Cardioprotection and mitochondrial S-nitrosation: Effects of S-nitroso-2-mercaptopropionyl glycine (SNO-MPG) in cardiac ischemia-reperfusion injury

Journal of Molecular and Cellular Cardiology

Volumn 42, Issue 4, 2007, Pages 812-825

  Nadtochiy, Sergiy M ^a   Burwell, Lindsay S ^a   Brookes, Paul S ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Complex I; Experimental therapeutics; MPG; NO donor; Preconditioning; S nitrosothiol

Indexed keywords

NITRIC OXIDE; NITROSO DERIVATIVE; REACTIVE OXYGEN METABOLITE; S NITROSO 2 MERCAPTOPROPIONYL GLYCINE; S NITROSOGLUTATHIONE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CELL RESPIRATION; CONTROLLED STUDY; FEMALE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PERFUSION; HEART PROTECTION; ISCHEMIC PRECONDITIONING; MALE; NITROSATION; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION INJURY;

ANIMALS; CALCIUM; CARDIOTONIC AGENTS; MALE; MEMBRANE POTENTIALS; MITOCHONDRIA, HEART; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; NITROSATION; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; THIOPRONINE;

EID: 34047142614     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2007.01.010     Document Type: Article

References (87)

1. Brookes P.S., Yoon Y., Robotham J.L., Anders M.W., and Sheu S.S. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am. J. Physiol.: Cell Physiol. 287 (2004) C817-C833
2. Hausenloy D.J., and Yellon D.M. The mitochondrial permeability transition pore: its fundamental role in mediating cell death during ischaemia and reperfusion. J. Mol. Cell. Cardiol. 35 (2003) 339-341
3. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341 (1999) 233-249
4. Di Lisa F., and Bernardi P. Mitochondria and ischemia-reperfusion injury of the heart: fixing a hole. Cardiovasc. Res. 70 (2006) 191-199
5. Murry C.E., Jennings R.B., and Reimer K.A. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74 (1986) 1124-1136
6. + channels and myocardial preconditioning. Circ. Res. 84 (1999) 973-979
7. Liu Y., Sato T., Seharaseyon J., Szewczyk A., Rourke O.'B., and Marban E. Mitochondrial ATP-dependent potassium channels. Viable candidate effectors of ischemic preconditioning. Ann. N. Y. Acad. Sci. 874 (1999) 27-37
8. ATP opening on heart mitochondria. Am. J. Physiol.: Heart Circ. Physiol. 290 (2006) H406-H415
9. + leak and ROS generation: an odd couple. Free Radical Biol. Med. 38 (2005) 12-23
10. Nadtochiy S.M., Tompkins A.J., and Brookes P.S. Different mechanisms of mitochondrial proton leak in ischemia-reperfusion injury and preconditioning: implications for pathology and cardioprotection. Biochem. J. 395 (2006) 611-618
11. McLeod C.J., Aziz A., Hoyt Jr. R.F., McCoy Jr. J.P., and Sack M.N. Uncoupling proteins 2 and 3 function in concert to augment tolerance to cardiac ischemia. J. Biol. Chem. 280 (2005) 33470-33476
12. Lebuffe G., Schumacker P.T., Shao Z.H., Anderson T., Iwase H., and Vanden Hoek T.L. ROS and NO trigger early preconditioning: relationship to mitochondrial KATP channel. Am. J. Physiol.: Heart Circ. Physiol. 284 (2003) H299-H308
13. Javadov S.A., Clarke S., Das M., Griffiths E.J., Lim K.H., and Halestrap A.P. Ischaemic preconditioning inhibits opening of mitochondrial permeability transition pores in the reperfused rat heart. J. Physiol. 549 (2003) 513-524
14. Hausenloy D., Wynne A., Duchen M., and Yellon D. Transient mitochondrial permeability transition pore opening mediates preconditioning-induced protection. Circulation 109 (2004) 1714-1717
15. Bell R.M., and Yellon D.M. The contribution of endothelial nitric oxide synthase to early ischaemic preconditioning: the lowering of the preconditioning threshold. An investigation in eNOS knockout mice. Cardiovasc. Res. 52 (2001) 274-280
16. Jones S.P., and Bolli R. The ubiquitous role of nitric oxide in cardioprotection. J. Mol. Cell. Cardiol. 40 (2006) 16-23
17. Laude K., Favre J., Thuillez C., and Richard V. NO produced by endothelial NO synthase is a mediator of delayed preconditioning-induced endothelial protection. Am. J. Physiol.: Heart Circ. Physiol. 284 (2003) H2053-H2060
18. Bolli R. Cardioprotective function of inducible nitric oxide synthase and role of nitric oxide in myocardial ischemia and preconditioning: an overview of a decade of research. J. Mol. Cell. Cardiol. 33 (2001) 1897-1918
19. Ma X.L., Gao F., Liu G.L., Lopez B.L., Christopher T.A., Fukuto J.M., et al. Opposite effects of nitric oxide and nitroxyl on postischemic myocardial injury. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 14617-14622
20. Jneid H., Leessar M., and Bolli R. Cardiac preconditioning during percutaneous coronary interventions. Cardiovasc. Drugs Ther. 19 (2005) 211-217
21. Duranski M.R., Greer J.J., Dejam A., Jaganmohan S., Hogg N., Langston W., et al. Cytoprotective effects of nitrite during in vivo ischemia-reperfusion of the heart and liver55. J. Clin. Invest. 115 (2005) 1232-1240
22. Wang G., Liem D.A., Vondriska T.M., Honda H.M., Korge P., Pantaleon D.M., et al. Nitric oxide donors protect murine myocardium against infarction via modulation of mitochondrial permeability transition. Am. J. Physiol.: Heart Circ. Physiol. 288 (2005) H1290-H1295
23. Carver J., Doctor A., Zaman K., and Gaston B. S-nitrosothiol formation. Methods Enzymol. 396 (2005) 95-105
24. Hess D.T., Matsumoto A., Kim S.O., Marshall H.E., and Stamler J.S. Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell Biol. 6 (2005) 150-166
25. Hogg N. The biochemistry and physiology of S-nitrosothiols. Annu. Rev. Pharmacol. Toxicol. 42 (2002) 585-600
26. Mannick J.B., Schonhoff C., Papeta N., Ghafourifar P., Szibor M., Fang K., et al. S-Nitrosylation of mitochondrial caspases. J. Cell Biol. 154 (2001) 1111-1116
27. Burwell L.S., Nadtochiy S.M., Tompkins A.J., Young S., and Brookes P.S. Direct evidence for S-nitrosation of mitochondrial complex I. Biochem. J. 394 (2006) 627-634
28. Clementi E., Brown G.C., Feelisch M., and Moncada S. Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 7631-7636
29. Chen Q., Hoppel C.L., and Lesnefsky E.J. Blockade of electron transport before cardiac ischemia with the reversible inhibitor amobarbital protects rat heart mitochondria. J. Pharmacol. Exp. Ther. 316 (2006) 200-207
30. Chen Q, Camara A, Stowe DF, Hoppel, CL, Lesnefsky EJ. Modulation of electron transport protects cardiac mitochondria and decreases myocardial injury during ischemia and reperfusion. Am J Physiol Cell Physiol in press.
31. Konorev E.A., Joseph J., Tarpey M.M., and Kalyanaraman B. The mechanism of cardioprotection by S-nitrosoglutathione monoethyl ester in rat isolated heart during cardioplegic ischaemic arrest. Br. J. Pharmacol. 119 (1996) 511-518
32. 35S-2-mercaptopropionylglycine. Yakugaku Zasshi 93 (1973) 112-118
33. Tanonaka K., Iwai T., Motegi K., and Takeo S. Effects of N-(2-mercaptopropionyl)-glycine on mitochondrial function in ischemic-reperfused heart. Cardiovasc. Res. 57 (2003) 416-425
34. Tripathi Y., Hegde B.M., Rai Y.S., and Raghuveer C.V. Effect of N-2-mercaptopropionylglycine in limiting myocardial reperfusion injury following 90 minutes of ischemia in dogs. Indian J. Physiol. Pharmacol. 44 (2000) 290-296
35. {radical dot}. Am. J. Physiol.: Heart Circ. Physiol. 281 (2001) H2261-H2269
36. Tompkins A.J., Burwell L.S., Digerness S.B., Zaragoza C., Holman W.L., and Brookes P.S. Mitochondrial dysfunction in cardiac ischemia-reperfusion injury: ROS from complex I, without inhibition. Biochim. Biophys. Acta 1762 (2006) 223-231
37. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 (1951) 265-275
38. Gladwin M.T., Wang X., Reiter C.D., Yang B.K., Vivas E.X., Bonaventura C., et al. S-Nitrosohemoglobin is unstable in the reductive erythrocyte environment and lacks O2/NO-linked allosteric function. J. Biol. Chem. 277 (2002) 27818-27828
39. Brookes P.S., Salinas E.P., Darley-Usmar K., Eiserich J.P., Freeman B.A., Darley-Usmar V.M., et al. Concentration-dependent effects of nitric oxide on mitochondrial permeability transition and cytochrome c release. J. Biol. Chem. 275 (2000) 20474-20479
40. Borutaite V., Mildaziene V., Brown G.C., and Brand M.D. Control and kinetic analysis of ischemia-damaged heart mitochondria: which parts of the oxidative phosphorylation system are affected by ischemia?. Biochim. Biophys. Acta 1272 (1995) 154-158
41. Jekabsone A., Dapkunas Z., Brown G.C., and Borutaite V. S-nitrosothiol-induced rapid cytochrome c release, caspase activation and mitochondrial permeability transition in perfused heart. Biochem. Pharmacol. 66 (2003) 1513-1519
42. Konorev E.A., Tarpey M.M., Joseph J., Baker J.E., and Kalyanaraman B. S-nitrosoglutathione improves functional recovery in the isolated rat heart after cardioplegic ischemic arrest-evidence for a cardioprotective effect of nitric oxide. J. Pharmacol. Exp. Ther. 274 (1995) 200-206
43. Claycomb W.C., and Palazzo M.C. Culture of the terminally differentiated adult cardiac muscle cell: a light and scanning electron microscope study. Dev. Biol. 80 (1980) 466-482
44. Brookes P.S., Digerness S.B., Parks D.A., and Darley-Usmar V. Mitochondrial function in response to cardiac ischemia-reperfusion after oral treatment with quercetin. Free Radical Biol. Med. 32 (2002) 1220-1228
45. Becker L.B., Vanden Hoek T.L., Shao Z.H., Li C.Q., and Schumacker P.T. Generation of superoxide in cardiomyocytes during ischemia before reperfusion. Am. J. Physiol. 277 (1999) H2240-H2246
46. Jaffrey S.R. Detection and characterization of protein nitrosothiols. Methods Enzymol. 396 (2005) 105-118
47. Borutaite V., Morkuniene R., and Brown G.C. Nitric oxide donors, nitrosothiols and mitochondrial respiration inhibitors induce caspase activation by different mechanisms. FEBS Lett. 467 (2000) 155-159
48. Brown G.C., and Borutaite V. Inhibition of mitochondrial respiratory complex I by nitric oxide, peroxynitrite and S-nitrosothiols. Biochim. Biophys. Acta 1658 (2004) 44-49
49. Brookes PS, Shiva, S, Patel RP, Darley-Usmar VM. Measurement of mitochondrial respiratory thresholds and the control of respiration by nitric oxide. Methods Enzymol 359:305-19.
50. Ng E.S., Jourd'heuil D., McCord J.M., Hernandez D., Yasui M., Knight D., et al. Enhanced S-nitroso-albumin formation from inhaled NO during ischemia/reperfusion. Circ. Res. 94 (2004) 559-565
51. Frost M.T., Wang Q., Moncada S., and Singer M. Hypoxia accelerates nitric oxide-dependent inhibition of mitochondrial complex I in activated macrophages. Am. J. Physiol.: Regul., Integr. Comp. Physiol. 288 (2005) R394-R400
52. Borutaite V., and Brown G.C. S-nitrosothiol inhibition of mitochondrial complex I causes a reversible increase in mitochondrial hydrogen peroxide production. Biochim. Biophys. Acta 1757 (2006) 562-566
53. Schulz R., Kelm M., and Heusch G. Nitric oxide in myocardial ischemia/reperfusion injury. Cardiovasc. Res. 61 (2004) 402-413
54. Jugdutt B.I. Nitric oxide and cardioprotection during ischemia-reperfusion. Heart Fail. Rev. 7 (2002) 391-405
55. Cohen M.V., Yang X.M., and Downey J.M. Nitric oxide is a preconditioning mimetic and cardioprotectant and is the basis of many available infarct-sparing strategies. Cardiovasc. Res. 70 (2006) 231-239
56. Horwitz L.D., Fennessey P.V., Shikes R.H., and Kong Y. Marked reduction in myocardial infarct size due to prolonged infusion of an antioxidant during reperfusion. Circulation 89 (1994) 1792-1801
57. Fuchs J., Veit P., and Zimmer G. Uncoupler- and hypoxia-induced damage in the working rat heart and its treatment. II. Hypoxic reduction of aortic flow and its reversal. Basic Res. Cardiol. 80 (1985) 231-240
58. Vanden-Hoek T., Becker L.B., Shao Z.H., Li C.Q., and Schumacker P.T. Preconditioning in cardiomyocytes protects by attenuating oxidant stress at reperfusion. Circ. Res. 86 (2000) 541-548
59. Tanaka M., Fujiwara H., Yamasaki K., and Sasayama S. Superoxide dismutase and N-2-mercaptopropionyl glycine attenuate infarct size limitation effect of ischaemic preconditioning in the rabbit. Cardiovasc. Res. 28 (1994) 980-986
60. ATP channel-independent targets of diazoxide and 5-hydroxydecanoate in the heart. J. Physiol. 542 (2002) 735-741
61. Wyatt K.M., Skene C., Veitch K., Hue L., and McCormack J.G. The antianginal agent ranolazine is a weak inhibitor of the respiratory complex I, but with greater potency in broken or uncoupled than in coupled mitochondria. Biochem. Pharmacol. 50 (1995) 1599-1606
62. ATP channel. Am. J. Physiol.: Heart Circ. Physiol. 280 (2001) H2406-H2411
63. Turan N., Csonka C., Csont T., Giricz Z., Fodor G., Bencsik P., et al. The role of peroxynitrite in chemical preconditioning with 3-nitropropionic acid in rat hearts. Cardiovasc. Res. 70 (2006) 384-390
64. Pan T.T., Feng Z.N., Lee S.W., Moore P.K., and Bian J.S. Endogenous hydrogen sulfide contributes to the cardioprotection by metabolic inhibition preconditioning in the rat ventricular myocytes. J. Mol. Cell. Cardiol. 40 (2006) 119-130
65. Khan A.A., Schuler M.M., Prior M.G., Yong S., Coppock R.W., Florence L.Z., et al. Effects of hydrogen sulfide exposure on lung mitochondrial respiratory chain enzymes in rats. Toxicol. Appl. Pharmacol. 103 (1990) 482-490
66. Stein A.B., Guo Y., Tan W., Wu W.J., Zhu X., Li Q., et al. Administration of a CO-releasing molecule induces late preconditioning against myocardial infarction. J. Mol. Cell. Cardiol. 38 (2005) 127-134
67. Vogt A.M., Poolman M., Ackermann C., Yildiz M., Schoels W., Fell D.A., et al. Regulation of glycolytic flux in ischemic preconditioning. A study employing metabolic control analysis. J. Biol. Chem. 277 (2002) 24411-24419
68. Vedia L., McDonald B., Reep B., Brune B., Di S.M., Billiar T.R., et al. Nitric oxide-induced S-nitrosylation of glyceraldehyde-3-phosphate dehydrogenase inhibits enzymatic activity and increases endogenous ADP-ribosylation. J. Biol. Chem. 267 (1992) 24929-24932
69. 2+ overload. Am. J. Physiol.: Heart Circ. Physiol. 288 (2005) H1900-H1908
70. 2+ overloading, trigger pH- and mitochondrial permeability transition-dependent death of adult rat myocytes after ischemia-reperfusion. Am. J. Physiol.: Heart Circ. Physiol. 290 (2006) H2024-H2034
71. Griffiths E.J., and Halestrap A.P. Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion. Biochem. J. 307 (1995) 93-98
72. Digerness S.B., Brookes P.S., Goldberg S.P., Katholi C.R., and Holman W.L. Modulation of mitochondrial adenosine triphosphate-sensitive potassium channels and sodium-hydrogen exchange provide additive protection from severe ischemia-reperfusion injury. J. Thorac. Cardiovasc. Surg. 125 (2003) 863-871
73. 2+ exchanger inhibitor, reduces calcium overload induced by ischemia and reperfusion in mouse ventricular myocytes. Physiol Res in press.
74. Hardy L., Clark J.B., Darley-Usmar V.M., Smith D.R., and Stone D. Reoxygenation-dependent decrease in mitochondrial NADH:CoQ reductase (Complex I) activity in the hypoxic/reoxygenated rat heart. Biochem. J. 274 (1991) 133-137
75. Zhao K., Zhao G.M., Wu D., Soong Y., Birk A.V., Schiller P.W., et al. Cell-permeable peptide antioxidants targeted to inner mitochondrial membrane inhibit mitochondrial swelling, oxidative cell death, and reperfusion injury. J. Biol. Chem. 279 (2004) 34682-34690
76. Adlam V.J., Harrison J.C., Porteous C.M., James A.M., Smith R.A., Murphy M.P., et al. Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury. FASEB J. 19 (2005) 1088-1095
77. 2+ channel α1 subunit and reduced ischemia/reperfusion injury. Circ. Res. 98 (2006) 403-411
78. 2 sensor and NO signaling functions. Cell 102 (2000) 499-509
79. Haendeler J., Hoffmann J., Tischler V., Berk B.C., Zeiher A.M., and Dimmeler S. Redox regulatory and anti-apoptotic functions of thioredoxin depend on S-nitrosylation at cysteine 69. Nat. Cell Biol. 4 (2002) 743-749
80. Gow A.J., and Stamler J.S. Reactions between nitric oxide and haemoglobin under physiological conditions. Nature 391 (1998) 169-173
81. Dahlem Y.A., Horn T.F., Buntinas L., Gonoi T., Wolf G., and Siemen D. The human mitochondrial KATP channel is modulated by calcium and nitric oxide: a patch-clamp approach. Biochim. Biophys. Acta 1656 (2004) 46-56
82. Sasaki N., Sato T., Ohler A., O'Rourke B., and Marban E. Activation of mitochondrial ATP-dependent potassium channels by nitric oxide. Circulation 101 (2000) 439-445
83. Yoshida T., Inoue R., Morii T., Takahashi N., Yamamoto S., Hara Y., et al. Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat. Chem. Biol. 2 (2006) 596-607
84. Trinchieri A., Dormia G., Montanari E., and Zanetti G. Cystinuria: definition, epidemiology and clinical aspects. Arch. Ital. Urol. Androl. 76 (2004) 129-134
85. Webb A., Bond R., McLean P., Uppal R., Benjamin N., and Ahluwalia A. Reduction of nitrite to nitric oxide during ischemia protects against myocardial ischemia-reperfusion damage. Proc. Natl. Acad. Sci. U. S. A. 101 (2004 (Sep)) 13683-13688
86. Huang Z., Shiva S., Kim-Shapiro D.B., Patel R.P., Ringwood L.A., Irby C.E., et al. Enzymatic function of hemoglobin as a nitrite reductase that produces NO under allosteric control. J. Clin. Invest. 115 (2005) 2099-2107
87. Castello P.R., David P.S., McClure T., Crook Z., and Poyton R.O. Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes. Cell Metab. 3 (2006) 277-287