Increased protein S-nitrosylation in mitochondria: a key mechanism of exercise-induced cardioprotection.
Ischemia–reperfusion
Nitric oxide
S-Nitrosylation
mPTP
Journal
Basic research in cardiology
ISSN: 1435-1803
Titre abrégé: Basic Res Cardiol
Pays: Germany
ID NLM: 0360342
Informations de publication
Date de publication:
23 12 2021
23 12 2021
Historique:
received:
25
01
2021
accepted:
17
12
2021
revised:
16
12
2021
entrez:
23
12
2021
pubmed:
24
12
2021
medline:
14
1
2022
Statut:
epublish
Résumé
Endothelial nitric oxide synthase (eNOS) activation in the heart plays a key role in exercise-induced cardioprotection during ischemia-reperfusion, but the underlying mechanisms remain unknown. We hypothesized that the cardioprotective effect of exercise training could be explained by the re-localization of eNOS-dependent nitric oxide (NO)/S-nitrosylation signaling to mitochondria. By comparing exercised (5 days/week for 5 weeks) and sedentary Wistar rats, we found that exercise training increased eNOS level and activation by phosphorylation (at serine 1177) in mitochondria, but not in the cytosolic subfraction of cardiomyocytes. Using confocal microscopy, we confirmed that NO production in mitochondria was increased in response to H
Identifiants
pubmed: 34940922
doi: 10.1007/s00395-021-00906-3
pii: 10.1007/s00395-021-00906-3
doi:
Substances chimiques
Protein S
0
Nitric Oxide
31C4KY9ESH
Hydrogen Peroxide
BBX060AN9V
Nitric Oxide Synthase Type III
EC 1.14.13.39
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
66Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany.
Références
Amanakis G, Sun J, Fergusson MM, McGinty S, Liu C, Molkentin JD, Murphy E (2021) Cysteine 202 of cyclophilin D is a site of multiple post-translational modifications and plays a role in cardioprotection. Cardiovasc Res. https://doi.org/10.1093/cvr/cvaa053
doi: 10.1093/cvr/cvaa053
pubmed: 32129829
Andersson DC, Fauconnier J, Yamada T, Lacampagne A, Zhang S-J, Katz A, Westerblad H (2011) Mitochondrial production of reactive oxygen species contributes to the β-adrenergic stimulation of mouse cardiomycytes. J Physiol 589:1791–1801. https://doi.org/10.1113/jphysiol.2010.202838
doi: 10.1113/jphysiol.2010.202838
pubmed: 21486840
pmcid: 3099030
Bassot A, Chauvin M-A, Bendridi N, Ji-Cao J, Vial G, Monnier L, Bartosch B, Alves A, Cottet-Rousselle C, Gouriou Y, Rieusset J, Morio B (2019) Regulation of mitochondria-associated membranes (MAMs) by NO/sGC/PKG participates in the control of hepatic insulin response. Cells 8:E1319. https://doi.org/10.3390/cells8111319
doi: 10.3390/cells8111319
pubmed: 31731523
Boengler K, Ruiz-Meana M, Gent S, Ungefug E, Soetkamp D, Miro-Casas E, Cabestrero A, Fernandez-Sanz C, Semenzato M, Lisa FD, Rohrbach S, Garcia-Dorado D, Heusch G, Schulz R, Mercola M (2012) Mitochondrial connexin 43 impacts on respiratory complex I activity and mitochondrial oxygen consumption. J Cell Mol Med 16:1649–1655. https://doi.org/10.1111/j.1582-4934.2011.01516.x
doi: 10.1111/j.1582-4934.2011.01516.x
pubmed: 22212640
pmcid: 3822677
Bøtker HE, Cabrera-Fuentes HA, Ruiz-Meana M, Heusch G, Ovize M (2020) Translational issues for mitoprotective agents as adjunct to reperfusion therapy in patients with ST-segment elevation myocardial infarction. J Cell Mol Med 24:2717–2729. https://doi.org/10.1111/jcmm.14953
doi: 10.1111/jcmm.14953
pubmed: 31967733
pmcid: 7077531
Boulghobra D, Coste F, Geny B, Reboul C (2020) Exercise training protects the heart against ischemia–reperfusion injury: a central role for mitochondria? Free Radic Biol Med 152:395–410. https://doi.org/10.1016/j.freeradbiomed.2020.04.005
doi: 10.1016/j.freeradbiomed.2020.04.005
pubmed: 32294509
Boulghobra D, Grillet P-E, Laguerre M, Tenon M, Fauconnier J, Fança-Berthon P, Reboul C, Cazorla O (2020) Sinapine, but not sinapic acid, counteracts mitochondrial oxidative stress in cardiomyocytes. Redox Biol 34:101554. https://doi.org/10.1016/j.redox.2020.101554
doi: 10.1016/j.redox.2020.101554
pubmed: 32464499
pmcid: 7251366
Burwell LS, Brookes PS (2007) Mitochondria as a target for the cardioprotective effects of nitric oxide in ischemia–reperfusion injury. Antioxid Redox Signal 10:579–600. https://doi.org/10.1089/ars.2007.1845
doi: 10.1089/ars.2007.1845
Cadenas S (2018) ROS and redox signaling in myocardial ischemia–reperfusion injury and cardioprotection. Free Radic Biol Med 117:76–89. https://doi.org/10.1016/j.freeradbiomed.2018.01.024
doi: 10.1016/j.freeradbiomed.2018.01.024
pubmed: 29373843
Calvert JW, Condit ME, Pablo AJ, Nicholson CK, Moody BF, Hood RL, Sindler AL, Susheel G, Seals DR, Barouch LA, Lefer DJ (2011) Exercise protects against myocardial ischemia–reperfusion injury via stimulation of β3-adrenergic receptors and increased nitric oxide signaling: role of nitrite and nitrosothiols. Circ Res 108:1448–1458. https://doi.org/10.1161/CIRCRESAHA.111.241117
doi: 10.1161/CIRCRESAHA.111.241117
pubmed: 21527738
pmcid: 3140870
Carvalho PC, Yates JR, Barbosa VC (2012) Improving the TFold test for differential shotgun proteomics. Bioinformatics 28:1652–1654. https://doi.org/10.1093/bioinformatics/bts247
doi: 10.1093/bioinformatics/bts247
pubmed: 22539673
pmcid: 3371870
Casin KM, Fallica J, Mackowski N, Veenema RJ, Chan A, St. Paul A, Zhu G, Bedja D, Biswal S, Kohr MJ (2018) S-Nitrosoglutathione reductase is essential for protecting the female heart from ischemia–reperfusion injury. Circ Res 123:1232–1243. https://doi.org/10.1161/CIRCRESAHA.118.313956
doi: 10.1161/CIRCRESAHA.118.313956
pubmed: 30571462
pmcid: 6310045
Cazorla O, Szilagyi S, Le Guennec J-Y, Vassort G, Lacampagne A (2005) Transmural stretch-dependent regulation of contractile properties in rat heart and its alteration after myocardial infarction. FASEB J 19:88–90. https://doi.org/10.1096/fj.04-2066fje
doi: 10.1096/fj.04-2066fje
pubmed: 15498894
Chang AHK, Sancheti H, Garcia J, Kaplowitz N, Cadenas E, Han D (2014) Respiratory substrates regulate S-nitrosylation of mitochondrial proteins through a thiol-dependent pathway. Chem Res Toxicol 27:794–804. https://doi.org/10.1021/tx400462r
doi: 10.1021/tx400462r
pubmed: 24716714
pmcid: 4033640
Chouchani ET, James AM, Methner C, Pell VR, Prime TA, Erickson BK, Forkink M, Lau GY, Bright TP, Menger KE, Fearnley IM, Krieg T, Murphy MP (2017) Identification and quantification of protein S-nitrosation by nitrite in the mouse heart during ischemia. J Biol Chem 292:14486–14495. https://doi.org/10.1074/jbc.M117.798744
doi: 10.1074/jbc.M117.798744
pubmed: 28710281
pmcid: 5582841
Chouchani ET, Methner C, Nadtochiy SM, Logan A, Pell VR, Ding S, James AM, Cochemé HM, Reinhold J, Lilley KS, Partridge L, Fearnley IM, Robinson AJ, Hartley RC, Smith RAJ, Krieg T, Brookes PS, Murphy MP (2013) Cardioprotection by S-nitrosation of a cysteine switch on mitochondrial complex I. Nat Med 19:753–759. https://doi.org/10.1038/nm.3212
doi: 10.1038/nm.3212
pubmed: 23708290
pmcid: 4019998
Costa ADT, Pierre SV, Cohen MV, Downey JM, Garlid KD (2008) cGMP signalling in pre- and post-conditioning: the role of mitochondria. Cardiovasc Res 77:344–352. https://doi.org/10.1093/cvr/cvm050
doi: 10.1093/cvr/cvm050
pubmed: 18006449
Costa Alexandre DT, Garlid KD, West IC, Lincoln TM, Downey JM, Cohen MV, Critz SD (2005) Protein kinase G transmits the cardioprotective signal from cytosol to mitochondria. Circ Res 97:329–336. https://doi.org/10.1161/01.RES.0000178451.08719.5b
doi: 10.1161/01.RES.0000178451.08719.5b
pubmed: 16037573
Dedkova EN, Blatter LA (2009) Characteristics and function of cardiac mitochondrial nitric oxide synthase. J Physiol 587:851–872. https://doi.org/10.1113/jphysiol.2008.165423
doi: 10.1113/jphysiol.2008.165423
pubmed: 19103678
Doulias P-T, Tenopoulou M, Greene JL, Raju K, Ischiropoulos H (2013) Nitric oxide regulates mitochondrial fatty acid metabolism through reversible protein S-nitrosylation. Sci Signal 6:rs1. https://doi.org/10.1126/scisignal.2003252
doi: 10.1126/scisignal.2003252
pubmed: 23281369
pmcid: 4010156
Ejlersen H, Andersen ZJ, von Euler-Chelpin MC, Johansen PP, Schnohr P, Prescott E (2017) Prognostic impact of physical activity prior to myocardial infarction: case fatality and subsequent risk of heart failure and death. Eur J Prev Cardiol 24:1112–1119. https://doi.org/10.1177/2047487317702046
doi: 10.1177/2047487317702046
pubmed: 28399634
Erusalimsky JD, Moncada S (2007) Nitric oxide and mitochondrial signaling: from physiology to pathophysiology. Arterioscler Thromb Vasc Biol 27:2524–2531. https://doi.org/10.1161/ATVBAHA.107.151167
doi: 10.1161/ATVBAHA.107.151167
pubmed: 17885213
Farah C, Kleindienst A, Bolea G, Meyer G, Gayrard S, Geny B, Obert P, Cazorla O, Tanguy S, Reboul C (2013) Exercise-induced cardioprotection: a role for eNOS uncoupling and NO metabolites. Basic Res Cardiol 108:389. https://doi.org/10.1007/s00395-013-0389-2
doi: 10.1007/s00395-013-0389-2
pubmed: 24105420
Fauconnier J, Andersson DC, Zhang S-J, Lanner JT, Wibom R, Katz A, Bruton JD, Westerblad H (2007) Effects of palmitate on Ca
doi: 10.2337/db06-0739
pubmed: 17229941
Gao S, Chen J, Brodsky SV, Huang H, Adler S, Lee JH, Dhadwal N, Cohen-Gould L, Gross SS, Goligorsky MS (2004) Docking of endothelial nitric oxide synthase (eNOS) to the mitochondrial outer membrane a pentabasic amino acid sequence in the autoinhibitory domain Of eNOS targets a proteinase K-cleavable peptide on the cytoplasmic face of mitochondria. J Biol Chem 279:15968–15974. https://doi.org/10.1074/jbc.M308504200
doi: 10.1074/jbc.M308504200
pubmed: 14761967
García-Niño WR, Correa F, Rodríguez-Barrena JI, León-Contreras JC, Buelna-Chontal M, Soria-Castro E, Hernández-Pando R, Pedraza-Chaverri J, Zazueta C (2017) Cardioprotective kinase signaling to subsarcolemmal and interfibrillar mitochondria is mediated by caveolar structures. Basic Res Cardiol 112:15. https://doi.org/10.1007/s00395-017-0607-4
doi: 10.1007/s00395-017-0607-4
pubmed: 28160133
Görlach A, Bertram K, Hudecova S, Krizanova O (2015) Calcium and ROS: a mutual interplay. Redox Biol 6:260–271. https://doi.org/10.1016/j.redox.2015.08.010
doi: 10.1016/j.redox.2015.08.010
pubmed: 26296072
pmcid: 4556774
Guo Y, Li Q, Xuan Y-T, Wu W-J, Tan W, Slezak J, Zhu X, Tomlin A, Bolli R (2021) Exercise-induced late preconditioning in mice is triggered by eNOS-dependent generation of nitric oxide and activation of PKCε and is mediated by increased iNOS activity. Int J Cardiol 340:68–78. https://doi.org/10.1016/j.ijcard.2021.08.021
doi: 10.1016/j.ijcard.2021.08.021
pubmed: 34400167
Heinzel FR, Luo Y, Li X, Boengler K, Buechert A, García-Dorado D, Di Lisa F, Schulz R, Heusch G (2005) Impairment of diazoxide-induced formation of reactive oxygen species and loss of cardioprotection in connexin 43 deficient mice. Circ Res 97:583–586. https://doi.org/10.1161/01.RES.0000181171.65293.65
doi: 10.1161/01.RES.0000181171.65293.65
pubmed: 16100048
Heusch G (2020) Myocardial ischaemia–reperfusion injury and cardioprotection in perspective. Nat Rev Cardiol 17(12):773–789. https://doi.org/10.1038/s41569-020-0403-y
doi: 10.1038/s41569-020-0403-y
pubmed: 32620851
Jaffrey SR, Snyder SH (2001) The biotin switch method for the detection of S-nitrosylated proteins. Sci STKE 200:pl1. https://doi.org/10.1126/stke.2001.86.pl1
doi: 10.1126/stke.2001.86.pl1
Klein G, Mathé C, Biola-Clier M, Devineau S, Drouineau E, Hatem E, Marichal L, Alonso B, Gaillard J, Lagniel G, Armengaud J, Carrière M, Chédin S, Boulard Y, Pin S, Renault J, Aude J, Labarre J (2016) RNA-binding proteins are a major target of silica nanoparticles in cell extracts. In: Nanotoxicology. https://www.pubmed.ncbi.nlm.nih.gov/27705051/ . Accessed 2 Dec 2020
Kleindienst A, Battault S, Belaidi E, Tanguy S, Rosselin M, Boulghobra D, Meyer G, Gayrard S, Walther G, Geny B, Durand G, Cazorla O, Reboul C (2016) Exercise does not activate the β3 adrenergic receptor–eNOS pathway, but reduces inducible NOS expression to protect the heart of obese diabetic mice. Basic Res Cardiol 111:40. https://doi.org/10.1007/s00395-016-0559-0
doi: 10.1007/s00395-016-0559-0
pubmed: 27164904
Kohr M, Aponte A, J S, Gucek M, Steenbergen C, Murphy E (2012) Measurement of S-nitrosylation occupancy in the myocardium with cysteine-reactive tandem mass tags: short communication. In: Circulation research https://www.pubmed.ncbi.nlm.nih.gov/22865876/ . Accessed 8 Nov 2020
Kohr MJ, Aponte AM, Sun J, Wang G, Murphy E, Gucek M, Steenbergen C (2011) Characterization of potential S-nitrosylation sites in the myocardium. Am J Physiol Heart Circ Physiol 300:H1327-1335. https://doi.org/10.1152/ajpheart.00997.2010
doi: 10.1152/ajpheart.00997.2010
pubmed: 21278135
pmcid: 3075037
Koncsos G, Varga ZV, Baranyai T, Ferdinandy P, Schulz R, Giricz Z, Boengler K (2018) Nagarse treatment of cardiac subsarcolemmal and interfibrillar mitochondria leads to artefacts in mitochondrial protein quantification. J Pharmacol Toxicol Methods 91:50–58. https://doi.org/10.1016/j.vascn.2018.01.004
doi: 10.1016/j.vascn.2018.01.004
pubmed: 29378341
Kuznetsov AV, Margreiter R (2009) Heterogeneity of mitochondria and mitochondrial function within cells as another level of mitochondrial complexity. Int J Mol Sci 10:1911–1929. https://doi.org/10.3390/ijms10041911
doi: 10.3390/ijms10041911
pubmed: 19468346
pmcid: 2680654
Lacza Z, Pankotai E, Busija DW (2009) Mitochondrial nitric oxide synthase: current concepts and controversies. Front Biosci Landmark Ed 14:4436–4443
doi: 10.2741/3539
Lee Y, Min K, Talbert EE, Kavazis AN, Smuder AJ, Willis WT, Powers SK (2012) Exercise protects cardiac mitochondria against ischemia–reperfusion injury. Med Sci Sports Exerc 44:397–405. https://doi.org/10.1249/MSS.0b013e318231c037
doi: 10.1249/MSS.0b013e318231c037
pubmed: 21857373
Leite ACR, Oliveira HCF, Utino FL, Garcia R, Alberici LC, Fernandes MP, Castilho RF, Vercesi AE (2010) Mitochondria generated nitric oxide protects against permeability transition via formation of membrane protein S-nitrosothiols. Biochim Biophys Acta BBA Bioenergy 1797:1210–1216. https://doi.org/10.1016/j.bbabio.2010.01.034
doi: 10.1016/j.bbabio.2010.01.034
Lemasters J, Theruvath T, Zhong Z, Al N (2009) Mitochondrial calcium and the permeability transition in cell death. In: Biochimica Biophysica Acta. https://www.pubmed.ncbi.nlm.nih.gov/19576166/ . Accessed 8 Nov 2020
Lima B, Forrester MT, Hess DT, Stamler JS (2010) S-Nitrosylation in cardiovascular signaling. Circ Res 106:633–646. https://doi.org/10.1161/CIRCRESAHA.109.207381
doi: 10.1161/CIRCRESAHA.109.207381
pubmed: 20203313
pmcid: 2891248
Lindenmayer G, Sordahl L, Schwartz A (1968) Reevaluation of oxidative phosphorylation in cardiac mitochondria from normal animals and animals in heart failure. In: Circulation resarch https://www.pubmed.ncbi.nlm.nih.gov/5676454/ . Accessed 2 Dec 2020
Liu Y, Zhang Y (2015) CHCHD2 connects mitochondrial metabolism to apoptosis. Mol Cell Oncol. https://doi.org/10.1080/23723556.2015.1004964
doi: 10.1080/23723556.2015.1004964
pubmed: 27314073
pmcid: 4845206
Magalhães J, Gonçalves IO, Lumini-Oliveira J, Marques-Aleixo I, Passos E, Rocha-Rodrigues S, Machado NG, Moreira AC, Rizo D, Viscor G, Oliveira PJ, Torrella JR, Ascensão A (2014) Modulation of cardiac mitochondrial permeability transition and apoptotic signaling by endurance training and intermittent hypobaric hypoxia. Int J Cardiol 173:40–45. https://doi.org/10.1016/j.ijcard.2014.02.011
doi: 10.1016/j.ijcard.2014.02.011
pubmed: 24602319
Marcil M, Bourduas K, Ascah A, Burelle Y (2006) Exercise training induces respiratory substrate-specific decrease in Ca
doi: 10.1152/ajpheart.00913.2005
pubmed: 16284229
Marongiu E, Crisafulli A (2014) Cardioprotection acquired through exercise: the role of ischemic preconditioning. Curr Cardiol Rev 10:336–348. https://doi.org/10.2174/1573403X10666140404110229
doi: 10.2174/1573403X10666140404110229
pubmed: 24720421
pmcid: 4101198
McMillin-Wood J, Wolkowicz PE, Chu A, Tate CA, Goldstein MA, Entman ML (1980) Calcium uptake by two preparations of mitochondria from heart. Biochim Biophys Acta BBA Bioenergy 591:251–265. https://doi.org/10.1016/0005-2728(80)90157-7
doi: 10.1016/0005-2728(80)90157-7
Methner C, Lukowski R, Grube K, Loga F, Smith RAJ, Murphy MP, Hofmann F, Krieg T (2013) Protection through postconditioning or a mitochondria-targeted S-nitrosothiol is unaffected by cardiomyocyte-selective ablation of protein kinase G. Basic Res Cardiol 108:337. https://doi.org/10.1007/s00395-013-0337-1
doi: 10.1007/s00395-013-0337-1
pubmed: 23423145
Meziat C, Boulghobra D, Strock E, Battault S, Bornard I, Walther G, Reboul C (2019) Exercise training restores eNOS activation in the perivascular adipose tissue of obese rats: Impact on vascular function. Nitric Oxide 86:63–67. https://doi.org/10.1016/j.niox.2019.02.009
doi: 10.1016/j.niox.2019.02.009
pubmed: 30836135
Murphy E, Kohr M, Sun J, Nguyen T, Steenbergen C (2012) S-Nitrosylation: a radical way to protect the heart. J Mol Cell Cardiol 52:568–577. https://doi.org/10.1016/j.yjmcc.2011.08.021
doi: 10.1016/j.yjmcc.2011.08.021
pubmed: 21907718
Murphy E, Steenbergen C (2007) Preconditioning: the mitochondrial connection. Annu Rev Physiol 69:51–67. https://doi.org/10.1146/annurev.physiol.69.031905.163645
doi: 10.1146/annurev.physiol.69.031905.163645
pubmed: 17007587
Nguyen TT, Stevens MV, Kohr M, Steenbergen C, Sack MN, Murphy E (2011) Cysteine 203 of cyclophilin D is critical for cyclophilin D activation of the mitochondrial permeability transition pore. J Biol Chem 286:40184–40192. https://doi.org/10.1074/jbc.M111.243469
doi: 10.1074/jbc.M111.243469
pubmed: 21930693
pmcid: 3220546
Olgar Y, Degirmenci S, Durak A, Billur D, Can B, Kayki-Mutlu G, Arioglu-Inan EE, Turan B (2018) Aging related functional and structural changes in the heart and aorta: MitoTEMPO improves aged-cardiovascular performance. Exp Gerontol 110:172–181. https://doi.org/10.1016/j.exger.2018.06.012
doi: 10.1016/j.exger.2018.06.012
pubmed: 29908347
Palmer JW, Tandler B, Hoppel CL (1977) Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J Biol Chem 252:8731–8739
doi: 10.1016/S0021-9258(19)75283-1
Palmer JW, Tandler B, Hoppel CL (1986) Heterogeneous response of subsarcolemmal heart mitochondria to calcium. Am J Physiol Heart Circ Physiol 250:H741–H748. https://doi.org/10.1152/ajpheart.1986.250.5.H741
doi: 10.1152/ajpheart.1986.250.5.H741
Pan X, Liu J, Nguyen T, Liu C, Sun J, Teng Y, Fergusson MM, Rovira II, Allen M, Springer DA, Aponte AM, Gucek M, Balaban RS, Murphy E, Finkel T (2013) The physiological role of mitochondrial calcium revealed by mice lacking the mitochondrial calcium uniporter (MCU). Nat Cell Biol 15:1464–1472. https://doi.org/10.1038/ncb2868
doi: 10.1038/ncb2868
pubmed: 24212091
pmcid: 3852190
Panel M, Ghaleh B, Morin D (2017) Ca
doi: 10.1038/s41598-017-04618-4
pubmed: 28655872
pmcid: 5487341
Penna C, Angotti C, Pagliaro P (2014) Protein S-nitrosylation in preconditioning and postconditioning. Exp Biol Med 239:647–662. https://doi.org/10.1177/1535370214522935
doi: 10.1177/1535370214522935
Perez-Riverol Y, Csordas A, Bai J, Bernal-Llinares M, Hewapathirana S, Kundu D, Inuganti A, Griss J, Mayer G, Eisenacher M, Pérez E, Uszkoreit J, Pfeuffer J, Sachsenberg T, Yilmaz S, Tiwary S, Cox J, Audain E, Walzer M, Jarnuczak A, Ternent T, Brazma A, Vizcaíno J (2019) The PRIDE database and related tools and resources in 2019: improving support for quantification data. In: Nucleic acids research. https://www.pubmed.ncbi.nlm.nih.gov/30395289/ . Accessed 22 Jan 2021
Rassaf T, Totzeck M, Hendgen-Cotta UB, Shiva S, Heusch G, Kelm M (2014) Circulating nitrite contributes to cardioprotection by remote ischemic preconditioning. Circ Res 114:1601–1610. https://doi.org/10.1161/CIRCRESAHA.114.303822
doi: 10.1161/CIRCRESAHA.114.303822
pubmed: 24643960
Reboul C, Tanguy S, Juan JM, Dauzat M (1985) Obert P (2005) Cardiac remodeling and functional adaptations consecutive to altitude training in rats: implications for sea level aerobic performance. J Appl Physiol Bethesda Md 98:83–92. https://doi.org/10.1152/japplphysiol.00214.2004
doi: 10.1152/japplphysiol.00214.2004
Riva A, Tandler B, Loffredo F, Vazquez E, Hoppel C (2005) Structural differences in two biochemically defined populations of cardiac mitochondria. Am J Physiol Heart Circ Physiol 289:H868–H872. https://doi.org/10.1152/ajpheart.00866.2004
doi: 10.1152/ajpheart.00866.2004
pubmed: 15821034
Rodríguez-Sinovas A, Ruiz-Meana M, Denuc A, García-Dorado D (2018) Mitochondrial Cx43, an important component of cardiac preconditioning. Biochim Biophys Acta BBA Biomembr 1860:174–181. https://doi.org/10.1016/j.bbamem.2017.06.011
doi: 10.1016/j.bbamem.2017.06.011
Rohart F, Gautier B, Singh A, Lê Cao K-A (2017) mixOmics: An R package for ‘omics feature selection and multiple data integration. PLoS Comput Biol. https://doi.org/10.1371/journal.pcbi.1005752
doi: 10.1371/journal.pcbi.1005752
pubmed: 29099853
pmcid: 5687754
Roth GA, Johnson C, Abajobir A, Abd-Allah F, Abera SF, Abyu G, Ahmed M, Aksut B, Alam T, Alam K, Alla F, Alvis-Guzman N, Amrock S, Ansari H, Ärnlöv J, Asayesh H, Atey TM, Avila-Burgos L, Awasthi A, Banerjee A, Barac A, Bärnighausen T, Barregard L, Bedi N, Belay Ketema E, Bennett D, Berhe G, Bhutta Z, Bitew S, Carapetis J, Carrero JJ, Malta DC, Castañeda-Orjuela CA, Castillo-Rivas J, Catalá-López F, Choi J-Y, Christensen H, Cirillo M, Cooper L, Criqui M, Cundiff D, Damasceno A, Dandona L, Dandona R, Davletov K, Dharmaratne S, Dorairaj P, Dubey M, Ehrenkranz R, El Sayed ZM, Faraon EJA, Esteghamati A, Farid T, Farvid M, Feigin V, Ding EL, Fowkes G, Gebrehiwot T, Gillum R, Gold A, Gona P, Gupta R, Habtewold TD, Hafezi-Nejad N, Hailu T, Hailu GB, Hankey G, Hassen HY, Abate KH, Havmoeller R, Hay SI, Horino M, Hotez PJ, Jacobsen K, James S, Javanbakht M, Jeemon P, John D, Jonas J, Kalkonde Y, Karimkhani C, Kasaeian A, Khader Y, Khan A, Khang Y-H, Khera S, Khoja AT, Khubchandani J, Kim D, Kolte D, Kosen S, Krohn KJ, Kumar GA, Kwan GF, Lal DK, Larsson A, Linn S, Lopez A, Lotufo PA, El Razek HMA, Malekzadeh R, Mazidi M, Meier T, Meles KG, Mensah G, Meretoja A, Mezgebe H, Miller T, Mirrakhimov E, Mohammed S, Moran AE, Musa KI, Narula J, Neal B, Ngalesoni F, Nguyen G, Obermeyer CM, Owolabi M, Patton G, Pedro J, Qato D, Qorbani M, Rahimi K, Rai RK, Rawaf S, Ribeiro A, Safiri S, Salomon JA, Santos I, Santric Milicevic M, Sartorius B, Schutte A, Sepanlou S, Shaikh MA, Shin M-J, Shishehbor M, Shore H, Silva DAS, Sobngwi E, Stranges S, Swaminathan S, Tabarés-Seisdedos R, Tadele Atnafu N, Tesfay F, Thakur JS, Thrift A, Topor-Madry R, Truelsen T, Tyrovolas S, Ukwaja KN, Uthman O, Vasankari T, Vlassov V, Vollset SE, Wakayo T, Watkins D, Weintraub R, Werdecker A, Westerman R, Wiysonge CS, Wolfe C, Workicho A, Xu G, Yano Y, Yip P, Yonemoto N, Younis M, Yu C, Vos T, Naghavi M, Murray C (2017) Global, regional, and national burden of cardiovascular diseases for 10 causes, 1990 to 2015. J Am Coll Cardiol 70:1–25. https://doi.org/10.1016/j.jacc.2017.04.052
doi: 10.1016/j.jacc.2017.04.052
pubmed: 28527533
pmcid: 5491406
Ruiz-Meana M, Núñez E, Miro-Casas E, Martínez-Acedo P, Barba I, Rodriguez-Sinovas A, Inserte J, Fernandez-Sanz C, Hernando V, Vázquez J, Garcia-Dorado D (2014) Ischemic preconditioning protects cardiomyocyte mitochondria through mechanisms independent of cytosol. J Mol Cell Cardiol 68:79–88. https://doi.org/10.1016/j.yjmcc.2014.01.001
doi: 10.1016/j.yjmcc.2014.01.001
pubmed: 24434643
Sartoretto JL, Kalwa H, Pluth MD, Lippard SJ, Michel T (2011) Hydrogen peroxide differentially modulates cardiac myocyte nitric oxide synthesis. Proc Natl Acad Sci 108:15792–15797. https://doi.org/10.1073/pnas.1111331108
doi: 10.1073/pnas.1111331108
pubmed: 21896719
pmcid: 3179126
Schulman IH, Hare JM (2012) Regulation of cardiovascular cellular processes by S-nitrosylation. Biochim Biophys Acta 1820:752–762. https://doi.org/10.1016/j.bbagen.2011.04.002
doi: 10.1016/j.bbagen.2011.04.002
pubmed: 21536106
Soetkamp D, Nguyen TT, Menazza S, Hirschhäuser C, Hendgen-Cotta UB, Rassaf T, Schlüter KD, Boengler K, Murphy E, Schulz R (2014) S-nitrosation of mitochondrial connexin 43 regulates mitochondrial function. Basic Res Cardiol 109:433. https://doi.org/10.1007/s00395-014-0433-x
doi: 10.1007/s00395-014-0433-x
pubmed: 25115184
pmcid: 4168224
Srisakuldee W, Makazan Z, Nickel BE, Zhang F, Thliveris JA, Pasumarthi KBS, Kardami E (2014) The FGF-2-triggered protection of cardiac subsarcolemmal mitochondria from calcium overload is mitochondrial connexin 43-dependent. Cardiovasc Res 103:72–80. https://doi.org/10.1093/cvr/cvu066
doi: 10.1093/cvr/cvu066
pubmed: 24654232
Sun J, Kohr MJ, Nguyen T, Aponte AM, Connelly PS, Esfahani SG, Gucek M, Daniels MP, Steenbergen C, Murphy E (2012) Disruption of caveolae blocks ischemic preconditioning-mediated S-nitrosylation of mitochondrial proteins. Antioxid Redox Signal 16:45–56. https://doi.org/10.1089/ars.2010.3844
doi: 10.1089/ars.2010.3844
pubmed: 21834687
pmcid: 3218381
Sun J, Morgan M, Shen R-F, Steenbergen C, Murphy E (2007) Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport. Circ Res 101:1155–1163. https://doi.org/10.1161/CIRCRESAHA.107.155879
doi: 10.1161/CIRCRESAHA.107.155879
pubmed: 17916778
Sun J, Murphy E (2010) Protein S-nitrosylation and cardioprotection. Circ Res 106:285–296. https://doi.org/10.1161/CIRCRESAHA.109.209452
doi: 10.1161/CIRCRESAHA.109.209452
pubmed: 20133913
pmcid: 3137884
Sun J, Nguyen T, Aponte AM, Menazza S, Kohr MJ, Roth DM, Patel HH, Murphy E, Steenbergen C (2015) Ischaemic preconditioning preferentially increases protein S-nitrosylation in subsarcolemmal mitochondria. Cardiovasc Res 106:227–236. https://doi.org/10.1093/cvr/cvv044
doi: 10.1093/cvr/cvv044
pubmed: 25694588
pmcid: 4416121