Preconditioning with a novel metallopharmaceutical NO donor in anesthetized rats subjected to brain ischemia/reperfusion

Neurochemical Research

Volumn 37, Issue 4, 2012, Pages 749-758

  Campelo, Marcio Wilker Soares ^a   Oriá, Reinaldo Barreto ^a   Lopes De França, Luiz Gonzaga ^a   De Castro Brito, Gerly Anne ^a   Dos Santos, Armenio Aguiar ^a   De Vasconcelos, Raquel Cavalcante ^a   Da Silva, Francisco Ordelei Nascimento ^a   Nobrega, Beatrice Nuto ^a   Bento Silva, Moisés Tolentino ^a   De Vasconcelos, Paulo Roberto Leitão ^a  

^a FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

Author keywords

Brain; Ischemia reperfusion; Nitric oxide; Nitrosyl ruthenium complex; Nuclear factor B

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NITRATE; NITRIC OXIDE DONOR; NITRITE; NITROSYL RUTHENIUM COMPLEX; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CAROTID ARTERY OBSTRUCTION; CONTROLLED STUDY; HIPPOCAMPUS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; ISCHEMIC PRECONDITIONING; MALE; MEAN ARTERIAL PRESSURE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPERFUSION; WESTERN BLOTTING;

ANESTHESIA; ANIMALS; BRAIN; BRAIN ISCHEMIA; ISCHEMIC PRECONDITIONING; MALE; NEUROPROTECTIVE AGENTS; NITRIC OXIDE DONORS; RATS; RATS, WISTAR; REACTIVE NITROGEN SPECIES; REPERFUSION INJURY; RUTHENIUM COMPOUNDS;

RATTUS;

EID: 84862841826     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-011-0669-x     Document Type: Article

References (61)

1. Kung HC, Hoyert DL, Xu J, Murphy SL (2008) Deaths: final data for 2005. National Vital Statistics Reports 56:1-120
2. Dawson VL, Dawson TM (1998) Nitric oxide in neurodegeneration. Prog Brain Res 118:215-229 (Pubitemid 28530669)
3. Dawson VL, Dawson TM (1995) Physiological and toxicological actions of nitric oxide in the central nervous system. Adv Pharmacol 34:323-342
4. Willmot M, Gibson C, Gray L, Murphy S, Bath P (2005) Nitric oxide synthase inhibitors in experimental ischemic stroke and their effects on infarct size and cerebral blood flow: a systematic review. Free Radic Biol Med 39:412-425 (Pubitemid 40916222)
5. Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G (1987) Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 84:9265-9269
6. Dimmeler S, Haendeler J, Nehls M, Zeiher AM (1997) Suppression of apoptosis by nitric oxide via inhibition of interleukin- 1 b-converting enzyme (ICE)-like and cysteine protease protein (CPP)-32-like proteases. J Exp Med 185:601-607 (Pubitemid 27098145)
7. Rossig L, Haendeler J, Hermann C et al (2000) Nitric oxide down-regulates MKP-3 mRNA levels: involvement in endothelial cell protection from apoptosis. J Biol Chem 275:25502-25507
8. Zhuang P, Ji H, Zhang YH, Min ZL, Ni QG, You R (2010) ZJM-289, a Novel nitric oxide donor, alleviates the cerebral ischemic-reperfusion injury in rats. Clin Exp Pharmacol Physiol 37:e121-e127
9. Ignarro LJ, Cirino G, Casini A, Napoli C (1999) Nitric oxide as a signaling molecule in the vascular system: an overview. J Car-diovasc Pharmacol 34:879-886
10. Ignarro LJ, Napoli C, Loscalzo J (2002) Nitric oxide donors and cardiovascular agents modulating the bioactivity of nitric oxide: an overview. Circ Res 90:21-28 (Pubitemid 34074604)
11. Wainwright MS, Grundhoefer D, Sharma S, Black SM (2007) A nitric oxide donor reduces brain injury and enhances recovery of cerebral blood flow after hypoxia-ischemia in the newborn rat. Neurosci Lett 415:124-129 (Pubitemid 46386325)
12. Khan M, Jatana M, Elango C, Paintlia AS, Singh AK, Singh I (2006) Cerebrovascular protection by various nitric oxide donors in rats after experimental stroke. Nitric Oxide 15:114-124 (Pubitemid 44175884)
13. Zhang R, Zhang L, Zhang Z, Wang Y, Lu M, Lapointe M, Chopp M (2001) A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats. Ann Neurol 50:602-611 (Pubitemid 33021918)
14. Silva FON, Araujo SXB, Holanda AKM, Meyer E, Sales FAM, Diogenes ICN, Carvalho IMM, Moreira IS, Lopes LGF (2006) Synthesis, Characterization, and NO Release Study of the cis- and trans-[Ru(Bpy)2(SO3)(NO)]+ complexes Eur J Inorg Chem 2020-2026
15. Fricker SP, Slade E, Powell NA, Vaughan OJ, Henderson GR, Murrer BA et al (1997) Ruthenium complexes as nitric oxide scavengers: a potential therapeutic approach to nitric oxidemediated diseases. Br J Pharmacol 122:1441-1449 (Pubitemid 27503936)
16. Hutchings SR, Song D, Fricker SP, Pang CC (2005) The ruthenium-based nitric oxide scavenger, AMD6221, augments cardiovascular responsiveness to noradrenaline in rats with streptozotocin-induced diabetes. Eur J Pharmacol 528:132-136 (Pubitemid 41773663)
17. Silva JJN, Guedes PMM, Zottis A, Balliano TL, Silva FON, Lopes LGF, Ellena J, Oliva G, Andricopulo AD, Franco DW, Silva JS (2010) Novel ruthenium complexes as potential drugs for Chagas's disease: enzyme inhibition and in vitro/in vivo trypanocidal activity. Br J Pharmacol 160:260-269
18. Cerqueira JB, Silva LF, Lopes LG, Moraes ME, Nascimento NR (2008) Relaxation of rabbit corpus cavernosum smooth muscle and aortic vascular endothelium induced by new nitric oxide donor substances of the nitrosyl-ruthenium complex. Int Braz J Urol 34:638-646
19. Silva FO, Candido MC, Holanda AK, Diogenes IC, Sousa EH, Lopes LG (2011) Mechanism and biological implications of the NO release of cis-[Ru(bpy)2L(NO)]n+ complexes: a key role of physiological thiols. J Inorg Biochem 105:624-629
20. Bonaventura D, de Lima RG, Vercesi JA, da Silva RS, Bendhack LM (2007) Comparison of the mechanisms underlying the relaxation induced by two nitric oxide donors: sodium nitro-prusside and a new ruthenium complex. Vascul Pharmaco 46:215-222 (Pubitemid 46096814)
21. Muniz LRF, Faria MHG, Vasconcelos PRL (2004) Metabolic evaluation of ischemic and reperfusion brain injury following bilateral occlusion of common carotid arteries: an experimental study in rats. Acta Cir Bras 19:529-534
22. Ibayashi S, Nagao T, Kitazono T, Ooboshi H, Kitayama J, Sa- doshima S, Fujishima M (2000) Calcium antagonist is radipine reduces metabolic alterations in acute cerebral ischemia in spontaneously hypertensive rats. Neurochem Res 25:349-355 (Pubitemid 30161480)
23. Li Z, Wang Y, Xie Y, Yang Z, Zhang T (2011) Protective effects of exogenous hydrogen sulfide on neurons of hippocampus in a rat model of brain ischemia. Neurochem Res 36:1840-1849
24. Paxinos G, Watson C (2004) The rat brain in stereotaxic coordinates, 5th edn. Elsevier Academic Press, Burlington
25. Joshi CN, Jain SK, Murthy PS (2004) An optimized triphenyl-tetrazolium chloride method for identification of cerebral infarcts. Brain Res Brain Res Protoc 13:11-17 (Pubitemid 38519594)
26. Bederson JB, Pitts LH, Germano SM, Nishimura MC, Davis RL, Bartkowski HM (1986) Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats. Stroke 17:1304-1308 (Pubitemid 17008976)
27. Benedek A, Moricz K, Juranyi Z, Gigler G, Levay G, Harsing LG Jr et al (2006) Use of TTC staining for the evaluation of tissue injury in the early phases of reperfusion after focal cerebral ischemia in rats. Brain Res 1116:159-165 (Pubitemid 44485008)
28. Isayama K, Pitts LH, Nishimura MC (1991) Evaluation of 2, 3, 5-triphenyltetrazolium chloride staining to delineate rat brain infarcts. Stroke 22:1394-1398
29. Leinonen JS, Ahonen JP, Lonnrot K, Jehkonen M, Dastidar P, Molnar G, Alho H (2000) Low plasma antioxidant activity is associated with high lesion volume and neurological impairment in stroke. Stroke 31:33-39 (Pubitemid 30035749)
30. Goldlust EJ, Paczynski RP, He YY, Hsu CY, Goldberg MP (1996) Automated measurement of infarct size with scanned images of triphenyltetrazolium chloride-stained rat brains. Stroke 27:1657-1662 (Pubitemid 26295920)
31. Kaku Y, Yonekawa Y, Tsukahara T, Ogata N, Kimura T, Taniguchi T (1993) Alterations of a 200 kDa Neurofilament in the Rat Hippocampus after Forebrain Ischemia. J Cereb Blood Flow Metab 13:402-408 (Pubitemid 23129393)
32. Green LC, Wagner DA, Glogowski J (1982) Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem 126:131-138 (Pubitemid 13203451)
33. Irmak MK, Fadillioglu E, Sogut S, Erdogan H, Gulec M, Ozer M, Yagmurca M, Gozukara ME (2003) Effects of caffeic acid phenethyl ester and alpha-tocopherol on reperfusion injury in rat brain. Cell Biochem Funct 21:283-289 (Pubitemid 36988383)
34. Dirnagl U, Iadecola C, Moskowitz MA (1999) Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22: 391-397 (Pubitemid 29453643)
35. Lo EH, Moskowitz MA, Jacobs TP (2005) Exciting, radical, suicidal: how brain cells die after stroke. Stroke 36:189-192 (Pubitemid 40170779)
36. Prieto-Arribas R, Pascual-Garvi JM, Gonzalez-Llanos F, Roda JM (2011) How to repair an ischemic brain injury? Value of experimental models in search of answers. Neurologia 26:65-73
37. Pluta RM, Rak R, Wink DA, Woodward JJ, Khaldi A, Oldfield EH, Watson JC (2001) Effects of nitric oxide on reactive oxygen species production and infarction size after brain reperfusion injury. Neurosurgery 48:884-892
38. Zhang D, Dhillon HS, Mattson MP, Yurek DM, Prasad RM (1999) Immunohistochemical detection of the lipid peroxidation product 4-hydroxynonenal after experimental brain injury in the rat. Neurosci Lett 272:57-61
39. Gaur V, Kumar A (2010) Protective effect of desipramine, ven- lafaxine and trazodone against experimental animal model of transient global ischemia: possible involvement of NO-cGMP pathway. Brain Res 1353:204-212
40. Buisson A, Plotkine M, Boulu RG (1992) The neuroprotective effect of a nitric oxide inhibitor in a rat model of focal cerebral ischaemia. Br J Pharmacol 106:766-767
41. Lei H, Grinberg O, Nwaigwe CI, Hou HG, Williams H, Swartz HM, Dunn JF (2001) The effects of ketamine-xylazine anesthesia on cerebral blood flow and oxygenation observed using nuclear magnetic resonance perfusion imaging and electron paramagnetic resonance oximetry. Brain Res 913:174-179 (Pubitemid 32817063)
42. Stein AB, Tiwari S, Thomas P, Hunt G, Levent C, Stoddard MF, Tang XL, Bolli R, Dawn B (2007) Effects of anesthesia on echocardiographic assessment of left ventricular structure and function in rats. Basic Res Cardiol 102:28-41 (Pubitemid 44932769)
43. Levine S (1960) Anoxic-ischemic encephalopathy in rats. Am J Pathol 36:1-17
44. Lipton P (1999) Ischemic cell death in brain neurons. Physiol Rev 79:1431-1568 (Pubitemid 29473320)
45. He Z, Ibayashi S, Sugimori H, Fujii K, Sadoshima S, Fujishima M (1997) Age-related ischemia in the brain following bilateral carotid artery occlusion-collateral blood flow and brain metabolism. Neurochem Res 22:37-42 (Pubitemid 27081989)
46. Glenner GG (1969) Tetrazolium salts. In: Lillie RD (ed) H.J. Con's biological stains. Williams and Wilkins, Baltimore, pp 154-162
47. Li F, Irie K, Anwer MS, Fisher M (1997) Delayed triphenyltet-razolium chloride staining remains useful for evaluating cerebral infarct volume in a rat stroke model. J Cereb Blood Flow Metab 17:1132-1135 (Pubitemid 27459342)
48. Marshall RS, Lazar RM, Pile-Spellman J, Young WL, Duong DH, Joshi S, Ostapkovich N (2001) Recovery of brain function during induced cerebral hypoperfusion. Brain 124:1208-1217 (Pubitemid 32510388)
49. Willmot MR, Bath PM (2003) The potential of nitric oxide therapeutics in stroke. Expert Opin Investig Drugs 12:455-470 (Pubitemid 36336415)
50. Sanchez A, Fernandez N, Monge L, Salcedo A, Climent B, Luis Garcia-Villalon A, Diequez G (2006) Goat cerebrovascular reactivity to ADP after ischemia-reperfusion. Role of nitric oxide, prostanoids and reactive oxygen species. Brain Res 1120: 114-123 (Pubitemid 44648006)
51. Wieraszkoa A, Clarkeb MJ, Langb DR, Lopes LGF, Franco DW (2001) The influence of NO-containing ruthenium complexes on mouse hippocampal evoked potentials in vitro. Life Sci 68:1535-1544 (Pubitemid 32168081)
52. Tardini DMS, Winston BY, Novelli ELB, Sequeira JL (2003) Evaluation of two brain ischemia and reperfusion experimental models in rats with carotid temporary occlusion associated or not to vertebral occlusion. Acta Cir Bras 18:514-517
53. De La Torre JC, Aliev G (2005) Inhibition of vascular nitric oxide after rat chronic brain hypoperfusion: spatial memory and immunocytochemical changes. J Cereb Blood Flow Metab 25: 663-672 (Pubitemid 40705602)
54. Greco R, Mangione AS, Amantea D, Bagetta G, Nappi G, Tassorelli C (2011) IkappaB-alpha expression following transient focal cerebral ischemia is modulated by nitric oxide. Brain Res 1372:145-151
55. Kaltschmidt B, Heinrich M, Kaltschmidt C (2002) Stimulus-dependent activation of NF-kappaB specifies apoptosis or neuroprotection in cerebellar granule cells. Neuromolecular Med 2:299-309 (Pubitemid 37070589)
56. Medling BD, Bueno R, Chambers C, Neumeister MW (2010) The effect of vitamin E succinate on ischemia reperfusion injury. Hand 5:60-64
57. Wang Q, Tang XN, Yenari MA (2007) The inflammatory response in stroke. J Neuroimmunol 184:53-68 (Pubitemid 46365991)
58. Desai A, Singh N, Raghubir R (2010) Neuroprotective potential of the NF-KB inhibitor peptide IKK-NBD in cerebralischemia-reperfusion injury. Neurochem Int 57:876-883
59. Lefer AM, Lefer DJ (1993) Pharmacology of the endothelium in ischemia-reperfusion and circulatory shock. Annu Rev Pharmacol Toxicol 33:71-90 (Pubitemid 23116001)
60. Thiagarajan RR, Winn RK, Harlan JM (1997) The role of leukocyte and endothelial adhesion molecules in ischemia-reperfu-sion injury. Thromb Haemost 78:310-314 (Pubitemid 27289260)
61. Goto S, Xue R, Sugo N, Sawada M, Blizzard KK, Poitras MF, Johns DC, Dawson TM, Dawson VL, Crain BJ, Traystman RJ, Mori S, Hurn PD (2002) Poly(ADP-ribose) polymerase impairs early and long-term experimental stroke recovery. Stroke 33: 1101-1106 (Pubitemid 34293598)