Ischaemic preconditioning preferentially increases protein S-nitrosylation in subsarcolemmal mitochondria

Cardiovascular Research

Volumn 106, Issue 2, 2015, Pages 227-236

  Sun, Junhui ^a   Nguyen, Tiffany ^a   Aponte, Angel M ^a   Menazza, Sara ^a   Kohr, Mark J ^a,b   Roth, David M ^c   Patel, Hemal H ^c   Murphy, Elizabeth ^a   Steenbergen, Charles ^b  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b DEPARTMENT OF PATHOLOGY   (United States)

^c University of California   (United States)

Author keywords

Caveolae; Ischaemic preconditioning; Protein S nitrosylation; Subsarcolemmal and interfibrillar mitochondria

Indexed keywords

BIOTIN; CAVEOLIN 3; CONNEXIN 43; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MALEIMIDE; NITRIC OXIDE; NOS3 PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; CAVEOLA; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DECOMPOSITION; HEART PERFUSION; HEART PROTECTION; ISCHEMIC PRECONDITIONING; ISOLATED HEART; MALE; MITOCHONDRION; MITOCHONDRION SWELLING; MOUSE; NITROSYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; SIGNAL TRANSDUCTION; SUBSARCOLEMMAL MITOCHONDRION; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE; GENETICS; HEART INFARCTION PREVENTION; HEART MITOCHONDRION; METABOLISM; PROCEDURES; PROTEIN PROCESSING; SARCOLEMMA;

ANIMALS; CAVEOLIN 3; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MALE; MICE, INBRED C57BL; MITOCHONDRIA, HEART; MYOCARDIUM; NITRIC OXIDE SYNTHASE TYPE III; PROTEIN PROCESSING, POST-TRANSLATIONAL; SARCOLEMMA;

EID: 84929071944     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvv044     Document Type: Article

References (50)

1. Murphy E, Steenbergen C. Preconditioning: the mitochondrial connection. Annu Rev Physiol 2007;69:51-67.
2. Penna C, Perrelli MG, Pagliaro P. Mitochondrial pathways, permeability transition pore, and redox signaling in cardioprotection: therapeutic implications. Antioxid Redox Signal 2012;18:556-599.
3. Garlid KD, Costa AD, Quinlan CL, Pierre SV, Dos Santos P. Cardioprotective signaling to mitochondria. J Mol Cell Cardiol 2009;46:858-866.
4. Quinlan CL, Costa ADT, Costa CL, Pierre SV, Dos Santos P, Garlid KD. Conditioning the heart induces formation of signalosomes that interact with mitochondria to open mito-KATP channels. Am J Physiol 2008;295:H953-H961.
5. Wang J, Schilling JM, Niesman IR, Headrick JP, Finley JC, Kwan E, Patel PM, Head BP, Roth DM, Yue Y, Patel HH. Cardioprotective trafficking of caveolin to mitochondria is Gi-protein dependent. Anesthesiology 2014;121:538-548.
6. Wong R, Aponte AM, Steenbergen C, Murphy E. Cardioprotection leads to novel changes in the mitochondrial proteome. Am J Physiol 2010;298:H75-H91.
7. Horikawa YT, Patel HH, Tsutsumi YM, Jennings MM, Kidd MW, Hagiwara Y, Ishikawa Y, Insel PA, Roth DM. Caveolin-3 expression and caveolae are required for isoflurane-induced cardiac protection from hypoxia and ischemia/reperfusion injury. J Mol Cell Cardiol 2008;44:123-130.
8. Sun J, Kohr MJ, Nguyen T, Aponte AM, Connelly PS, Esfahani SG, Gucek M, Daniels MP, Steenbergen C, Murphy E. Disruption of caveolae blocks ischemic preconditioning-mediated S-nitrosylation of mitochondrial proteins. Antioxid Redox Signal 2012;16: 45-56.
9. Tsutsumi YM, Horikawa YT, Jennings MM, Kidd MW, Niesman IR, Yokoyama U, Head BP, Hagiwara Y, Ishikawa Y, Miyanohar A, Patel PM, Insel PA, Patel HH, Roth DM. Cardiac-specific overexpression of caveolin-3 induces endogenous cardiac protection by mimicking ischemic preconditioning. Circulation 2008;118:1979-1988.
10. Fridolfsson HN, Kawaraguchi Y, Ali SS, Panneerselvam M, Niesman IR, Finley JC, Kellerhals SE, Migita MY, Okada H, Moreno AL, Jennings M, Kidd MW, Bonds JA, Balijepalli RC, Ross RS, Patel PM, Miyanohara A, Chen Q, Lesnefsky EJ, Head BP, Roth DM, Insel PA, Patel HH. Mitochondria-localized caveolin in adaptation to cellular stress and injury. FASEB J 2012;26:4637-4649.
11. Insel PA, Head BP, Ostrom RS, Patel HH, Swaney JS, Tang CM, Roth DM. Caveolae and lipid rafts: G protein-coupled receptor signaling microdomains in cardiac myocytes. Ann N Y Acad Sci 2005;1047:166-172.
12. Patel HH, Murray F, Insel PA. Caveolaeas organizers of pharmacologically relevant signal transduction molecules. Annu Rev Pharmacol Toxicol 2008;48:359-391.
13. Feron O, Balligand J-L. Caveolins and the regulation ofendothelial nitric oxide synthase in the heart. Cardiovasc Res 2006;69:788-797.
14. Michel T, Vanhoutte P. Cellular signaling and NO production. Pflügers Arch 2010;459: 807-816.
15. Post H, Schulz R, Behrends M, Gres P, Umschlag C, Heusch G. No involvement of endogenous nitric oxide in classical ischemic preconditioning in swine. J Mol Cell Cardiol 2000;32:725-733.
16. Nakano A, Liu GS, Heusch G, Downey JM, Cohen MV. Exogenousnitric oxidecantrigger a preconditioned state through a free radical mechanism, but endogenous nitric oxide is notatriggerof classical ischemic preconditioning. J Mol Cell Cardiol 2000;32:1159-1167.
17. Guo Y, Li Q, WuW-J, Tan W, Zhu X, Mu J, Bolli R. Endothelial nitric oxide synthaseisnot necessary for the early phase of ischemic preconditioning in the mouse. J Mol Cell Cardiol 2008;44:496-501.
18. Talukder MAH, Yang F, Shimokawa H, Zweier JL. eNOS is required for acute in vivo is-chemic preconditioning of the heart: effects of ischemic duration and sex. Am J Physiol 2010;299:H437-H445.
19. 2S and CO in myocardial ischaemia/reperfusion injury and cardioprotection by preconditioning, postconditioning and remote conditioning. Br J Pharmacol 2014; doi: 10.1111/bph.12811.
20. Lima B, Forrester MT, Hess DT, Stamler JS. S-Nitrosylation in cardiovascular signaling. Circ Res 2010;106:633-646.
21. Schulman IH, Hare JM. Regulationofcardiovascular cellular processes by S-nitrosylation. Biochim Biophys Acta 2012;1820:752-762.
22. Sun J, Murphy E. Protein S-nitrosylation and cardioprotection. Circ Res 2010;106: 285-296.
23. Sun J. Protein S-nitrosylation: a role of nitric oxide signaling in cardiac ischemic preconditioning. Acta Physiol Sin 2007;59:544-552.
24. Palmer JW, Tandler B, Hoppel CL. Biochemical properties of subsarcolemmal and inter-fibrillarmitochondria isolated from rat cardiac muscle.JBiol Chem 1977;252:8731-8739.
25. Riva A, Tandler B, Loffredo F, Vazquez E, Hoppel C. Structural differences in two biochemically defined populations of cardiac mitochondria. Am J Physiol 2005;289: H868-H872.
26. Chang AHK, Sancheti H, Garcia J, Kaplowitz N, Cadenas E, Han D. Respiratory substrates regulate S-nitrosylation of mitochondrial proteins through a thiol-dependent pathway. Chem Res Toxicol 2014;27:794-804.
27. Boengler K, Stahlhofen S, van de Sand A, Gres P, Ruiz-Meana M, Garcia-Dorado D, Heusch G, Schulz R. Presence of connexin 43 in subsarcolemmal, but not in interfibrillar cardiomyocyte mitochondria. Basic Res Cardiol 2009;104:141-147.
28. Jaffrey SR, Snyder SH. The biotin switch method for the detection of S-nitrosylated proteins. Sci STKE 2001;86:PL1.
29. Sun J, Morgan M, Shen R-F, Steenbergen C, Murphy E. Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport. Circ Res 2007;101:1155-1163.
30. Lin J, Steenbergen C, Murphy E, Sun J. Estrogen receptor-b activation results in S-nitrosylation of proteins involved in cardioprotection. Circulation 2009;120:245-254.
31. Tong G, Aponte AM, Kohr MJ, Steenbergen C, Murphy E, Sun J. Postconditioning leads to an increase in protein S-nitrosylation. Am J Physiol 2014;306:H825-H832.
32. Kohr MJ, Sun J, Aponte A, Wang G, Gucek M, Murphy E, Steenbergen C. Simultaneous measurement of protein oxidation and S-nitrosylation during preconditioning and ische-mia/reperfusion injury with resin-assisted capture. Circ Res 2011;108:418-426.
33. Shaul PW. Regulation of endothelial nitric oxide synthase: location, location, location. Annu Rev Physiol 2002;64:749-774.
34. Dessy C, Feron O, Balligand J-L. The regulation of endothelial nitric oxide synthase by caveolin: a paradigm validated in vivo and shared by the 'endothelium-derived hyperpo-larizing factor'. Pflügers Arch 2010;459:817-827.
35. Feron O, Belhhassen L, Kobzik L, Smith TW, Kelly RA, Michel T. Endothelial nitric oxide synthase targeting to caveolae. Specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. J Biol Chem 1996;271:22810-22814.
36. Song KS, Scherer PE, Tang Z, Okamoto T, Li S, Chafel M, Chu C, Kphtz DS, Lisanti MP. Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the sarcolemma and co-fractionates with dystrophin and dystrophin-associated glycoproteins. J Biol Chem 1996;271:15160-15165.
37. Boengler K, Dodoni G, Rodriguez-Sinovas A, Cabestrero A, Ruiz-Meana M, Gres P, Konietzka I, Lopez-Iglesias C, Carcia-Dorado D, Di Lisa F, Heusch G, Schulz R. Connexin 43 in cardiomyocyte mitochondria and its increase by ischemic preconditioning. Cardio-vasc Res 2005;67:234-244.
38. Sun J, Aponte AM, Kohr MJ, Tong G, Steenbergen C, Murphy E. Essential role of nitric oxide in acute ischemic preconditioning: S-Nitros(yl)ation versus sGC/cGMP/PKG signaling? Free Radic Biol Med 2013;54:105-112.
39. Palmer JW, Tandler B, Hoppel CL. Heterogeneous response of subsarcolemmal heart mitochondria to calcium. Am J Physiol 1986;250:H741-H748.
40. Chen Q, Paillard M, Gomez L, Li H, Hu Y, Lesnefsky EJ. Postconditioning modulates ischemia-damaged mitochondria during reperfusion. J Cardiovasc Pharmacol 2012;59: 101-108.
41. Jennings RB. Historical perspectiveonthe pathologyof myocardial ischemia/reperfusion injury. Circ Res 2013;113:428-438.
42. Khan M, Cheema Y, Shahbaz A, Ahokas R, Sun Y, Gerling I, Bhattacharya SK, Weber KT. Mitochondria play a central role in nonischemic cardiomyocyte necrosis: common to acute and chronic stressor states. Pflügers Arch 2012;464:123-131.
43. Hoppel CL, Tandler B, Fujioka H, Riva A. Dynamic organization of mitochondria in human heart and in myocardial disease. Int J Biochem Cell Biol 2009;41:1949-1956.
44. Holmuhamedov EL, Oberlin A, Short K, Terzic A, Jahangir A. Cardiac subsarcolemmal and interfibrillar mitochondria display distinct responsiveness to protection by diazox-ide. PLoS One 2012;7:e44667.
45. Kohr MJ, Aponte A, Sun J, Gucek M, Steenbergen C, Murphy E. Measurement of S-nitrosylation occupancy in the myocardium with cysteine-reactive tandem mass tags. Circ Res 2012;111:1308-1312.
46. Iwakiri Y, Satoh A, Chatterjee S, Toomre DK, Chalouni CM, Fulton D, Groszmann RJ, Shah VH, Sessa WC. Nitric oxide synthase generates nitric oxide locallytoregulate compartmentalized protein S-nitrosylation and protein trafficking. Proc Natl Acad Sci USA 2006;103:19777-19782.
47. Maniatis NA, Brovkovych V, Allen SE, John TA, Shajahan AN, Tiruppathi C, Vogel SM, Skidgel RA, Malik AB, Minshall RD. Novel mechanism of endothelial nitric oxide synthase activation mediated by caveolae internalization in endothelial cells. Circ Res 2006;99:870-877.
48. Sanchez FA, Rana R, Kim DD, Iwahashi T, Zheng R, Lal BK, Gordon DM, Meininger CJ, Duran WN. Internalization of eNOS and NO delivery to subcellular targets determine agonist-induced hyperpermeability. Proc Natl Acad Sci USA 2009;106:6849-6853.
49. Ruiz-Meana M, Nunez E, Miro-Casas E, Martinez-Acedo P, Barba I, Rodriguez-Sinovas A, Inserte J, Fernandez-Sanz C, Hernando V, Vazquez J, Garcia-Dorado D. Ischemic preconditioning protects cardiomyocyte mitochondria through mechanisms independent of cytosol. J Mol Cell Cardiol 2014;68:79-88.
50. Wang S-B, Foster DB, Rucker J, O'Rourke B, Kass DA, Van Eyk JE. Redox regulation of mitochondrial ATP synthase: implications for cardiac resynchronization therapy. Circ Res 2011;109:750-757.