Cardiovascular Research

Ca2+/Calmodulin-dependent protein kinase II δ mediates myocardial ischemia/reperfusion injury through nuclear factor-κB.

Authors: Haiyun Ling|||Charles B B Gray|||Alexander C Zambon|||Michael Grimm|||Yusu Gu|||Nancy Dalton|||Nicole H Purcell|||Kirk Peterson|||Joan Heller Brown

Affiliations: + Expand

Abstract

Ca(2+)/calmodulin-dependent protein kinase II (CaMKII) has been implicated as a maladaptive mediator of cardiac ischemic injury. We hypothesized that the inflammatory response associated with in vivo ischemia/reperfusion (I/R) is initiated through CaMKII signaling.

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Chemical List

I-kappa B Proteins|||NF-kappa B|||Transcription Factor RelA|||Cyclosporine|||Calcium-Calmodulin-Dependent Protein Kinase Type 2

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Reference List

Murphy E, Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiological reviews. 2008;88:581–609.|||Weiss JN, Korge P, Honda HM, Ping P. Role of the mitochondrial permeability transition in myocardial disease. Circulation research. 2003;93:292–301.|||Coggins M, Rosenzweig A. The fire within: Cardiac inflammatory signaling in health and disease. Circulation research. 2012;110:116–125.|||Entman ML, Michael L, Rossen RD, Dreyer WJ, Anderson DC, Taylor AA, Smith CW. Inflammation in the course of early myocardial ischemia. FASEB journal : official publication of the Federation of American Societies for Experimental Biology. 1991;5:2529–2537.|||Marchant DJ, Boyd JH, Lin DC, Granville DJ, Garmaroudi FS, McManus BM. Inflammation in myocardial diseases. Circulation research. 2012;110:126–144.|||Li C, Browder W, Kao RL. Early activation of transcription factor nf-kappab during ischemia in perfused rat heart. The American journal of physiology. 1999;276:H543–H552.|||Chandrasekar B, Smith JB, Freeman GL. Ischemia-reperfusion of rat myocardium activates nuclear factor-kappab and induces neutrophil infiltration via lipopolysaccharide-induced cxc chemokine. Circulation. 2001;103:2296–2302.|||Izumi T, Saito Y, Kishimoto I, Harada M, Kuwahara K, Hamanaka I, Takahashi N, Kawakami R, Li Y, Takemura G, Fujiwara H, Garbers DL, Mochizuki S, Nakao K. Blockade of the natriuretic peptide receptor guanylyl cyclase-a inhibits nf-kappab activation and alleviates myocardial ischemia/reperfusion injury. The Journal of clinical investigation. 2001;108:203–213.|||Kis A, Yellon DM, Baxter GF. Role of nuclear factor-kappa b activation in acute ischaemia-reperfusion injury in myocardium. British journal of pharmacology. 2003;138:894–900.|||Brown M, McGuinness M, Wright T, Ren X, Wang Y, Boivin GP, Hahn H, Feldman AM, Jones WK. Cardiac-specific blockade of nf-kappab in cardiac pathophysiology: Differences between acute and chronic stimuli in vivo. American journal of physiology. Heart and circulatory physiology. 2005;289:H466–H476.|||Pye J, Ardeshirpour F, McCain A, Bellinger DA, Merricks E, Adams J, Elliott PJ, Pien C, Fischer TH, Baldwin AS, Jr, Nichols TC. Proteasome inhibition ablates activation of nf-kappa b in myocardial reperfusion and reduces reperfusion injury. American journal of physiology. Heart and circulatory physiology. 2003;284:H919–H926.|||Kim YS, Kim JS, Kwon JS, Jeong MH, Cho JG, Park JC, Kang JC, Ahn Y. Bay 11-7082, a nuclear factor-kappab inhibitor, reduces inflammation and apoptosis in a rat cardiac ischemia-reperfusion injury model. International heart journal. 2010;51:348–353.|||Onai Y, Suzuki J, Kakuta T, Maejima Y, Haraguchi G, Fukasawa H, Muto S, Itai A, Isobe M. Inhibition of ikappab phosphorylation in cardiomyocytes attenuates myocardial ischemia/reperfusion injury. Cardiovascular research. 2004;63:51–59.|||Moss NC, Stansfield WE, Willis MS, Tang RH, Selzman CH. Ikkbeta inhibition attenuates myocardial injury and dysfunction following acute ischemia-reperfusion injury. American journal of physiology. Heart and circulatory physiology. 2007;293:H2248–H2253.|||Erickson JR, Joiner ML, Guan X, Kutschke W, Yang J, Oddis CV, Bartlett RK, Lowe JS, O'Donnell SE, Aykin-Burns N, Zimmerman MC, Zimmerman K, Ham AJ, Weiss RM, Spitz DR, Shea MA, Colbran RJ, Mohler PJ, Anderson ME. A dynamic pathway for calcium-independent activation of camkii by methionine oxidation. Cell. 2008;133:462–474.|||Vila-Petroff M, Salas MA, Said M, Valverde CA, Sapia L, Portiansky E, Hajjar RJ, Kranias EG, Mundina-Weilenmann C, Mattiazzi A. Camkii inhibition protects against necrosis and apoptosis in irreversible ischemia-reperfusion injury. Cardiovascular research. 2007;73:689–698.|||Salas MA, Valverde CA, Sanchez G, Said M, Rodriguez JS, Portiansky EL, Kaetzel MA, Dedman JR, Donoso P, Kranias EG, Mattiazzi A. The signalling pathway of camkii-mediated apoptosis and necrosis in the ischemia/reperfusion injury. Journal of molecular and cellular cardiology. 2010;48:1298–1306.|||Zhang R, Khoo MS, Wu Y, Yang Y, Grueter CE, Ni G, Price EE, Jr, Thiel W, Guatimosim S, Song LS, Madu EC, Shah AN, Vishnivetskaya TA, Atkinson JB, Gurevich VV, Salama G, Lederer WJ, Colbran RJ, Anderson ME. Calmodulin kinase ii inhibition protects against structural heart disease. Nature medicine. 2005;11:409–417.|||Singh MV, Kapoun A, Higgins L, Kutschke W, Thurman JM, Zhang R, Singh M, Yang J, Guan X, Lowe JS, Weiss RM, Zimmermann K, Yull FE, Blackwell TS, Mohler PJ, Anderson ME. Ca2+/calmodulin-dependent kinase ii triggers cell membrane injury by inducing complement factor b gene expression in the mouse heart. The Journal of clinical investigation. 2009;119:986–996.|||Zhang X, Wheeler D, Tang Y, Guo L, Shapiro RA, Ribar TJ, Means AR, Billiar TR, Angus DC, Rosengart MR. Calcium/calmodulin-dependent protein kinase (camk) iv mediates nucleocytoplasmic shuttling and release of hmgb1 during lipopolysaccharide stimulation of macrophages. J Immunol. 2008;181:5015–5023.|||Zhang X, Guo L, Collage RD, Stripay JL, Tsung A, Lee JS, Rosengart MR. Calcium/calmodulin-dependent protein kinase (camk) ialpha mediates the macrophage inflammatory response to sepsis. Journal of leukocyte biology. 2011;90:249–261.|||Huang W, Ghisletti S, Perissi V, Rosenfeld MG, Glass CK. Transcriptional integration of tlr2 and tlr4 signaling at the ncor derepression checkpoint. Molecular cell. 2009;35:48–57.|||Ling H, Zhang T, Pereira L, Means CK, Cheng H, Gu Y, Dalton ND, Peterson KL, Chen J, Bers D, Brown JH. Requirement for ca2+/calmodulin-dependent kinase ii in the transition from pressure overload-induced cardiac hypertrophy to heart failure in mice. The Journal of clinical investigation. 2009;119:1230–1240.|||Tobimatsu T, Fujisawa H. Tissue-specific expression of four types of rat calmodulin-dependent protein kinase ii mrnas. The Journal of biological chemistry. 1989;264:17907–17912.|||Schworer CM, Rothblum LI, Thekkumkara TJ, Singer HA. Identification of novel isoforms of the delta subunit of ca2+/calmodulin-dependent protein kinase ii. Differential expression in rat brain and aorta. The Journal of biological chemistry. 1993;268:14443–14449.|||Mayer P, Mohlig M, Idlibe D, Pfeiffer A. Novel and uncommon isoforms of the calcium sensing enzyme calcium/calmodulin dependent protein kinase ii in heart tissue. Basic research in cardiology. 1995;90:372–379.|||Baltas LG, Karczewski P, Krause EG. The cardiac sarcoplasmic reticulum phospholamban kinase is a distinct delta-cam kinase isozyme. FEBS letters. 1995;373:71–75.|||Chen J, Kubalak SW, Chien KR. Ventricular muscle-restricted targeting of the rxralpha gene reveals a non-cell-autonomous requirement in cardiac chamber morphogenesis. Development. 1998;125:1943–1949.|||Zambon AC, Zhang L, Minovitsky S, Kanter JR, Prabhakar S, Salomonis N, Vranizan K, Dubchak I, Conklin BR, Insel PA. Gene expression patterns define key transcriptional events in cell-cycle regulation by camp and protein kinase a. Proceedings of the National Academy of Sciences of the United States of America. 2005;102:8561–8566.|||Passier R, Zeng H, Frey N, Naya FJ, Nicol RL, McKinsey TA, Overbeek P, Richardson JA, Grant SR, Olson EN. Cam kinase signaling induces cardiac hypertrophy and activates the mef2 transcription factor in vivo. The Journal of clinical investigation. 2000;105:1395–1406.|||Gordon JW, Shaw JA, Kirshenbaum LA. Multiple facets of nf-kappab in the heart: To be or not to nf-kappab. Circulation research. 2011;108:1122–1132.|||Haudek SB, Spencer E, Bryant DD, White DJ, Maass D, Horton JW, Chen ZJ, Giroir BP. Overexpression of cardiac i-kappabalpha prevents endotoxin-induced myocardial dysfunction. American journal of physiology. Heart and circulatory physiology. 2001;280:H962–H968.|||Chao W. Toll-like receptor signaling: A critical modulator of cell survival and ischemic injury in the heart. American journal of physiology. Heart and circulatory physiology. 2009;296:H1–H12.|||Singh MV, Swaminathan PD, Luczak ED, Kutschke W, Weiss RM, Anderson ME. Myd88 mediated inflammatory signaling leads to camkii oxidation, cardiac hypertrophy and death after myocardial infarction. Journal of molecular and cellular cardiology. 2012;52:1135–1144.|||Thiemermann C. Inhibition of the activation of nuclear factor kappa b to reduce myocardial reperfusion injury and infarct size. Cardiovascular research. 2004;63:8–10.|||Kashiwase K, Higuchi Y, Hirotani S, Yamaguchi O, Hikoso S, Takeda T, Watanabe T, Taniike M, Nakai A, Tsujimoto I, Matsumura Y, Ueno H, Nishida K, Hori M, Otsu K. Camkii activates ask1 and nf-kappab to induce cardiomyocyte hypertrophy. Biochemical and biophysical research communications. 2005;327:136–142.|||Liu X, Yao M, Li N, Wang C, Zheng Y, Cao X. Camkii promotes tlr-triggered proinflammatory cytokine and type i interferon production by directly binding and activating tak1 and irf3 in macrophages. Blood. 2008;112:4961–4970.|||Kolattukudy PE, Niu J. Inflammation, endoplasmic reticulum stress, autophagy, and the monocyte chemoattractant protein-1/ccr2 pathway. Circulation research. 2012;110:174–189.