Overexpression of the muscle-specific protein, melusin, protects from cardiac ischemia/reperfusion injury

Basic Research in Cardiology

Volumn 109, Issue 4, 2014, Pages

  Penna, Claudia ^a,b   Brancaccio, Mara ^a   Tullio, Francesca ^a,b   Rubinetto, Cristina ^a   Perrelli, Maria Giulia ^a,b   Angotti, Carmelina ^a,b   Pagliaro, Pasquale ^a,b   Tarone, Guido ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b National Institute for Cardiovascular Research   (Italy)

Author keywords

AKT; Chaperone; ERK; Hsp90; I R injury; Melusin

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; GLYCOGEN SYNTHASE KINASE 3BETA; HEAT SHOCK PROTEIN 90; LACTATE DEHYDROGENASE; MELUSIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MUSCLE PROTEIN; PROTEIN KINASE B; UNCLASSIFIED DRUG; WORTMANNIN; CYTOSKELETON PROTEIN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; ITGB1BP2 PROTEIN, MOUSE; MAPK1 PROTEIN, MOUSE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME BLOOD LEVEL; ENZYME INHIBITION; ENZYME RELEASE; HEART MUSCLE ISCHEMIA; HEART PROTECTION; ISCHEMIC POSTCONDITIONING; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REPERFUSION INJURY; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; ENZYME ACTIVATION; GENETICS; HEART MUSCLE; METABOLISM; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; PATHOLOGY; PHOSPHORYLATION; TIME; TRANSGENIC MOUSE; UPREGULATION;

ANIMALS; CYTOSKELETAL PROTEINS; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; GLYCOGEN SYNTHASE KINASE 3; HSP90 HEAT-SHOCK PROTEINS; MALE; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MUSCLE PROTEINS; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; PHOSPHATIDYLINOSITOL 3-KINASE; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TIME FACTORS; UP-REGULATION;

EID: 84901575580     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-014-0418-9     Document Type: Article

References (71)

1. Baines CP (2009) The mitochondrial permeability transition pore and ischemia-reperfusion injury. Basic Res Cardiol 104:181-188. doi:10.1007/s00395- 009-0004-8
2. Baker JE (2004) Oxidative stress and adaptation of the infant heart to hypoxia and ischemia. Antioxid Redox Signal 6:423-429. doi:10.1089/ 152308604322899495
3. Basso AD, Solit DB, Chiosis G, Giri B, Tsichlis P, Rosen N (2002) Akt forms an intracellular complex with heat shock protein 90 (Hsp90) and Cdc37 and is destabilized by inhibitors of Hsp90 function. J Biol Chem 277:39858-39866. doi:10.1074/jbc.M206322200 (Pubitemid 35190971)
4. Bell RM, Mocanu MM, Yellon DM (2011) Retrograde heart perfusion: the Langendorff technique of isolated heart perfusion. J Mol Cell Cardiol 50:940-950. doi:10.1016/j.yjmcc.2011.02.018
5. Bencsik P, Pálóczi J, Kocsis GF, Pipis J, Belecz I, Varga ZV, Csonka C, Görbe A, Csont T, Ferdinandy P (2014) Moderate inhibition of myocardial matrix metalloproteinase-2 by ilomastat is cardioprotective. Pharmacol Res 80:36-42. doi:10.1016/j.phrs. 2013.12.007
6. Bergmeyer HU, Bernt E (1974) UV-assay with pyruvate and NADH. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol II, 2nd edn. Academic Press, New York, pp 574-579
7. Bolli R, Bhatti ZA, Tang XL, Qiu Y, Zhang Q, Guo Y, Jadoon AK (1997) Evidence that late preconditioning against myocardial stunning in conscious rabbits is triggered by the generation of nitric oxide. Circ Res 81:42-52. doi:10.1161/01.RES.81.1.42 (Pubitemid 27272981)
8. Brancaccio M, Fratta L, Notte A, Hirsch E, Poulet R, Guazzone S, De Acetis M, Vecchione C, Marino G, Altruda F, Silengo L, Tarone G, Lembo G (2003) Melusin, a muscle-specific integrin beta1-interacting protein, is required to prevent cardiac failure in response to chronic pressure overload. Nat Med 9:68-75. doi:10.1038/nm805 (Pubitemid 36098262)
9. Budas GR, Churchill EN, Disatnik MH, Sun L, Mochly-Rosen D (2010) Mitochondrial import of PKCepsilon is mediated by HSP90: a role in cardioprotection from ischaemia and reperfusion injury. Cardiovasc Res 88:83-92. doi:10.1093/cvr/cvq154
10. Bulhak AA, Jung C, Ostenson CG, Lundberg JO, Sjöquist PO, Pernow J (2009) PPAR-alpha activation protects the type 2 diabetic myocardium against ischemia-reperfusion injury: involvement of the PI3-Kinase/Akt and NO pathway. Am J Physiol Heart Circ Physiol 296:H719-H727. doi:10.1152/ajpheart.00394.2008
11. Chen Z, Chua CC, Ho YS, Hamdy RC, Chua BH (2001) Over-expression of Bcl-2 attenuates apoptosis and protects against myocardial I/R injury in transgenic mice. Am J Physiol 280:H2313-H2320
12. Choudhury S, Bae S, Ke Q, Lee JY, Kim J, Kang PM (2011) Mitochondria to nucleus translocation of AIF in mice lacking Hsp70 during ischemia/reperfusion. Basic Res Cardiol 106:397-407. doi:10.1007/s00395-011-0164-1
13. Cohen MV, Downey JM (2011) Ischemic postconditioning: from receptor to end-effector. Antioxid Redox Signal 14:821-831. doi:10.1089/ars.2010.3318
14. Darling CE, Jiang R, Maynard M, Whittaker P, Vinten-Johansen J, Przyklenk K (2005) 'Postconditioning' via stuttering reperfusion limits myocardial infarct size in rabbit hearts: role of ERK 1/2. Am J Physiol Heart Circ Physiol 289:H1618-H1626. doi:10.1152/ajpheart.00055.2005 (Pubitemid 41369005)
15. De Acetis M, Notte A, Accornero F, Selvetella G, Brancaccio M, Vecchione C, Sbroggiò M, Collino F, Pacchioni B, Lanfranchi G, Aretini A, Ferretti R, Maffei A, Altruda F, Silengo L, Tarone G, Lembo G (2005) Cardiac overexpression of melusin protects from dilated cardiomyopathy due to long-standing pressure overload. Circ Res 96:1087-1094. doi:10.1161/01.RES. 0000168028.36081.e0 (Pubitemid 40791381)
16. Dent P (2014) Crosstalk between ERK, AKT, and cell survival. Cancer Biol Ther 15:245-246. doi:10.4161/cbt.27541
17. Eeftting F, Rensing B, Wigman J, Pannekoek WJ, Liu WM, Cramer MJ, Lips DJ, Doevendans PA (2004) Role of apoptosis in reperfusion injury. Cardiovasc Res 61:414-426. doi:10.1016/j.cardiores.2003.12.023 (Pubitemid 38210148)
18. Efthymiou CA, Mocanu MM, de Belleroche J, Wells DJ, Latchmann DS, Yellon DM (2004) Heat shock protein 27 protects the heart against myocardial infarction. Basic Res Cardiol 99:392-394. doi:10.1007/s00395-004-0483-6 (Pubitemid 39462361)
19. Engelman DT, Watanabe M, Engelman RM, Rousou JA, Kisin E, Kagan VE, Maulik N, Das DK (1995) Hypoxic preconditioning preserves antioxidant reserve in the working rat heart. Cardiovasc Res 29:133-140. doi:10.1016/S0008-6363(96) 88558-0
20. Ferretti R, Sbroggiò M, Di Savino A, Fusella F, Bertero A, Michowski W, Tarone G, Brancaccio M (2011) Morgana and melusin: two fairies chaperoning signal transduction. Cell Cycle 10:3678-3683. doi:10.4161/cc.10.21. 18202
21. Gottlieb RA, Burleson KO, Kloner RA, Babior BM, Engler RL (1994) Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest 94:1621-1628. doi:10.1172/JCI117504 (Pubitemid 24309885)
22. Gu R, Zheng D, Bai J, Xie J, Dai Q, Xu B (2012) Altered melusin pathways involved in cardiac remodeling following acute myocardial infarction. Cardiovasc Pathol 21:105-111. doi:10.1016/j. carpath.2011.03.002
23. Halkos ME, Kerendi F, Corvera JS, Wang NP, Kin H, Payne CS, Sun HY, Guyton RA, Vinten-Johansen J, Zhao ZQ (2004) Myocardial protection with postconditioning is not enhanced by ischemic preconditioning. Ann Thorac Surg 78:961-969. doi:10. 1016/j.athoracsur.2004.03.033 discussion 969
24. Hausenloy DJ, Lecour S, Yellon DM (2011) Reperfusion injury salvage kinase and survivor activating factor enhancement prosurvival signaling pathways in ischemic postconditioning: two sides of the same coin. Antioxid Redox Signal 14:893-907. doi:10.1089/ars.2010.3360
25. 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
26. Hausenloy DJ, Tsang A, Mocanu MM, Yellon DM (2005) Ischemic preconditioning protects by activating prosurvival kinases at reperfusion. Am J Physiol Heart Circ Physiol 288:H971-H976. doi:10.1152/ajpheart.00374.2004 (Pubitemid 40139686)
27. Hausenloy DJ, Tsang A, Yellon DM (2005) The reperfusion injury salvage kinase pathway: a common target for both ischemic preconditioning and postconditioning. Trends Cardiovasc Med 15:69-75 (Pubitemid 40693390)
28. Heusch G (2013) Remote conditioning: the future of cardioprotection? J Cardiovasc Med (Hagerstown) 14:176-179. doi:10. 2459/JCM.0b013e328358e507
29. Heusch G (2013) Cardioprotection: chances and challenges of its translation to the clinic. Lancet 381:166-175. doi:10.1016/S0140-6736(12)60916-7
30. Heusch G, Boengler K, Schulz R (2008) Cardioprotection: nitric oxide, protein kinases, and mitochondria. Circulation 118:1915-1919. doi:10.1161/CIRCULATIONAHA.108.805242
31. 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
32. Hong TJ, Kim S, Wi AR, Lee P, Kang M, Jeong JH, Hahn JS (2013) Dynamic nucleotide-dependent interactions of cysteineand histidine-rich domain (CHORD)-containing Hsp90 cochaperones Chp-1 and melusin with cochaperones PP5 and Sgt1. J Biol Chem 288:215-222. doi:10.1074/jbc.M112.398636
33. Iliodromitis EK, Karavolias GK, Bofilis E, Yellon DM, Kremastinos DT (1999) Enhanced protection of heat shock in myocardial infarction: inhibition of detrimental effect of systemic hyperthermia. Cardiovasc Drugs Ther 13:223-231. doi:10.1023/A:1007796125902 (Pubitemid 29312818)
34. Kingma JG Jr (1999) Cardiac adaptation to ischemia-reperfusion injury. Ann N Y Acad Sci 874:83-99. doi:10.1111/j.1749-6632. 1999.tb09227.x1
35. Kupatt C, Dessy C, Hinkel R, Raake P, Daneau G, Bouzin C, Boekstegers P, Feron O (2004) Heat shock protein 90 transfection reduces ischemia-reperfusion- induced myocardial dysfunction via reciprocal endothelial NO synthase serine 1177 phosphorylation and threonine 495 dephosphorylation. Arterioscler Thromb Vasc Biol 24:1435-1441. doi:10.1161/01.ATV.0000134300.87476.d1 (Pubitemid 39050437)
36. Lacerda L, Somers S, Opie LH, Lecour S (2009) Ischaemic postconditioning protects against reperfusion injury via the SAFE pathway. Cardiovasc Res 84:201-208. doi:10.1093/cvr/cvp274
37. Lavu M, Gundewar S, Lefer DJ (2011) Gene therapy for ischemic heart disease. J Mol Cell Cardiol 50:742-750. doi:10.1016/j. yjmcc.2010.06.007
38. Liu Y, Yang XM, Iliodromitis EK, Kremastinos DT, Dost T, Cohen MV, Downey JM (2008) Redox signaling at reperfusion is required for protection from ischemic preconditioning but not from a direct PKC activator. Basic Res Cardiol 103:54-59. doi:10.1007/s00395-007-0683-y (Pubitemid 50002795)
39. Logue SE, Gustafsson AB, Samali A, Gottlieb RA (2005) Ischemia/reperfusion injury at the intersection with cell death. J Mol Cell Cardiol 38:21-33. doi:10.1016/j.yjmcc.2004.11.009 (Pubitemid 40044759)
40. Luan HF, Zhao ZB, Zhao QH, Zhu P, Xiu MY, Ji Y (2012) Hydrogen sulfide postconditioning protects isolated rat hearts against ischemia and reperfusion injury mediated by the JAK2/ STAT3 survival pathway. Braz J Med Biol Res 45:898-905. doi:10.1590/S0100-879X2012007500090
41. Marais E, Genade S, Salie R, Huisamen B, Maritz S, Moolman JA, Lochner A (2005) The temporal relationship between p38 MAPK and HSP27 activation in ischaemic and pharmacological preconditioning. Basic Res Cardiol 100:35-47. doi:10.1007/ s00395-004-0495-7
42. Marber MS, Latchman DS, Walker JM, Yellon DM (1993) Cardiac stress protein elevation 24 hours after brief ischemia or heat stress is associated with resistance to myocardial infarction. Circulation 88:1264-1272. doi:10.1161/01.CIR.88.3.1264 (Pubitemid 23264047)
43. Maulik N, Watanabe M, Engelman DT, Engelman RM, Das DK (1995) Oxidative stress adaptation improves postischemic ventricular recovery. Mol Cell Biochem 144:67-74. doi:10.1007/BF00926742
44. Mavria G, Vercoulen Y, Yeo M, Paterson H, Karasarides M, Marais R, Bird D, Marshall CJ (2006) ERK-MAPK signaling opposes Rho-kinase to promote endothelial cell survival and sprouting during angiogenesis. Cancer Cell 9:33-44. doi:10.1016/j.ccr.2005.12.021 (Pubitemid 43069509)
45. Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124-1136. doi:10.1161/01.CIR.74.5.1124 (Pubitemid 17174962)
46. Okubo S, Wildner O, Shah MR, Chelliah JC, Hess ML, Kukreja RC (2001) Gene transfer of heat-shock protein 70 reduces infarct size in vivo after ischemia/reperfusion in the rabbit heart. Circulation 103:877-881. doi:10.1161/01.CIR.103.6.877 (Pubitemid 32163888)
47. Pagliaro P, Gattullo D, Rastaldo R, Losano G (2001) Ischemic preconditioning: from the first to the second window of protection. Life Sci 69:1-15 (Pubitemid 32536730)
48. Pagliaro P, Moro F, Tullio F, Perrelli MG, Penna C (2011) Cardioprotective pathways during reperfusion: focus on redox signaling and other modalities of cell signaling. Antioxid Redox Signal 14:833-850. doi:10.1089/ars.2010.3245
49. Penna C, Cappello S, Mancardi D, Raimondo S, Rastaldo R, Gattullo D, Losano G, Pagliaro P (2006) Post-conditioning reduces infarct size in the isolated rat heart: role of coronary flow and pressure and the nitric oxide/cGMP pathway. Basic Res Cardiol 101:168-179. doi:10.1007/s00395-005-0543-6 (Pubitemid 43250809)
50. Penna C, Perrelli MG, Pagliaro P (2013) Mitochondrial pathways, permeability transition pore, and redox signaling in cardioprotection: therapeutic implications. Antioxid Redox Signal 18:556-599. doi:10.1089/ars. 2011.4459
51. Penna C, Tullio F, Merlino A, Moro F, Raimondo S, Rastaldo R, Perrelli MG, Mancardi D, Pagliaro P (2009) Postconditioning cardioprotection against infarct size and post-ischemic systolic dysfunction is influenced by gender. Basic Res Cardiol 104:390-402. doi:10.1007/s00395-008-0762-8
52. Philipp S, Critz SD, Cui L, Solodushko V, Cohen MV, Downey JM (2006) Localizing extracellular signal-regulated kinase (ERK) in pharmacological preconditioning's trigger pathway. Basic Res Cardiol 101:159-167. doi:10.1007/s00395-005-0566-z (Pubitemid 43250808)
53. Prasad MR, Liu X, Rousou JA, Engelman RM, Jones R, George A, Das DK (1992) Reduced free radical generation during reperfusion of hypothermically arrested hearts. Mol Cell Biochem 111:97-102. doi:10.1007/BF002295791
54. Sato S, Fujita N, Tsuruo T (2000) Modulation of Akt kinase activity by binding to HSP90. Proc Natl Acad Sci USA 97:10832-10837. doi:10.1073/pnas. 170276797
55. Sbroggiò M, Bertero A, Velasco S, Fusella F, De Blasio E, Bahou WF, Silengo L, Turco E, Brancaccio M, Tarone G (2011) ERK1/2 activation in heart is controlled by melusin, focal adhesion kinase and the scaffold protein IQGAP1. J Cell Sci 124:3515-3524. doi:10.1242/jcs.091140
56. Sbroggiò M, Carnevale D, Bertero A, Cifelli G, De Blasio E, Mascio G, Hirsch E, Bahou WF, Turco E, Silengo L, Brancaccio M, Lembo G, Tarone G (2011) IQGAP1 regulates ERK1/2 and AKT signalling in the heart and sustains functional remodelling upon pressure overload. Cardiovasc Res 91:456-464. doi:10. 1093/cvr/cvr103
57. Sbroggiò M, Ferretti R, Percivalle E, Gutkowska M, Zylicz A, Michowski W, Kuznicki J, Accornero F, Pacchioni B, Lanfranchi G, Hamm J, Turco E, Silengo L, Tarone G, Brancaccio M (2008) The mammalian CHORD-containing protein melusin is a stress response protein interacting with Hsp90 and Sgt1. FEBS Lett 582:1788-1794. doi:10.1016/j.febslet.2008.04.058
58. Schulz R, Rose J, Post H, Heusch G (1995) Involvement of endogenous adenosine in ischaemic preconditioning in swine. Pflugers Arch 430:273-282. doi:10.1007/BF00374659
59. Shaul YD, Seger R (2007) The MEK/ERK cascade: from signaling specificity to diverse functions. Biochim Biophys Acta 1773(8):1213-1226. doi:10.1016/j.bbamcr.2006.10.005 (Pubitemid 47125968)
60. Sivaraman V, Mudalagiri NR, Di Salvo C, Kolvekar S, Hayward M, Yap J, Keogh B, Hausenloy DJ, Yellon DM (2007) Postconditioning protects human atrial muscle through the activation of the RISK pathway. Basic Res Cardiol 102:453-459. doi:10. 1007/s00395-007-0664-1
61. Skyschally A, Van Caster P, Boengler K, Gres P, Musiolik J, Schilawa D, Schulz R, Heusch G (2009) Ischemic postconditioning in pigs: no causal role for RISK activation. Circ Res 104:15-18. doi:10.1161/CIRCRESAHA.108.186429
62. Skyschally A, van Caster P, Iliodromitis EK, Schulz R, Kremastinos DT, Heusch G (2009) Ischemic postconditioning: experimental models and protocol algorithms. Basic Res Cardiol 104:469-483. doi:10.1007/s00395-009-0040-4
63. Suzuki K, Sawa Y, Kagisaki K, Taketani S, Ichikawa H, Kaneda Y, Matsuda H (2000) Reduction in myocardial apoptosis associated with overexpression of heat shock protein 70. Basic Res Cardiol 95:397-403. doi:10.1007/s003950070039
64. Tarone G, Sbroggiò M, Brancaccio M (2013) Key role of ERK1/2 molecular scaffolds in heart pathology. Cell Mol Life Sci 70:4047-4054. doi:10.1007/s00018-013-1321-5
65. Unsöld B, Kaul A, Sbroggiò M, Schubert C, Regitz-Zagrosek V, Brancaccio M, Damilano F, Hirsch E, van Bilsen M, Munts C, Sipido K, Bito V, Detre E, Wagner NM, Schäfer K, Seidler T, Vogt J, Neef S, Bleckmann A, Maier LS, Balligand JL, Bouzin C, Clapier RV, Garnier A, Eschenhagen T, El-Armouche A, Knöll R, Tarone G, Hasenfuß G (2013) Melusin protects from cardiac rupture and improves functional remodelling after myocardial infarction. Cardiovasc Res. doi:10.1093/cvr/cvt235
66. Vinten-Johansen J, Granfeldt A, Mykytenko J, Undyala VV, Dong Y, Przyklenk K (2011) The multidimensional physiological responses to postconditioning. Antioxid Redox Signal 14:791-810. doi:10.1089/ars.2010.3396
67. Vinten-Johansen J, Zhao ZQ, Zatta AJ, Kin H, Halkos ME, Kerendi F (2005) Postconditioning-A new link in nature's armor against myocardial ischemia-reperfusion injury. Basic Res Cardiol 100:295-310. doi:10.1007/s00395- 005-0539-2 (Pubitemid 40974080)
68. Waardenberg AJ, Bernardo BC, Ng DC, Shepherd PR, Cemerlang N, Sbroggiò M, Wells CA, Dalrymple BP, Brancaccio M, Lin RC, McMullen JR (2011) Phosphoinositide 3-kinase (PI3K(p110alpha)) directly regulates key components of the Z-disc and cardiac structure. J Biol Chem 286:30837-30846. doi:10.1074/jbc.M111.271684
69. Willis MS, Patterson C (2010) Hold me tight: role of the heat shock protein family of chaperones in cardiac disease. Circulation 122:1740-1751. doi:10.1161/CIRCULATIONAHA.110.942250
70. Zhang J, Cai H (2010) Netrin-1 prevents ischemia/reperfusion-induced myocardial infarction via a DCC/ERK1/2/eNOS s1177/NO/DCC feed-forward mechanism. J Mol Cell Cardiol 48:1060-1070. doi:10.1016/j.yjmcc.2009.11.020
71. Zhao ZQ, Nakamura M, Wang NP, Wilcox JN, Shearer S, Ronson RS, Guyton RA, Vinten-Johansen J (2000) Reperfusion induces myocardial apoptotic cell death. Cardiovasc Res 45:651-660. doi:10.1016/S0008-6363(99)00354-5 (Pubitemid 30047131)