Cardioprotective function of mitochondrial-targeted and transcriptionally inactive STAT3 against ischemia and reperfusion injury

Basic Research in Cardiology

Volumn 110, Issue 6, 2015, Pages

  Szczepanek, Karol ^a   Xu, Aijun ^a,c   Hu, Ying ^a   Thompson, Jeremy ^a   He, Jun ^a   Larner, Andrew C ^d   Salloum, Fadi N ^a   Chen, Qun ^a   Lesnefsky, Edward J ^a,b,d  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^d VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Apoptosis; Mitochondrial permeability transition; Myocardial infarction; Necrosis; Reactive oxygen species

Indexed keywords

REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); STAT3 PROTEIN; UBIQUINOL CYTOCHROME C REDUCTASE; REACTIVE OXYGEN METABOLITE; STAT3 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRON TRANSPORT; HEART INFARCTION SIZE; HEART INJURY; HEART MUSCLE ISCHEMIA; HEART PROTECTION; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REPERFUSION INJURY; RESPIRATORY CHAIN; SURVIVAL RATE; TRANSCRIPTION REGULATION; ANIMAL; HEART MITOCHONDRION; IN VITRO STUDY; METABOLISM; MORTALITY; MYOCARDIAL REPERFUSION INJURY; TRANSGENIC MOUSE;

ANIMALS; IN VITRO TECHNIQUES; MICE; MICE, TRANSGENIC; MITOCHONDRIA, HEART; MYOCARDIAL REPERFUSION INJURY; REACTIVE OXYGEN SPECIES; STAT3 TRANSCRIPTION FACTOR;

EID: 84941351339     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-015-0509-2     Document Type: Article

References (44)

1. Aldakkak M, Stowe DF, Chen Q, Lesnefsky EJ, Camara AK (2008) Inhibited mitochondrial respiration by amobarbital during cardiac ischaemia improves redox state and reduces matrix Ca2+ overload and ROS release. Cardiovasc Res 77:406–415. doi:10.1016/j.cardiores.2007.08.008
2. Boengler K, Buechert A, Heinen Y, Roeskes C, Hilfiker-Kleiner D, Heusch G, Schulz R (2008) Cardioprotection by ischemic postconditioning is lost in aged and STAT3-deficient mice. Circ Res 102:131–135. doi:10.1161/CIRCRESAHA.107.164699
3. Boengler K, Hilfiker-Kleiner D, Drexler H, Heusch G, Schulz R (2008) The myocardial JAK/STAT pathway: from protection to failure. Pharmacol Ther 120:172–185. doi:10.1016/j.pharmthera.2008.08.002
4. Boengler K, Hilfiker-Kleiner D, Heusch G, Schulz R (2010) Inhibition of permeability transition pore opening by mitochondrial STAT3 and its role in myocardial ischemia/reperfusion. Basic Res Cardiol 105:771–785. doi:10.1007/s00395-010-0124-1
5. Boengler K, Ungefug E, Heusch G, Schulz R (2013) The STAT3 inhibitor stattic impairs cardiomyocyte mitochondrial function through increased reactive oxygen species formation. Curr Pharm Des 19:6890–6895. doi:10.2174/138161281939131127115940
6. Borutaite V, Brown GC (2003) Mitochondria in apoptosis of ischemic heart. FEBS Lett 541:1–5. doi:10.1016/S0014-5793(03)00278-3
7. Borutaite V, Budriunaite A, Morkuniene R, Brown GC (2001) Release of mitochondrial cytochrome c and activation of cytosolic caspases induced by myocardial ischaemia. Biochim Biophys Acta 1537:101–109. doi:10.1016/S0925-4439(01)00062-X
8. Chen Q, Moghaddas S, Hoppel CL, Lesnefsky EJ (2006) Reversible blockade of electron transport during ischemia protects mitochondria and decreases myocardial injury following reperfusion. J Pharmacol Exp Ther 319:1405–1412. doi:10.1124/jpet.106.110262
9. Chen Q, Moghaddas S, Hoppel CL, Lesnefsky EJ (2008) Ischemic defects in the electron transport chain increase the production of reactive oxygen species from isolated rat heart mitochondria. Am J Physiol Cell Physiol 294:C460–C466. doi:10.1152/ajpcell.00211.2007
10. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ (2003) Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem 278:36027–36031. doi:10.1074/jbc.M304854200
11. Cohen MV, Yang XM, Downey JM (2007) The pH hypothesis of postconditioning: staccato reperfusion reintroduces oxygen and perpetuates myocardial acidosis. Circulation 115:1895–1903. doi:10.1161/CIRCULATIONAHA.106.675710
12. Crompton M (1999) The mitochondrial permeability transition pore and its role in cell death. Biochem J 341:233–249. doi:10.1016/S0022-2828(03)00043-9
13. Darnell JE Jr (1997) STATs and gene regulation. Science 277:1630–1635. doi:10.1126/science.277.5332.1630
14. Doetschman T (2009) Influence of genetic background on genetically engineered mouse phenotypes. Methods Mol Biol 530:423–433. doi:10.1007/978-1-59745-471-1_23
15. Fuglesteg BN, Suleman N, Tiron C, Kanhema T, Lacerda L, Andreasen TV, Sack MN, Jonassen AK, Mjos OD, Opie LH, Lecour S (2008) Signal transducer and activator of transcription 3 is involved in the cardioprotective signalling pathway activated by insulin therapy at reperfusion. Basic Res Cardiol 103:444–453. doi:10.1007/s00395-008-0728-x
16. Guo Y, Flaherty MP, Wu WJ, Tan W, Zhu X, Li Q, Bolli R (2012) Genetic background, gender, age, body temperature, and arterial blood pH have a major impact on myocardial infarct size in the mouse and need to be carefully measured and/or taken into account: results of a comprehensive analysis of determinants of infarct size in 1074 mice. Basic Res Cardiol 107:288. doi:10.1007/s00395-012-0288-y
17. Halestrap AP, Clarke SJ, Javadov SA (2004) Mitochondrial permeability transition pore opening during myocardial reperfusion—a target for cardioprotection. Cardiovasc Res 61:372–385. doi:10.1016/S0008-6363(03)00533-9
18. Halestrap AP, Connern CP, Griffiths EJ, Kerr PM (1997) Cyclosporin A binding to mitochondrial cyclophilin inhibits the permeability transition pore and protects hearts from ischaemia/reperfusion injury. Mol Cell Biochem 174:167–172. doi:10.1023/A:1006879618176
19. Hausenloy DJ, Ong SB, Yellon DM (2009) The mitochondrial permeability transition pore as a target for preconditioning and postconditioning. Basic Res Cardiol 104:189–202. doi:10.1007/s00395-009-0010-x
20. Hedayati N, Schomisch SJ, Carino JL, Timothy Sherwood J, Lesnefsky EJ, Cmolik BL (2003) Cardioprotection by St Thomas’ solution is mediated by protein kinase C and tyrosine kinase. J Surg Res 113:121–127. doi:10.1016/S0022-4804(03)00146-X
21. Heusch G, Musiolik J, Gedik N, Skyschally A (2011) Mitochondrial STAT3 activation and cardioprotection by ischemic postconditioning in pigs with regional myocardial ischemia/reperfusion. Circ Res 109:1302–1308. doi:10.1161/CIRCRESAHA.111.255604
22. Hilfiker-Kleiner D, Kaminski K, Podewski E, Bonda T, Schaefer A, Sliwa K, Forster O, Quint A, Landmesser U, Doerries C, Luchtefeld M, Poli V, Schneider MD, Balligand JL, Desjardins F, Ansari A, Struman I, Nguyen NQ, Zschemisch NH, Klein G, Heusch G, Schulz R, Hilfiker A, Drexler H (2007) A cathepsin D-cleaved 16 kDa form of prolactin mediates postpartum cardiomyopathy. Cell 128:589–600. doi:10.1016/j.cell.2006.12.036
23. Lecour S, Suleman N, Deuchar GA, Somers S, Lacerda L, Huisamen B, Opie LH (2005) Pharmacological preconditioning with tumor necrosis factor-alpha activates signal transducer and activator of transcription-3 at reperfusion without involving classic prosurvival kinases (Akt and extracellular signal-regulated kinase). Circulation 112:3911–3918. doi:10.1161/CIRCULATIONAHA.105.581058
24. Lee Y, Lee HY, Gustafsson AB (2012) Regulation of autophagy by metabolic and stress signaling pathways in the heart. J Cardiovasc Pharmacol 60:118–124. doi:10.1097/FJC.0b013e318256cdd0
25. Lesnefsky EJ, Tandler B, Ye J, Slabe TJ, Turkaly J, Hoppel CL (1997) Myocardial ischemia decreases oxidative phosphorylation through cytochrome oxidase in subsarcolemmal mitochondria. Am J Physiol 273:H1544–H1554
26. Levy DE, Lee CK (2002) What does Stat3 do? J Clin Invest 109:1143–1148. doi:10.1172/JCI15650
27. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
28. Marques SM, Campos PP, Castro PR, Cardoso CC, Ferreira MA, Andrade SP (2011) Genetic background determines mouse strain differences in inflammatory angiogenesis. Microvasc Res 82:246–252. doi:10.1016/j.mvr.2011.08.011
29. Matsui Y, Takagi H, Qu X, Abdellatif M, Sakoda H, Asano T, Levine B, Sadoshima J (2007) Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ Res 100:914–922. doi:10.1161/01.RES.0000261924.76669.36
30. Nadtochiy SM, Burwell LS, Ingraham CA, Spencer CM, Friedman AE, Pinkert CA, Brookes PS (2009) In vivo cardioprotection by S-nitroso-2-mercaptopropionyl glycine. J Mol Cell Cardiol 46:960–968. doi:10.1016/j.yjmcc.2009.01.012
31. Narendra D, Tanaka A, Suen DF, Youle RJ (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 183:795–803. doi:10.1083/jcb.200809125
32. Natarajan SK, Becker DF (2012) Role of apoptosis-inducing factor, proline dehydrogenase, and NADPH oxidase in apoptosis and oxidative stress. Cell Health Cytoskelet 2012:11–27. doi:10.2147/CHC.S4955
33. Negoro S, Kunisada K, Fujio Y, Funamoto M, Darville MI, Eizirik DL, Osugi T, Izumi M, Oshima Y, Nakaoka Y, Hirota H, Kishimoto T, Yamauchi-Takihara K (2001) Activation of signal transducer and activator of transcription 3 protects cardiomyocytes from hypoxia/reoxygenation-induced oxidative stress through the upregulation of manganese superoxide dismutase. Circulation 104:979–981. doi:10.1161/hc3401.095947
34. Oshima Y, Fujio Y, Nakanishi T, Itoh N, Yamamoto Y, Negoro S, Tanaka K, Kishimoto T, Kawase I, Azuma J (2005) STAT3 mediates cardioprotection against ischemia/reperfusion injury through metallothionein induction in the heart. Cardiovasc Res 65:428–435. doi:10.1016/j.cardiores.2004.10.021
35. Paillard M, Gomez L, Augeul L, Loufouat J, Lesnefsky EJ, Ovize M (2009) Postconditioning inhibits mPTP opening independent of oxidative phosphorylation and membrane potential. J Mol Cell Cardiol 46:902–909. doi:10.1016/j.yjmcc.2009.02.017
36. Sarafian TA, Montes C, Imura T, Qi J, Coppola G, Geschwind DH, Sofroniew MV (2010) Disruption of astrocyte STAT3 signaling decreases mitochondrial function and increases oxidative stress in vitro. PLoS One 5:e9532. doi:10.1371/journal.pone.0009532
37. Smith CC, Dixon RA, Wynne AM, Theodorou L, Ong SG, Subrayan S, Davidson SM, Hausenloy DJ, Yellon DM (2010) Leptin-induced cardioprotection involves JAK/STAT signaling that may be linked to the mitochondrial permeability transition pore. Am J Physiol Heart Circ Physiol 299:H1265–H1270. doi:10.1152/ajpheart.00092.2010
38. Smith RM, Suleman N, Lacerda L, Opie LH, Akira S, Chien KR, Sack MN (2004) Genetic depletion of cardiac myocyte STAT-3 abolishes classical preconditioning. Cardiovasc Res 63:611–616. doi:10.1016/j.cardiores.2004.06.019
39. Stewart S, Lesnefsky EJ, Chen Q (2009) Reversible blockade of electron transport with amobarbital at the onset of reperfusion attenuates cardiac injury. Transl Res 153:224–231. doi:10.1016/j.trsl.2009.02.003
40. Szczepanek K, Chen Q, Derecka M, Salloum FN, Zhang Q, Szelag M, Cichy J, Kukreja RC, Dulak J, Lesnefsky EJ, Larner AC (2011) Mitochondrial-targeted Signal transducer and activator of transcription 3 (STAT3) protects against ischemia-induced changes in the electron transport chain and the generation of reactive oxygen species. J Biol Chem 286:29610–29620. doi:10.1074/jbc.M111.226209
41. Toldo S, Das A, Mezzaroma E, Chau VQ, Marchetti C, Durrant D, Samidurai A, Van Tassell BW, Yin C, Ockaili RA, Vigneshwar N, Mukhopadhyay ND, Kukreja RC, Abbate A, Salloum FN (2014) Induction of microRNA-21 with exogenous hydrogen sulfide attenuates myocardial ischemic and inflammatory injury in mice. Circulation Cardiovasc Genet 7:311–320. doi:10.1161/CIRCGENETICS.113.000381
42. Wegrzyn J, Potla R, Chwae YJ, Sepuri NB, Zhang Q, Koeck T, Derecka M, Szczepanek K, Szelag M, Gornicka A, Moh A, Moghaddas S, Chen Q, Bobbili S, Cichy J, Dulak J, Baker DP, Wolfman A, Stuehr D, Hassan MO, Fu XY, Avadhani N, Drake JI, Fawcett P, Lesnefsky EJ, Larner AC (2009) Function of mitochondrial Stat3 in cellular respiration. Science 323:793–797. doi:10.1126/science.1164551
43. Xu A, Szczepanek K, Maceyka MW, Ross T, Bowler E, Hu Y, Kenny B, Mehfoud C, Desai PN, Baumgarten CM, Chen Q, Lesnefsky EJ (2014) Transient complex I inhibition at the onset of reperfusion by extracellular acidification decreases cardiac injury. Am J Physiol Cell Physiol 306:C1142–C1153. doi:10.1152/ajpcell.00241.2013
44. Zhang Q, Raje V, Yakovlev VA, Yacoub A, Szczepanek K, Meier J, Derecka M, Chen Q, Hu Y, Sisler J, Hamed H, Lesnefsky EJ, Valerie K, Dent P, Larner AC (2013) Mitochondrial localized Stat3 promotes breast cancer growth via phosphorylation of serine 727. J Biol Chem 288:31280–31288. doi:10.1074/jbc.M113.505057