731.
16. Fujimura M., Morita-Fujimura Y., Kawase M., Chan P.H. Early decrease of apurinic/apyrimidinic endonuclease expression after transient focal cerebral ischemia in mice. J Cereb Blood Flow Metab 1999, 19:495-501.
17. Furuse M., Fujita K., Hiragi T., Fujimoto K., Tsukita S. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occluding. J Cell Biol 1998, 141:1539-1550.
18. Gasche Y., Fujimura M., Morita-Fujimura Y., Copin J.C., Kawase M., Massengale J., Chan P.H. 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 1999, 19:1020-1028.
19. Girouard H., Iadecola C. Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol 2006, 100:328-335.
20. Givvimani S., Sen U., Tyagi N., Munjal C., Tyagi S.C. X-ray imaging of differential vascular density in MMP-9-/-, PAR-1-/+, hyperhomocysteinemic (CBS-/+) and diabetic (Ins2-/+) mice. Arch Physiol Biochem 2011, 117:1-7.
21. Green L.C., Wagner D.A., Glogowski J., Skipper P.L., Wishnok J.S., Tannenbaum S.R. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 1982, 126:131-138.
22. Harigaya Y., Shoji M., Shirao T., Hirai S. Disappearance of actin-binding protein, drebrin, from hippocampal synapses in Alzheimer's disease. J Neurosci Res 1996, 43:87-92.
23. Haskins J., Gu L., Wittchen E.S., Hibbard J., Stevenson B.R. ZO-3, a novel member of the MAGUK protein family found at the tight junction, interacts with ZO1 and occludin. J Cell Biol 1998, 141:199-208.
24. Jesaitis L.A., Goodenough D.A. Molecular characterization and tissue distribution of ZO-2, a tight junction protein homologous to ZO1 and the Drosophila discs-large tumor suppressor protein. J Cell Biol 1994, 124:949-962.
25. Kalani A., Kamat P.K., Tyagi S.C., Tyagi N. Synergy of Homocysteine, MicroRNA, and Epigenetics: A Novel Therapeutic Approach for Stroke. Mol Neurobiol 2013, 48:157-168.
26. Kamat P.K., Tota S., Rai S., Shukla R., Ali S., Najmi A.K., Nath C. Okadaic acid induced neurotoxicity leads to central cholinergic dysfunction in rats. Eur J Pharmacol 2012, 690:90-98.
27. Kamat P.K., Tota S., Saxena G., Shukla R., Nath C. Okadaic acid (ICV) induced memory impairment in rats: a suitable experimental model to test anti-dementia activity. Brain Res 2010, 1309:66-74.
28. Kamat P.K., Tota S., Shukla R., Ali S., Najmi A.K., Nath C. Mitochondrial dysfunction: a crucial event in okadaic acid (ICV) induced memory impairment and apoptotic cell death in rat brain. Pharmacol Biochem Behav 2011, 100:311-319.
29. Kanani P.M., Sinkey C.A., Browning R.L., Allaman M., Knapp H.R., Haynes W.G. Role of oxidant stress in endothelial dysfunction produced by experimental hyperhomocyst(e)inemia in humans. Circulation 1999, 100:1161-1168.
30. Kimura Y., Kimura H. Hydrogen sulfide protects neurons from oxidative stress. FASEB J 2004, 18:1165-1167.
31. Lee G.A., Lin C.-H., Jiang H.-H., Chao H.-J., Wu C.-L., Hsueh C.-M. Microglia-derived glial cell line-derived neurotrophic factor could protect Sprague-Dawley rat astrocyte from in vitro ischemia-induced damage. Neurosci Lett 2004, 356:111-114.
32. Lee S.-R., Tsuji K., Lee S.-R., Lo E.H. Role of matrix metalloproteinases in delayed neuronal damage after transient global cerebral ischemia. J Neurosci 2004, 24:671-678.
33. Lee S.W., Song K.E., Shin D.S., Ahn S.M., Ha E.S., Kim D.J., Nam M.S., Lee K.W. Alterations in peripheral blood levels of TIMP-1, MMP-2, and MMP-9 in patients with type-2 diabetes. Diabetes Res Clin Pract 2005, 69:175-179.
34. Li X., Jin H., Bin G., Wang L., Tang C., Du J. Endogenous hydrogen sulfide regulates pulmonary artery collagen remodeling in rats with high pulmonary blood flow. Exp Biol Med 2009, 234:504-512.
35. Li L., Sun J., Wang C., Wang L., Hovart M., Sheil A.G. Graft histology and lymphocyte apoptosis in pancreas allografts combined with liver allografts. Transplant Proc 1998, 30:2956-2957.
36. Liu C., Zhou X.S., Geng Q.M. Evaluation oxygen free radicals related index before liver transplantation to forejudge prognosis. Zhongguo Wei Zhong Bing Ji Jiu Yi Xue 2003, 15:560-562.
37. Lominadze D., Joshua I.G., Schuschke D.A. Increased erythrocyte aggregation in spontaneously hypertensive rats. Am J Hypertens 1998, 11:784-789.
38. Lucas S.M., Rothwell N.J., Gibson R.M. The role of inflammation in CNS injury and disease. Br J Pharmacol 2006, 147(Suppl. 1):S232-S240.
39. Lyon D.R., Gunzelmann G.M. Functional equivalence and spatial path memory. Q J Exp Psychol (Hove) 2011, 64:2081-2087.
40. Mecocci P., Parnetti L., Romano G., Scarelli A., Chionne F., Cecchetti R., Polidori M.C., Palumbo B., Cherubini A., Senin U. Serum anti-GFAP and anti-S100 autoantibodies in brain aging, Alzheimer's disease and vascular dementia. J Neuroimmunol 1995, 57:165-170.
41. Mehta D., Malik A. Signaling mechanisms regulating endothelial permeability. Physiol Rev 2006, 86:279-367.
42. Min H.Y., Kim M.S., Jang D.S., Park E.J., Seo E.K., Lee S.K. Suppression of lipopolysaccharide-stimulated inducible nitric oxide synthase (iNOS) expression by a novel humulene derivative in macrophage cells. Int Immunopharmacol 2009, 9:844-849.
43. Mrak R.E., Griffin W.S. Interleukin-1, neuroinflammation, and Alzheimer's disease. Neurobiol Aging 2001, 22:903-908.
44. Musch M.W., Walsh-Reitz M.M., Chang E.B. Roles of ZO1, occludin, and actin in oxidant-induced barrier disruption. Am J Physiol Gastrointest Liver Physiol 2006, 290:222-231.
45. Myojin K., Taguchi A., Umetani K., Fukushima K., Nishiura N., Matsuyama T., Kimura H., Stern D.M., Imai Y., Mori H. Visualization of intracerebral arteries by synchrotron radiation microangiography. AJNR Am J Neuroradiol 2007, 28:953-957.
46. Obeid R., McCaddon A., Herrmann W. The role of hyperhomocysteinemia and B-vitamin deficiency in neurological and psychiatric diseases. Clin Chem Lab Med 2007, 45:1590-1606.
47. Parnetti L., Palumbo B., Cardinali L., Loreti F., Chionne F., Cecchetti R., Senin U. Cerebrospinal fluid neuron-specific enolase in Alzheimer's disease and vascular dementia. Neurosci Lett 1995, 183:43-45.
48. Patibandla P.K., Tyagi N., Dean W.L., Tyagi S.C., Roberts A.M., Lominadze D. Fibrinogen induces alterations of endothelial cell tight junction proteins. J Cell Physiol 2009, 221:195-203.
49. Perna A.F., Ingrosso D., De Santo N.G. Homocysteine and oxidative stress. Amino Acids 2003, 25:409-417.
50. Petursdottir A.L., Farr S.A., Morley J.E., Banks W.A., Skuladottir G.V. Lipid peroxidation in brain during aging in the senescence-accelerated mouse (SAM). Neurobiol Aging 2007, 28:1170-1178.
51. Rai S., Kamat P.K., Nath C., Shukla R. A study on neuroinflammation and NMDA receptor function in STZ (ICV) induced memory impaired rats. J Neuroimmunol 2013, 254:1-9.
52. Rao J.S., Kim H.W., Kellom M., Greenstein D., Chen M., Kraft A.D., Harry G.J., Rapoport S.I., Basselin M. Increased neuroinflammatory and arachidonic acid cascade markers, and reduced synaptic proteins, in brain of HIV-1 transgenic rats. J Neuroinflamm 2011, 8:101.
53. Refsum H., Ueland P.M., Nygard O., Vollset S.E. Homocysteine and cardiovascular disease. Annu Rev Med 1998, 49:31-62.
54. Romanic A.M., White R.F., Arleth A.J., Ohlstein E.H., Barone F.C. Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: inhibition of matrix metalloproteinase-9 reduces infarct size. Stroke 1998, 29:1020-1030.
55. Rossoni G., Manfredi B., Razzetti R., Civelli M., Berti F. Positive interaction of the novel beta2-agonist carmoterol and tiotropium bromide in the control of airway changes induced by different challenges in guinea-pigs. Pulm Pharmacol Ther 2007, 20:250-257.
56. Schmued L.C., Stowers C.C., Scallet A.C., Xu L. Fluoro-Jade C results in ultra-high resolution and contrast labeling of degenerating neurons. Brain Res 2005, 1035:24-31.
57. Singh S., Gupta A.K. Nitric oxide: role in tumour biology and iNOS/NO-based anticancer therapies. Cancer Chemother Pharmacol 2011, 67:1211-1224.
58. Stevenson B.R., Siliciano J.D., Mooseker M.S., Goodenough D.A. Identification of ZO1: a higher molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J Cell Biol 1986, 103:755-766.
59. Szabo C. Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 2007, 6:917-935.
60. Tada Y., Yagi K., Kitazato K.T., Tamura T., Kinouchi T., Shimada K., Matsushita N., Nakajima N., Satomi J., Kageji T., Nagahiro S. Reduction of endothelial tight junction proteins is related to cerebral aneurysm formation in rats. J Hypertens 2010, 28:1883-1891.
61. Takechi R., Pallebage-Gamarallage M.M., Lam V., Giles C., Mamo J.C. Aging-related changes in blood-brain barrier integrity and the effect of dietary fat. Neurodegener Dis 2012, 10.1159/000343211.
62. Tota S., Hanif K., Kamat P.K., Najmi A.K., Nath C. Role of central angiotensin receptors in scopolamine-induced impairment in memory, cerebral blood flow, and cholinergic function. Psychopharmacology 2012, 222:185-202.
63. Tsukita S., Furose M. Pores in the wall: claudins constitute tight junction strands containing aqueous pores. J Cell Biol 2000, 149:13-16.
64. Tyagi N., Givvimani S., Qipshidze N., Kundu S., Kapoor S., Vacek J.C., Tyagi S.C. Hydrogen sulfide mitigates matrix metalloproteinase-9 activity and neurovascular permeability in hyperhomocysteinemic mice. Neurochem Int 2010, 56:301-307.
65. Tyagi N., Moshal K.S., Sen U., Vacek T.P., Kumar M., Hughes W.M., Kundu S., Tyagi S.C. H2S protects against methionine-induced oxidative stress in brain endothelial cells. Antioxid Redox Signal 2009, 11:25-33.
66. Tyagi N., Ovechkin A.V., Lominadze D., Moshal K.S., Tyagi S.C. Mitochondrial mechanism of microvascular endothelial cells apoptosis in hyperhomocysteinemia. J Cell Biochem 2006, 98:1150-1162.
67. Uttara B., Singh A.V., Zamboni P., Mahajan R.T. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol 2009, 7:65-74.
68. Weiss N., Papatheodorou L., Morihara N., Hilge R., Ide N. Aged garlic extract restores nitric oxide bioavailability in cultured human endothelial cells even under conditions of homocysteine elevation. J Ethnopharmacol 2013, 145:162-167.
69. White A.R., Huang X., Jobling M.F., Barrow C.J., Beyreuther K., Masters C.L., Bush A.I., Cappai R. Homocysteine potentiates copper- and amyloid beta peptide-mediated toxicity in primary neuronal cultures: possible risk factors in the Alzheimer's-type neurodegenerative pathways. J Neurochem 2001, 76:1509-1520.
70. Williams W.M., Chung Y.W. Evidence for an age-related attenuation of cerebral microvascular antioxidant response to oxidative stress. Life Sci 2006, 79:1638-1644.
71. Yan S.K., Chang T., Wang H., Wu L., Wang R., Meng Q.H. Effects of hydrogen sulfide on homocysteine-induced oxidative stress in vascular smooth muscle cells. Biochem Biophys Res Commun 2006, 351:485-491.
72. Zhao S.P., Liu L., Gao M., Zhou Q.C., Li Y.L., Xia B. Impairment of endothelial function after a high-fat meal in patients with coronary artery disease. Coron Artery Dis 2001, 12:561-565.
73. Zlokovic B.V. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008, 57:178-201.