Administration of S-methyl-l-thiocitrulline protects against brain injuries after intracerebral hemorrhage

Neuroscience

Volumn 270, Issue , 2014, Pages 40-47

  Lu, A ^a   Wagner, K R ^a   Broderick, J P ^a   Clark, J F ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Brain injury; Intracerebral hemorrhage; Rats; S methyl l thiocitrulline

Indexed keywords

GLUTAMIC ACID; LAMININ; NITRIC OXIDE SYNTHASE; OCCLUDIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; S METHYLTHIOCITRULLINE; CITRULLINE; ENZYME INHIBITOR; NEUROPROTECTIVE AGENT; OCLN PROTEIN, RAT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; S-METHYLTHIOCITRULLINE; THIOUREA;

ANIMAL EXPERIMENT; ARTICLE; BRAIN HEMORRHAGE; BRAIN INJURY; BRAIN PROTECTION; CEREBROSPINAL FLUID; CONTROLLED STUDY; CORPUS STRIATUM; HISTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; ZYMOGRAPHY; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BODY POSTURE; BRAIN; CELL DEATH; CEREBRAL HEMORRHAGE; DISEASE MODEL; DRUG EFFECTS; METABOLISM; MICROVASCULATURE; MOTOR ACTIVITY; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; VASCULARIZATION;

ANIMALS; BRAIN; CELL DEATH; CEREBRAL HEMORRHAGE; CITRULLINE; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; LAMININ; MALE; MICROVESSELS; MOTOR ACTIVITY; NADPH DEHYDROGENASE; NEURONS; NEUROPROTECTIVE AGENTS; NITRIC OXIDE SYNTHASE; OCCLUDIN; POSTURE; RATS, SPRAGUE-DAWLEY; THIOUREA;

EID: 84899142479     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.04.004     Document Type: Article

References (50)

1. Alm P., Sharma H.S., Sjoquist P.O., Westman J. A new antioxidant compound H-290/51 attenuates nitric oxide synthase and heme oxygenase expression following hyperthermic brain injury. An experimental study using immunohistochemistry in the rat. Amino Acids 2000, 19:383-394.
2. Almaas R., Hanko E., Mollnes T.E., Rootwelt T. Dexamethasone reduces bilirubin-induced toxicity and IL-8 and MCP-1 release in human NT2-N neurons. Brain Res 2012, 1458:12-17.
3. Boehning D., Snyder S.H. Novel neural modulators. Annu Rev Neurosci 2003, 26:105-131.
4. Brito M.A., Vaz A.R., Silva S.L., Falcao A.S., Fernandes A., Silva R.F., Brites D. N-methyl-d-aspartate receptor and neuronal nitric oxide synthase activation mediate bilirubin-induced neurotoxicity. Mol Med 2010, 16:372-380.
5. Caliaperumal J., Ma Y., Colbourne F. Intra-parenchymal ferrous iron infusion causes neuronal atrophy, cell death and progressive tissue loss: implications for intracerebral hemorrhage. Exp Neurol 2012, 237:363-369.
6. Castillo J., Davalos A., Alvarez-Sabin J., Pumar J.M., Leira R., Silva Y., Montaner J., Kase C.S. Molecular signatures of brain injury after intracerebral hemorrhage. Neurology 2002, 58:624-629.
7. Chiang M.F., Chiu W.T., Lin F.J., Thajeb P., Huang C.J., Tsai S.H. Multiparametric analysis of cerebral substrates and nitric oxide delivery in cerebrospinal fluid in patients with intracerebral haemorrhage: correlation with hemodynamics and outcome. Acta Neurochir (Wien) 2006, 148:615-621.
8. Clark J.F., Loftspring M., Wurster W.L., Beiler S., Beiler C., Wagner K.R., Pyne-Geithman G.J. Bilirubin oxidation products, oxidative stress, and intracerebral hemorrhage. Acta Neurochir Suppl 2008, 105:7-12.
9. Coert B.A., Anderson R.E., Meyer F.B. Is neuroprotective efficacy of nNOS inhibitor 7-NI dependent on ischemic intracellular pH?. Am J Physiol Heart Circ Physiol 2003, 284:H151-H159.
10. Colado M.I., Camarero J., Mechan A.O., Sanchez V., Esteban B., Elliott J.M., Green A.R. A study of the mechanisms involved in the neurotoxic action of 3,4-methylenedioxymethamphetamine (MDMA, 'ecstasy') on dopamine neurones in mouse brain. Br J Pharmacol 2001, 134:1711-1723.
11. Darvesh A.S., Yamamoto B.K., Gudelsky G.A. Evidence for the involvement of nitric oxide in 3,4-methylenedioxymethamphetamine-induced serotonin depletion in the rat brain. J Pharmacol Exp Ther 2005, 312:694-701.
12. Dawson V.L., Dawson T.M. Nitric oxide neurotoxicity. J Chem Neuroanat 1996, 10:179-190.
13. Dawson V.L., Kizushi V.M., Huang P.L., Snyder S.H., Dawson T.M. Resistance to neurotoxicity in cortical cultures from neuronal nitric oxide synthase-deficient mice. J Neurosci 1996, 16:2479-2487.
14. Florczak-Rzepka M., Grond-Ginsbach C., Montaner J., Steiner T. Matrix metalloproteinases in human spontaneous intracerebral hemorrhage: an update. Cerebrovasc Dis 2012, 34:249-262.
15. Furfine E.S., Harmon M.F., Paith J.E., Knowles R.G., Salter M., Kiff R.J., Duffy C., Hazelwood R., Oplinger J.A., Garvey E.P. Potent and selective inhibition of human nitric oxide synthases. Selective inhibition of neuronal nitric oxide synthase by S-methyl-l-thiocitrulline and S-ethyl-L-thiocitrulline. J Biol Chem 1994, 269:26677-26683.
16. Gu Z., Kaul M., Yan B., Kridel S.J., Cui J., Strongin A., Smith J.W., Liddington R.C., Lipton S.A. S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 2002, 297:1186-1190.
17. Gulturk S., Kozan R., Bostanci M.O., Sefil F., Bagirici F. Inhibition of neuronal nitric oxide synthase prevents iron-induced cerebellar Purkinje cell loss in the rat. Acta Neurobiol Exp (Wars) 2008, 68:26-31.
18. Hara H., Huang P.L., Panahian N., Fishman M.C., Moskowitz M.A. Reduced brain edema and infarction volume in mice lacking the neuronal isoform of nitric oxide synthase after transient MCA occlusion. J Cereb Blood Flow Metab 1996, 16:605-611.
19. Hoque K.E., Indorkar R.P., Sammut S., West A.R. Impact of dopamine-glutamate interactions on striatal neuronal nitric oxide synthase activity. Psychopharmacology (Berl) 2010, 207:571-581.
20. Hua Y., Schallert T., Keep R.F., Wu J., Hoff J.T., Xi G. Behavioral tests after intracerebral hemorrhage in the rat. Stroke 2002, 33:2478-2484.
21. Huang Z., Huang P.L., Panahian N., Dalkara T., Fishman M.C., Moskowitz M.A. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 1994, 265:1883-1885.
22. Ishida A., Trescher W.H., Lange M.S., Johnston M.V. Prolonged suppression of brain nitric oxide synthase activity by 7-nitroindazole protects against cerebral hypoxic-ischemic injury in neonatal rat. Brain Dev 2001, 23:349-354.
23. Katsu M., Niizuma K., Yoshioka H., Okami N., Sakata H., Chan P.H. Hemoglobin-induced oxidative stress contributes to matrix metalloproteinase activation and blood-brain barrier dysfunction in vivo. J Cereb Blood Flow Metab 2010, 30:1939-1950.
24. Kiedrowski L., Costa E., Wroblewski J.T. Glutamate receptor agonists stimulate nitric oxide synthase in primary cultures of cerebellar granule cells. J Neurochem 1992, 58:335-341.
25. Kim D.W., Im S.H., Kim J.Y., Kim D.E., Oh G.T., Jeong S.W. Decreased brain edema after collagenase-induced intracerebral hemorrhage in mice lacking the inducible nitric oxide synthase gene. Laboratory investigation. J Neurosurg 2009, 111:995-1000.
26. Lampl Y., Shmuilovich O., Lockman J., Sadeh M., Lorberboym M. Prognostic significance of blood brain barrier permeability in acute hemorrhagic stroke. Cerebrovasc Dis 2005, 20:433-437.
27. Lee S.T., Chu K., Jung K.H., Kim J., Kim E.H., Kim S.J., Sinn D.I., Ko S.Y., Kim M., Roh J.K. Memantine reduces hematoma expansion in experimental intracerebral hemorrhage, resulting in functional improvement. J Cereb Blood Flow Metab 2006, 26:536-544.
28. Lee S.T., Chu K., Sinn D.I., Jung K.H., Kim E.H., Kim S.J., Kim J.M., Ko S.Y., Kim M., Roh J.K. Erythropoietin reduces perihematomal inflammation and cell death with eNOS and STAT3 activations in experimental intracerebral hemorrhage. J Neurochem 2006, 96:1728-1739.
29. Loftspring M.C., Johnson H.L., Feng R., Johnson A.J., Clark J.F. Unconjugated bilirubin contributes to early inflammation and edema after intracerebral hemorrhage. J Cereb Blood Flow Metab 2011, 31:1133-1142.
30. Lu A., Tang Y., Ran R., Ardizzone T.L., Wagner K.R., Sharp F.R. Brain genomics of intracerebral hemorrhage. J Cereb Blood Flow Metab 2006, 26:230-252.
31. Lu A., Clark J.F., Broderick J.P., Pyne-Geithman G.J., Wagner K.R., Ran R., Khatri P., Tomsick T., Sharp F.R. Reperfusion activates metalloproteinases that contribute to neurovascular injury. Exp Neurol 2008, 210:549-559.
32. MacLellan C.L., Silasi G., Poon C.C., Edmundson C.L., Buist R., Peeling J., Colbourne F. Intracerebral hemorrhage models in rat: comparing collagenase to blood infusion. J Cereb Blood Flow Metab 2008, 28:516-525.
33. Morris B.J., Simpson C.S., Mundell S., Maceachern K., Johnston H.M., Nolan A.M. Dynamic changes in NADPH-diaphorase staining reflect activity of nitric oxide synthase: evidence for a dopaminergic regulation of striatal nitric oxide release. Neuropharmacology 1997, 36:1589-1599.
34. Nilsson O.G., Polito A., Saveland H., Ungerstedt U., Nordstrom C.H. Are primary supratentorial intracerebral hemorrhages surrounded by a biochemical penumbra? A microdialysis study. Neurosurgery 2006, 59:521-528. discussion 521-528.
35. Park W.S., Chang Y.S., Lee M. Effect of 7-nitroindazole on bilirubin-induced changes in brain cell membrane function and energy metabolism in newborn piglets. Biol Neonate 2002, 82:61-65.
36. Qureshi A.I., Ali Z., Suri M.F., Shuaib A., Baker G., Todd K., Guterman L.R., Hopkins L.N. Extracellular glutamate and other amino acids in experimental intracerebral hemorrhage: an in vivo microdialysis study. Crit Care Med 2003, 31:1482-1489.
37. Qureshi A.I., Suri M.F., Ostrow P.T., Kim S.H., Ali Z., Shatla A.A., Guterman L.R., Hopkins L.N. Apoptosis as a form of cell death in intracerebral hemorrhage. Neurosurgery 2003, 52:1041-1047. discussion 1047-1048.
38. Qureshi A.I., Mendelow A.D., Hanley D.F. Intracerebral haemorrhage. Lancet 2009, 373:1632-1644.
39. Schaar K.L., Brenneman M.M., Savitz S.I. Functional assessments in the rodent stroke model. Exp Transl Stroke Med 2010, 2:13.
40. Sharma H.S., Badgaiyan R.D., Alm P., Mohanty S., Wiklund L. Neuroprotective effects of nitric oxide synthase inhibitors in spinal cord injury-induced pathophysiology and motor functions: an experimental study in the rat. Ann N Y Acad Sci 2005, 1053:422-434.
41. Sharma H.S., Wiklund L., Badgaiyan R.D., Mohanty S., Alm P. Intracerebral administration of neuronal nitric oxide synthase antiserum attenuates traumatic brain injury-induced blood-brain barrier permeability, brain edema formation, and sensory motor disturbances in the rat. Acta Neurochir Suppl 2006, 96:288-294.
42. Wakefield I.D., March J.E., Kemp P.A., Valentin J.P., Bennett T., Gardiner S.M. Comparative regional haemodynamic effects of the nitric oxide synthase inhibitors, S-methyl-l-thiocitrulline and L-NAME, in conscious rats. Br J Pharmacol 2003, 139:1235-1243.
43. Wang J., Tsirka S.E. Neuroprotection by inhibition of matrix metalloproteinases in a mouse model of intracerebral haemorrhage. Brain 2005, 128:1622-1633.
44. Wasserman J.K., Schlichter L.C. Minocycline protects the blood-brain barrier and reduces edema following intracerebral hemorrhage in the rat. Exp Neurol 2007, 207:227-237.
45. Wu J., Hua Y., Keep R.F., Nakamura T., Hoff J.T., Xi G. Iron and iron-handling proteins in the brain after intracerebral hemorrhage. Stroke 2003, 34:2964-2969.
46. Xi G., Keep R.F., Hoff J.T. Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol 2006, 5:53-63.
47. Xue M., Hollenberg M.D., Yong V.W. Combination of thrombin and matrix metalloproteinase-9 exacerbates neurotoxicity in cell culture and intracerebral hemorrhage in mice. J Neurosci 2006, 26:10281-10291.
48. Yang S., Chen Y., Deng X., Jiang W., Li B., Fu Z., Du M., Ding R. Hemoglobin-induced nitric oxide synthase overexpression and nitric oxide production contribute to blood-brain barrier disruption in the rat. J Mol Neurosci 2013, 51:352-363.
49. Zhao X., Zhang Y., Strong R., Zhang J., Grotta J.C., Aronowski J. Distinct patterns of intracerebral hemorrhage-induced alterations in NF-kappaB subunit, iNOS, and COX-2 expression. J Neurochem 2007, 101:652-663.
50. Zhou L., Zhu D.Y. Neuronal nitric oxide synthase: structure, subcellular localization, regulation, and clinical implications. Nitric Oxide 2009, 20:223-230.