Activation of PKN mediates survival of cardiac myocytes in the heart during ischemia/reperfusion

Circulation Research

Volumn 107, Issue 5, 2010, Pages 642-649

  Takagi, Hiromitsu ^a,b   Hsu, Chiao Po ^a,c   Kajimoto, Katsuya ^a   Shao, Dan ^a   Yang, Yanfei ^a   Maejima, Yasuhiro ^a   Zhai, Peiyong ^a   Yehia, Ghassan ^a   Yamada, Chikaomi ^b   Zablocki, Daniela ^a   Sadoshima, Junichi ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b DAIICHI SANKYO CO   (Japan)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

B crystallin; ischemia reperfusion; PKN; proteasome

Indexed keywords

ALPHA CRYSTALLIN; EPOXOMICIN; PROPRANOLOL; PROTEASOME; PROTEIN KINASE C; SHORT HAIRPIN RNA; CRYAB PROTEIN, MOUSE; HYDROGEN PEROXIDE; OLIGOPEPTIDE; PROTEIN KINASE N; PROTEINASE INHIBITOR; THREONINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENUATION; CELL DEATH; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; MOUSE; NICK END LABELING; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TRANSGENIC MOUSE; ANIMAL; APOPTOSIS; CELL CULTURE; DISEASE MODEL; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENETICS; HEART INFARCTION PREVENTION; METABOLISM; NEWBORN; PATHOLOGY; PHOSPHORYLATION; PROTEIN TRANSPORT; RAT; REPERFUSION INJURY; SIGNAL TRANSDUCTION; TIME; WISTAR RAT;

ALPHA-CRYSTALLIN B CHAIN; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CELL SURVIVAL; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; HYDROGEN PEROXIDE; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MICE; MICE, TRANSGENIC; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; OLIGOPEPTIDES; PHOSPHORYLATION; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN KINASE C; PROTEIN TRANSPORT; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; THREONINE; TIME FACTORS;

EID: 77957037945     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.110.217554     Document Type: Article

References (36)

1. Bolli R. Preconditioning: a paradigm shift in the biology of myocardial ischemia. Am J Physiol Heart Circ Physiol. 2007;292:H19-H27.
2. Mukai H, Ono Y. A novel protein kinase with leucine zipper-like sequences: its catalytic domain is highly homologous to that of protein kinase C. Biochem Biophys Res Commun. 1994;199:897-904.
3. Mukai H. The structure and function of PKN, a protein kinase having a catalytic domain homologous to that of PKC. J Biochem. 2003;133:17-27.
4. Kawamata T, Taniguchi T, Mukai H, Kitagawa M, Hashimoto T, Maeda K, Ono Y, Tanaka C. A protein kinase, PKN, accumulates in Alzheimer neurofibrillary tangles and associated endoplasmic reticulum-derived vesicles and phosphorylates tau protein. J Neurosci. 1998;18:7402-7410.
5. Manser C, Stevenson A, Banner S, Davies J, Tudor EL, Ono Y, Leigh PN, McLoughlin DM, Shaw CE, Miller CC. Deregulation of PKN1 activity disrupts neurofilament organisation and axonal transport. FEBS Lett. 2008;582:2303-2308.
6. Takahashi M, Mukai H, Toshimori M, Miyamoto M, Ono Y. Proteolytic activation of PKN by caspase-3 or related protease during apoptosis. Proc Natl Acad Sci\USA. 1998;95:11566-11571.
7. Sumioka K, Shirai Y, Sakai N, Hashimoto T, Tanaka C, Yamamoto M, Takahashi M, Ono Y, Saito N. Induction of a 55-kDa PKN cleavage product by ischemia/reperfusion model in the rat retina. Invest Ophthalmol Vis Sci. 2000;41:29-35.
8. Ueyama T, Ren Y, Sakai N, Takahashi M, Ono Y, Kondoh T, Tamaki N, Saito N. Generation of a constitutively active fragment of PKN in microglia/ macrophages after middle cerebral artery occlusion in rats. J Neurochem. 2001;79:903-913.
9. Fischer A, Stuckas H, Gluth M, Russell TD, Rudolph MC, Beeman NE, Bachmann S, Umemura S, Ohashi Y, Neville MC, Theuring F. Impaired tight junction sealing and precocious involution in mammary glands of PKN1 transgenic mice. J Cell Sci. 2007;120:2272-2283.
10. Morissette MR, Sah VP, Glembotski CC, Brown JH. The Rho effector, PKN, regulates ANF gene transcription in cardiomyocytes through a serum response element. Am J Physiol Heart Circ Physiol. 2000;278: H1769-H1774.
11. Yamamoto S, Yang G, Zablocki D, Liu J, Hong C, Kim SJ, Soler S, Odashima M, Thaisz J, Yehia G, Molina CA, Yatani A, Vatner DE, Vatner SF, Sadoshima J. Activation of Mst1 causes dilated cardiomyop-athy by stimulating apoptosis without compensatory ventricular myocyte hypertrophy. J Clin Invest. 2003;111:1463-1474.
12. Morrison LE, Hoover HE, Thuerauf DJ, Glembotski CC. Mimicking phosphorylation of alphaB-crystallin on serine-59 is necessary and sufficient to provide maximal protection of cardiac myocytes from apoptosis. Circ Res. 2003;92:203-211.
13. Kitagawa M, Mukai H, Takahashi M, Ono Y. The role of PKN in the regulation of alphaB-crystallin expression via heat shock transcription factor 1. Biochem Biophys Res Commun. 1998;252:561-565.
14. Djabali K, de Nechaud B, Landon F, Portier MM. AlphaB-crystallin interacts with intermediate filaments in response to stress. J Cell Sci. 1997;110(Pt 21):2759-2769.
15. Eaton P, Fuller W, Bell JR, Shattock MJ. AlphaB crystallin translocation and phosphorylation: signal transduction pathways and preconditioning in the isolated rat heart. J Mol Cell Cardiol. 2001;33:1659-1671.
16. Koteiche HA, McHaourab HS. Mechanism of chaperone function in small heat-shock proteins. Phosphorylation-induced activation of two-mode binding in alphaB-crystallin. J Biol Chem. 2003;278:10361-10367.
17. Davenport KR, Sohaskey M, Kamada Y, Levin DE, Gustin MC. A second osmosensing signal transduction pathway in yeast. Hypotonic shock activates the PKC1 protein kinase-regulated cell integrity pathway. J Biol Chem. 1995;270:30157-30161.
18. Pujol N, Bonet C, Vilella F, Petkova MI, Mozo-Villarias A, de la Torre-Ruiz MA. Two proteins from Saccharomyces cerevisiae: Pfy1 and Pkc1, play a dual role in activating actin polymerization and in increasing cell viability in the adaptive response to oxidative stress. FEMS Yeast Res. 2009;9:1196-1207.
19. Gerik KJ, Bhimireddy SR, Ryerse JS, Specht CA, Lodge JK. PKC1 is essential for protection against both oxidative and nitrosative stresses, cell integrity, and normal manifestation of virulence factors in the pathogenic fungus Cryptococcus neoformans. Eukaryot Cell. 2008;7:1685-1698.
20. Vandenberg JI, Rees SA, Wright AR, Powell T. Cell swelling and ion transport pathways in cardiac myocytes. Cardiovasc Res. 1996;32:85-97.
21. Murphy E, Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev. 2008;88:581-609.
22. Aghajanian A, Wittchen ES, Campbell SL, Burridge K. Direct activation of RhoA by reactive oxygen species requires a redox-sensitive motif. PLoS One. 2009;4:e8045.
23. Gopalakrishna R, Anderson WB. Ca2 +-and phospholipid-independent activation of protein kinase C by selective oxidative modification of the regulatory domain. Proc Natl Acad Sci USA. 1989;86:6758-6762.
24. Budas GR, Churchill EN, Mochly-Rosen D. Cardioprotective mechanisms of PKC isozyme-selective activators and inhibitors in the treatment of ischemia-reperfusion injury. Pharmacol Res. 2007;55:523-536.
25. Deaton RA, Su C, Valencia TG, Grant SR. Transforming growth factor-beta1-induced expression of smooth muscle marker genes involves activation of PKN and p38 MAPK. J Biol Chem. 2005;280:31172-31181.
26. Mukai H, Toshimori M, Shibata H, Takanaga H, Kitagawa M, Miyahara M, Shimakawa M, Ono Y. Interaction of PKN with alpha-actinin. J Biol Chem. 1997;272:4740-4746.
27. Sah VP, Minamisawa S, Tam SP, Wu TH, Dorn GW II, Ross J Jr, Chien KR, Brown JH. Cardiac-specific overexpression of RhoA results in sinus and atrioventricular nodal dysfunction and contractile failure. J Clin Invest. 1999;103:1627-1634.
28. Rossignol TM, Jones SV. Regulation of a family of inwardly rectifying potassium channels (Kir2) by the m1 muscarinic receptor and the small GTPase Rho. Pflugers Arch. 2006;452:164-174.
29. Yatani A, Irie K, Otani T, Abdellatif M, Wei L. RhoA GTPase regulates L-type Ca2+ currents in cardiac myocytes. Am J Physiol Heart Circ Physiol. 2005;288:H650-H659.
30. Arrigo AP, Simon S, Gibert B, Kretz-Remy C, Nivon M, Czekalla A, Guillet D, Moulin M, Diaz-Latoud C, Vicart P. Hsp27 (HspB1) and alphaB-crystallin (HspB5) as therapeutic targets. FEBS Lett. 2007;581:3665-3674.
31. Ray PS, Martin JL, Swanson EA, Otani H, Dillmann WH, Das DK. Transgene overexpression of alphaB crystallin confers simultaneous protection against cardiomyocyte apoptosis and necrosis during myocardial ischemia and reperfusion. FASEB J. 2001;15:393-402.
32. Hoover HE, Thuerauf DJ, Martindale JJ, Glembotski CC. alpha B-crystallin gene induction and phosphorylation by MKK6-activated p38. A potential role for alpha B-crystallin as a target of the p38 branch of the cardiac stress response. J Biol Chem. 2000;275:23825-23833.
33. Singh BN, Rao KS, Ramakrishna T, Rangaraj N, Rao Ch M. Association of alphaB-crystallin, a small heat shock protein, with actin: role in modulating actin filament dynamics in vivo. J Mol Biol. 2007;366:756-767.
34. Eaton P, Awad WI, Miller JI, Hearse DJ, Shattock MJ. Ischemic preconditioning: a potential role for constitutive low molecular weight stress protein translocation and phosphorylation? J Mol Cell Cardiol. 2000;32:961-971.
35. Wang X, Robbins J. Heart failure and protein quality control. Circ Res. 2006;99:1315-1328.
36. Churchill EN, Ferreira JC, Brum PC, Szweda LI, Mochly-Rosen D. Ischaemic preconditioning improves proteasomal activity and increases the degradation of deltaPKC during reperfusion. Cardiovasc Res. 85:385-394.