Circulation Research. 2002;90:390-397
Published online before print February 7, 2002, doi: 10.1161/01.RES.0000012702.90501.8D
Published online before print February 7, 2002, doi: 10.1161/01.RES.0000012702.90501.8D
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© 2002 American Heart Association, Inc.
Molecular Medicine |
Mitochondrial PKC
and MAPK Form Signaling Modules in the Murine Heart
Enhanced Mitochondrial PKC-MAPK Interactions and Differential MAPK Activation in PKC-Induced Cardioprotection
From the Department of Physiology and Biophysics and the Department of Medicine/Division of Cardiology, University of Louisville, and the Jewish Hospital Heart and Lung Institute, Louisville, Ky.
Correspondence to Peipei Ping, PhD, Department of Physiology and Biophysics and Division of Cardiology, Suite 122, Baxter Building, 570 S Preston St, Louisville, KY 40202. E-mail ping{at}ntr.net or peipeiping@hotmail.com
Although activation of protein kinase C (PKC) 
and mitogen-activated protein kinases (MAPKs) are known to play crucial roles in the manifestation of cardioprotection, the spatial organization of PKC signaling modules in naïve and protected myocardium remains unknown. Based on evidence that mitochondria are key mediators of the cardioprotective signal, we hypothesized that PKC and MAPKs interact, and that they form functional signaling modules in mitochondria during cardioprotection. Both immunoblotting and immunofluorescent staining demonstrated that PKC, ERKs, JNKs, and p38 MAPK co-localized with cardiac mitochondria. Moreover, transgenic activation of PKC greatly increased mitochondrial PKC expression and activity, which was concomitant with increased mitochondrial interaction of PKC with ERKs, JNKs, and p38 as determined by co-immunoprecipitation. These complex formations appeared to be independent of PKC activity, as the interactions were also observed in mice expressing inactive PKC. However, although both active and inactive PKC bound to all three MAPKs, increased phosphorylation of mitochondrial ERKs was only observed in mice expressing active PKC but not in mice expressing inactive PKC. Examination of potential downstream targets of mitochondrial PKC-ERK signaling modules revealed that phosphorylation of the pro-apoptotic protein Bad was elevated in mitochondria. Together, these data show that PKC forms subcellular-targeted signaling modules with ERKs, leading to the activation of mitochondrial ERKs. Furthermore, formation of mitochondrial PKC-ERK modules appears to play a role in PKC-mediated cardioprotection, in part by the phosphorylation and inactivation of Bad.
Key Words: mitochondria • protein-protein interactions • functional proteomics • signaling modules • cardioprotection
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X. Wang, C. Yin, L. Xi, and R. C. Kukreja Opening of Ca2+-activated K+ channels triggers early and delayed preconditioning against I/R injury independent of NOS in mice Am J Physiol Heart Circ Physiol, November 1, 2004; 287(5): H2070 - H2077. [Abstract] [Full Text] [PDF]
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M. Zaugg and M. C. Schaub Cellular mechanisms in sympatho-modulation of the heart Br. J. Anaesth., July 1, 2004; 93(1): 34 - 52. [Abstract] [Full Text] [PDF]
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V. U. Rao, H. Shiraishi, and P. J. McDermott PKC-{epsilon} regulation of extracellular signal-regulated kinase: a potential role in phenylephrine-induced cardiocyte growth Am J Physiol Heart Circ Physiol, June 1, 2004; 286(6): H2195 - H2203. [Abstract] [Full Text] [PDF]
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H. Tong, H. A. Rockman, W. J. Koch, C. Steenbergen, and E. Murphy G Protein-Coupled Receptor Internalization Signaling Is Required for Cardioprotection in Ischemic Preconditioning Circ. Res., April 30, 2004; 94(8): 1133 - 1141. [Abstract] [Full Text] [PDF]
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D. J. Lips, O. F. Bueno, B. J. Wilkins, N. H. Purcell, R. A. Kaiser, J. N. Lorenz, L. Voisin, M. K. Saba-El-Leil, S. Meloche, J. Pouyssegur, et al. MEK1-ERK2 Signaling Pathway Protects Myocardium From Ischemic Injury In Vivo Circulation, April 27, 2004; 109(16): 1938 - 1941. [Abstract] [Full Text] [PDF]
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R. A. Kaiser, O. F. Bueno, D. J. Lips, P. A. Doevendans, F. Jones, T. F. Kimball, and J. D. Molkentin Targeted Inhibition of p38 Mitogen-activated Protein Kinase Antagonizes Cardiac Injury and Cell Death Following Ischemia-Reperfusion in Vivo J. Biol. Chem., April 9, 2004; 279(15): 15524 - 15530. [Abstract] [Full Text] [PDF]
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P. Rosini, G. De Chiara, P. Bonini, M. Lucibello, M. E. Marcocci, E. Garaci, F. Cozzolino, and M. Torcia Nerve Growth Factor-dependent Survival of CESS B Cell Line Is Mediated by Increased Expression and Decreased Degradation of MAPK Phosphatase 1 J. Biol. Chem., April 2, 2004; 279(14): 14016 - 14023. [Abstract] [Full Text] [PDF]
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A. P Halestrap, S. J Clarke, and S. A Javadov Mitochondrial permeability transition pore opening during myocardial reperfusion--a target for cardioprotection Cardiovasc Res, February 15, 2004; 61(3): 372 - 385. [Abstract] [Full Text] [PDF]
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F. Eefting, B. Rensing, J. Wigman, W. J. Pannekoek, W. M. Liu, M. J. Cramer, D. J Lips, and P. A Doevendans Role of apoptosis in reperfusion injury Cardiovasc Res, February 15, 2004; 61(3): 414 - 426. [Abstract] [Full Text] [PDF]
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G. Nowak, D. Bakajsova, and G. L. Clifton Protein kinase C-{epsilon} modulates mitochondrial function and active Na+ transport after oxidant injury in renal cells Am J Physiol Renal Physiol, February 1, 2004; 286(2): F307 - F316. [Abstract] [Full Text] [PDF]
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E. Murphy Primary and Secondary Signaling Pathways in Early Preconditioning That Converge on the Mitochondria to Produce Cardioprotection Circ. Res., January 9, 2004; 94(1): 7 - 16. [Abstract] [Full Text] [PDF]
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M. Joyeux-Faure, C. Arnaud, D. Godin-Ribuot, and C. Ribuot Heat stress preconditioning and delayed myocardial protection: what is new? Cardiovasc Res, December 1, 2003; 60(3): 469 - 477. [Abstract] [Full Text] [PDF]
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B. P. S. Kang, A. Urbonas, A. Baddoo, S. Baskin, A. Malhotra, and L. G. Meggs IGF-1 inhibits the mitochondrial apoptosis program in mesangial cells exposed to high glucose Am J Physiol Renal Physiol, November 1, 2003; 285(5): F1013 - F1024. [Abstract] [Full Text] [PDF]
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P. Ping Identification of Novel Signaling Complexes by Functional Proteomics Circ. Res., October 3, 2003; 93(7): 595 - 603. [Abstract] [Full Text] [PDF]
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D. M. YELLON and J. M. DOWNEY Preconditioning the Myocardium: From Cellular Physiology to Clinical Cardiology Physiol Rev, October 1, 2003; 83(4): 1113 - 1151. [Abstract] [Full Text] [PDF]
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J. N. Weiss, P. Korge, H. M. Honda, and P. Ping Role of the Mitochondrial Permeability Transition in Myocardial Disease Circ. Res., August 22, 2003; 93(4): 292 - 301. [Abstract] [Full Text] [PDF]
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C. P. Baines, C.-X. Song, Y.-T. Zheng, G.-W. Wang, J. Zhang, O.-L. Wang, Y. Guo, R. Bolli, E. M. Cardwell, and P. Ping Protein Kinase C{epsilon} Interacts With and Inhibits the Permeability Transition Pore in Cardiac Mitochondria Circ. Res., May 2, 2003; 92(8): 873 - 880. [Abstract] [Full Text] [PDF]
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L. G. Kevin, A. K. S. Camara, M. L. Riess, E. Novalija, and D. F. Stowe Ischemic preconditioning alters real-time measure of O2 radicals in intact hearts with ischemia and reperfusion Am J Physiol Heart Circ Physiol, February 1, 2003; 284(2): H566 - H574. [Abstract] [Full Text] [PDF]
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C. Steenbergen, C. A. Afshari, J. G. Petranka, J. Collins, K. Martin, L. Bennett, A. Haugen, P. Bushel, and E. Murphy Alterations in apoptotic signaling in human idiopathic cardiomyopathic hearts in failure Am J Physiol Heart Circ Physiol, January 1, 2003; 284(1): H268 - H276. [Abstract] [Full Text] [PDF]
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K. A. Detillieux, F. Sheikh, E. Kardami, and P. A. Cattini Biological activities of fibroblast growth factor-2 in the adult myocardium Cardiovasc Res, January 1, 2003; 57(1): 8 - 19. [Abstract] [Full Text] [PDF]
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O. F. Bueno and J. D. Molkentin Involvement of Extracellular Signal-Regulated Kinases 1/2 in Cardiac Hypertrophy and Cell Death Circ. Res., November 1, 2002; 91(9): 776 - 781. [Abstract] [Full Text] [PDF]
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U. Schwanke, I. Konietzka, A. Duschin, X. Li, R. Schulz, and G. Heusch No ischemic preconditioning in heterozygous connexin43-deficient mice Am J Physiol Heart Circ Physiol, October 1, 2002; 283 (4): H1740 - H1742. [Abstract] [Full Text] [PDF]
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 R. D. Edmondson, T. M. Vondriska, K. J. Biederman, J. Zhang, R. C. Jones, Y. Zheng, D. L. Allen, J. X. Xiu, E. M. Cardwell, M. R. Pisano, et al. Protein Kinase C {epsilon} Signaling Complexes Include Metabolism- and Transcription/Translation-related Proteins: Complimentary Separation Techniques With LC/MS/MS Mol. Cell. Proteomics, June 1, 2002; 1(6): 421 - 433. [Abstract] [Full Text] [PDF]
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