Review

You have free access to this content

Mitochondria: A mirror into cellular dysfunction in heart disease

  1. Melanie Y. White Dr.1,3,*,
  2. Alistair V. G. Edwards2,
  3. Stuart J. Cordwell1,2,
  4. Jennifer E. Van Eyk3,4,5,6

Article first published online: 12 JUN 2008

DOI: 10.1002/prca.200780135

Issue

PROTEOMICS - Clinical Applications

PROTEOMICS - Clinical Applications

Special Issue: CARDIOVASCULAR PROTEOMICS

Volume 2, Issue 6, pages 845–861, No. 6 June 2008

Additional Information

How to Cite

White, M. Y., Edwards, A. V. G., Cordwell, S. J. and Van Eyk, J. E. (2008), Mitochondria: A mirror into cellular dysfunction in heart disease. Prot. Clin. Appl., 2: 845–861. doi: 10.1002/prca.200780135

Author Information

  1. 1

    School of Molecular and Microbial Biosciences, University of Sydney, New South Wales, Australia

  2. 2

    Discipline of Pathology, School of Medical Sciences, University of Sydney, New South Wales, Australia

  3. 3

    Department of Medicine, Johns Hopkins University, Baltimore, MD, USA

  4. 4

    Department of Biological Chemistry, Johns Hopkins University, Baltimore, MD, USA

  5. 5

    Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA

  6. 6

    The Technical Implementation and Coordination Core of NHLBI Proteomics Centre, Johns Hopkins University, Baltimore, MD, USA

*601 Mason F Lord Building, Centre Tower, 5200 Eastern Ave, Johns Hopkins University, Baltimore, MD 21224, USA Fax: +1-410-550-8712

Publication History

  1. Issue published online: 12 JUN 2008
  2. Article first published online: 12 JUN 2008
  3. Manuscript Received: 25 NOV 2007

Funded by

  • National Health and Medical Research Foundation. Grant Number: 464905
  • University of Sydney
  • National Heart Lung and Blood Institute Proteomic Initiative. Grant Number: N0-HV-28180
  • NIH. Grant Number: P01HL081427 and P01HL077180
  • Donald P. Amos Family Foundation

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

Get PDF (355K)

References

  • 1
    Robinson, D. J., Christenson, R. H., Creatine kinase and its CK-MB isoenzyme: the conventional marker for the diagnosis of acute myocardial infarction. J. Emerg. Med. 1999, 17, 95–104.
  • 2
    Schlattner, U., Tokarska-Schlattner, M., Wallimann, T., Mitochondrial creatine kinase in human health and disease. Biochim. Biophys. Acta 2006, 1762, 164–180.
  • 3
    Collins, T. J., Berridge, M. J., Lipp, P., Bootman, M. D., Mitochondria are morphologically and functionally heterogeneous within cells. EMBO J. 2002, 21, 1616–1627.
  • 4
    Forner, F., Foster, L. J., Campanaro, S., Valle, G., Mann, M., Quantitative proteomic comparison of rat mitochondria from muscle, heart, and liver. Mol. Cell. Proteomics 2006, 5, 608–619.
  • 5
    Johnson, D. T., Harris, R. A., French, S., Blair, P. V. et al., Tissue heterogeneity of the mammalian mitochondrial proteome. Am. J. Physiol. Cell Physiol. 2007, 292, C689–C697.
  • 6
    Palmer, J. W., Tandler, B., Hoppel, C. L., Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J. Biol. Chem. 1977, 252, 8731–8739.
  • 7
    McMillin-Wood, J., Wolkowicz, P. E., Chu, A., Tate, C. A. et al., Calcium uptake by two preparations of mitochondria from heart. Biochim. Biophys. Acta 1980, 591, 251–265.
  • 8
    Van Jaarsveld, H., Lochner, A., Oxidative phosphorylation function of two mitochondrial preparations from heart: effects of ischaemia and cytochrome C. Basic Res. Cardiol. 1982, 77, 388–403.
  • 9
    Duan, J. M., Karmazyn, M., Acute effects of hypoxia and phosphate on two populations of heart mitochondria. Mol. Cell. Biochem. 1989, 90, 47–56.
  • 10
    Agnetti, G., Kane, L. A., Guarnieri, C., Caldarera, C. M., Van Eyk, J. E., Proteomic technologies in the study of kinases: novel tools for the investigation of PKC in the heart. Pharmacol. Res. 2007, 55, 511–522.
  • 11
    Da Cruz, S., Parone, P. A., Martinou, J. C., Building the mitochondrial proteome. Expert Rev. Proteomics 2005, 2, 541–551.
  • 12
    Gabaldon, T., Huynen, M. A., Shaping the mitochondrial proteome. Biochim. Biophys. Acta 2004, 1659, 212–220.
  • 13
    McDonald, T. G., Van Eyk, J. E., Mitochondrial proteomics Undercover in the lipid bilayer. Basic Res. Cardiol. 2003, 98, 219–227.
  • 14
    Verma, M., Kagan, J., Sidransky, D., Srivastava, S., Proteomic analysis of cancer-cell mitochondria. Nat. Rev. Cancer 2003, 3, 789–795.
  • 15
    Ferrari, R., Oxygen-free radicals at myocardial level: effects of ischaemia and reperfusion. Adv. Exp. Med. Biol. 1994, 366, 99–111.
  • 16
    Di Lisa, F., Menabo, R., Canton, M., Petronilli, V., The role of mitochondria in the salvage and the injury of the ischemic myocardium. Biochim. Biophys. Acta 1998, 1366, 69–78.
  • 17
    Liu, Y., Sato, T., O'Rourke, B., Marban, E., Mitochondrial ATP-dependent potassium channels: novel effectors of cardioprotection? Circulation 1998, 97, 2463–2469.
  • 18
    Sato, T., Sasaki, N., Seharaseyon, J., O'Rourke, B., Marban, E., Selective pharmacological agents implicate mitochondrial but not sarcolemmal K(ATP) channels in ischemic cardioprotection. Circulation 2000, 101, 2418–2423.
  • 19
    Flameng, W., Andres, J., Ferdinande, P., Mattheussen, M., Van Belle, H., Mitochondrial function in myocardial stunning. J. Mol. Cell. Cardiol. 1991, 23, 1–11.
  • 20
    Rouslin, W., Mitochondrial complexes I, II, III, IV, and V in myocardial ischemia and autolysis. Am. J. Physiol. Heart Circ. Physiol. 1983, 244, H743–748.
  • 21
    Ataka, K., Chen, D., Levitsky, S., Jimenez, E., Feinberg, H., Effect of aging on intracellular Ca 2+, pHi, and contractility during ischemia and reperfusion. Circulation 1992, 86, II371–376.
  • 22
    Shlafer, M., Myers, C. L., Adkins, S., Mitochondrial hydrogen peroxide generation and activities of glutathione peroxidase and superoxide dismutase following global ischemia. J. Mol. Cell. Cardiol. 1987, 19, 1195–1206.
  • 23
    Ferrari, R., The role of mitochondria in ischemic heart disease. J. Cardiovasc. Pharmacol. 1996, 28 Suppl 1, S1–S10.
  • 24
    Lesnefsky, E. J., Moghaddas, S., Tandler, B., Kerner, J., Hoppel, C. L., Mitochondrial dysfunction in cardiac disease: ischemia–reperfusion, aging, and heart failure. J. Mol. Cell. Cardiol. 2001, 33, 1065–1089.
  • 25
    Allen, B. S., Rosenkranz, E. R., Buckberg, G. D., Vinten-Johansen, J. et al., High oxygen requirements of dyskinetic cardiac muscle. J. Thorac. Cardiovasc. Surg. 1986, 92, 543–552.
  • 26
    Laster, S. B., Becker, L. C., Ambrosio, G., Jacobus, W. E., Reduced aerobic metabolic efficiency in globally “stunned” myocardium. J. Mol. Cell. Cardiol. 1989, 21, 419–426.
  • 27
    Schipke, J. D., Korbmacher, B., Schwanke, U., Frehen, D. et al., Basal metabolism does not account for high O2 consumption in stunned myocardium. Am. J. Physiol. Heart Circ. Physiol. 1998, 274, H743–746.
  • 28
    Schwanke, U., Heusch, G., Schipke, J. D., Mismatch of local blood flow and oxidative metabolism in stunned myocardium. Physiol Res 2002, 51, 17–25.
  • 29
    Burkhoff, D., Myocardial energetics and the postischemic heart. [comment]. Ann. Thorac. Surg. 1990, 49, 525–527.
  • 30
    Jeremy, R. W., Koretsune, Y., Marban, E., Becker, L. C., Relation between glycolysis and calcium homeostasis in postischemic myocardium. Circ. Res. 1992, 70, 1180–1190.
  • 31
    Narula, J., Haider, N., Virmani, R., DiSalvo, T. G. et al., Apoptosis in myocytes in end-stage heart failure. N. Engl. J. Med. 1996, 335, 1182–1189.
  • 32
    Saraste, A., Pulkki, K., Kallajoki, M., Henriksen, K. et al., Apoptosis in human acute myocardial infarction. Circulation 1997, 95, 320–323.
  • 33
    Dec, G. W., Fuster, V., Idiopathic dilated cardiomyopathy. N. Engl. J. Med. 1994, 331, 1564–1575.
  • 34
    Zhang, H., Li, Y., McClean, D. R., Richardson, P. J, et al., Detection of enterovirus capsid protein VP1 in myocardium from cases of myocarditis or dilated cardiomyopathy by immunohistochemistry: further evidence of enterovirus persistence in myocytes. Med. Microbiol. Immunol. 2004, 193, 109–114.
  • 35
    Stern, T. N., Dilated cardiomyopathy: current concepts. Compr. Ther. 1986, 12, 57–62.
  • 36
    Towbin, J. A., Solaro, R. J., Genetics of dilated cardiomyopathy: more genes that kill. J. Am. Coll. Cardiol. 2004, 44, 2041–2043.
  • 37
    Bione, S., D'Adamo, P., Maestrini, E., Gedeon, A. K. et al., A novel X-linked gene, G4.5. is responsible for Barth syndrome. Nat. Genet. 1996, 12, 385–389.
  • 38
    Barth, P. G., Scholte, H. R., Berden, J. A., Van der Klei-Van Moorsel, J. M. et al., An X-linked mitochondrial disease affecting cardiac muscle, skeletal muscle and neutrophil leucocytes. J. Neurol. Sci. 1983, 62, 327–355.
  • 39
    Schlame, M., Kelley, R. I., Feigenbaum, A., Towbin, J. A. et al., Phospholipid abnormalities in children with Barth syndrome. J. Am. Coll. Cardiol. 2003, 42, 1994–1999.
  • 40
    Marin-Garcia, J., Goldenthal, M. J., Ananthakrishnan, R., Pierpont, M. E. et al., Mitochondrial function in children with idiopathic dilated cardiomyopathy. J. Inherit. Metab. Dis. 1996, 19, 309–312.
  • 41
    Quigley, A. F., Kapsa, R. M., Esmore, D., Hale, G., Byrne, E., Mitochondrial respiratory chain activity in idiopathic dilated cardiomyopathy. J. Card. Fail. 2000, 6, 47–55.
  • 42
    Liao, R., Nascimben, L., Friedrich, J., Gwathmey, J. K., Ingwall, J. S., Decreased energy reserve in an animal model of dilated cardiomyopathy. Relationship to contractile performance. Circ. Res. 1996, 78, 893–902.
  • 43
    Conway, M. A., Allis, J., Ouwerkerk, R., Niioka, T. et al., Detection of low phosphocreatine to ATP ratio in failing hypertrophied human myocardium by 31P magnetic resonance spectroscopy. Lancet 1991, 338, 973–976.
  • 44
    Hardy, C. J., Weiss, R. G., Bottomley, P. A., Gerstenblith, G., Altered myocardial high-energy phosphate metabolites in patients with dilated cardiomyopathy. Am. Heart J. 1991, 122, 795–801.
  • 45
    Neubauer, S., Krahe, T., Schindler, R., Horn, M. et al., 31P magnetic resonance spectroscopy in dilated cardiomyopathy and coronary artery disease. Altered cardiac high-energy phosphate metabolism in heart failure. Circulation 1992, 86, 1810–1818.
  • 46
    Herrmann, G., Decherd, G. M., The chemical nature of heart failure. Ann. Intern. Med. 1939, 12, 1233–1244.
  • 47
    Ingwall, J. S., Weiss, R. G., Is the failing heart energy starved? On using chemical energy to support cardiac function. Circ. Res. 2004, 95, 135–145.
  • 48
    Ventura-Clapier, R., Garnier, A., Veksler, V., Energy metabolism in heart failure. J. Physiol. 2004, 555, 1–13.
    Direct Link:
  • 49
    Neubauer, S., The failing heart--an engine out of fuel. N. Engl. J. Med. 2007, 356, 1140–1151.
  • 50
    Gomberg-Maitland, M., Baran, D. A., Fuster, V., Treatment of congestive heart failure: guidelines for the primary care physician and the heart failure specialist. Arch. Intern. Med. 2001, 161, 342–352.
  • 51
    Shen, W., Asai, K., Uechi, M., Mathier, M. A. et al., Progressive loss of myocardial ATP due to a loss of total purines during the development of heart failure in dogs: a compensatory role for the parallel loss of creatine. Circulation 1999, 100, 2113–2118.
  • 52
    Barger, P. M., Kelly, D. P., Fatty acid utilization in the hypertrophied and failing heart: molecular regulatory mechanisms. Am. J. Med. Sci. 1999, 318, 36–42.
  • 53
    Osorio, J. C., Stanley, W. C., Linke, A., Castellari, M. et al., Impaired myocardial fatty acid oxidation and reduced protein expression of retinoid X receptor-alpha in pacing-induced heart failure. Circulation 2002, 106, 606–612.
  • 54
    Sabbah, H. H., Stanley, W. C., Partial fatty acid oxidation inhibitors: a potentially new class of drugs for heart failure. Eur. J. Heart Fail. 2002, 4, 3–6.
  • 55
    Kalsi, K. K., Smolenski, R. T., Pritchard, R. D., Khaghani, A. et al., Energetics and function of the failing human heart with dilated or hypertrophic cardiomyopathy. Eur. J. Clin. Invest. 1999, 29, 469–477.
    Direct Link:
  • 56
    Razeghi, P., Young, M. E., Alcorn, J. L., Moravec, C. S. et al., Metabolic gene expression in fetal and failing human heart. Circulation 2001, 104, 2923–2931.
  • 57
    Taylor, M., Wallhaus, T. R., Degrado, T. R., Russell, D. C. et al., An evaluation of myocardial fatty acid and glucose uptake using PET with [18F]fluoro-6-thia-heptadecanoic acid and [18F]FDG in patients with congestive heart failure. J. Nucl. Med. 2001, 42, 55–62.
  • 58
    Casademont, J., Miro, O., Electron transport chain defects in heart failure. Heart Fail. Rev. 2002, 7, 131–139.
  • 59
    Marin-Garcia, J., Goldenthal, M. J., Moe, G. W., Abnormal cardiac and skeletal muscle mitochondrial function in pacing-induced cardiac failure. Cardiovasc. Res. 2001, 52, 103–110.
  • 60
    Murray, A. J., Anderson, R. E., Watson, G. C., Radda, G. K., Clarke, K., Uncoupling proteins in human heart. Lancet 2004, 364, 1786–1788.
  • 61
    Beer, M., Seyfarth, T., Sandstede, J., Landschutz, W. et al., Absolute concentrations of high-energy phosphate metabolites in normal, hypertrophied, and failing human myocardium measured noninvasively with (31)P-SLOOP magnetic resonance spectroscopy. J. Am. Coll. Cardiol. 2002, 40, 1267–1274.
  • 62
    Nascimben, L., Ingwall, J. S., Pauletto, P., Friedrich, J. et al., Creatine kinase system in failing and nonfailing human myocardium. Circulation 1996, 94, 1894–1901.
  • 63
    Weiss, R. G., Gerstenblith, G., Bottomley, P. A., ATP flux through creatine kinase in the normal, stressed, and failing human heart. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 808–813.
  • 64
    Ye, Y., Gong, G., Ochiai, K., Liu, J., Zhang, J., High-energy phosphate metabolism and creatine kinase in failing hearts: a new porcine model. Circulation 2001, 103, 1570–1576.
  • 65
    Trifunovic, A., Mitochondrial DNA and ageing. Biochim. Biophys. Acta 2006, 1757, 611–617.
  • 66
    Cleland, K. W., Slater, E. C., Respiratory granules of heart muscle. Biochem. J. 1953, 53, 547–556.
  • 67
    Lochner, A., Brink, A. J., Oxidative phosphorylation and glycolysis in the hereditary muscular dystrophy of the Syrian hamster. Clin. Sci. 1967, 33, 409–423.
  • 68
    Pande, S. V., Blanchaer, M. C., Preferential loss of ATP-dependent long-chain fatty acid activating enzyme in mitochondria prepared using Nagarse. Biochim. Biophys. Acta 1970, 202, 43–48.
  • 69
    Hansford, R. G., Lipid oxidation by heart mitochondria from young adult and senescent rats. Biochem. J. 1978, 170, 285–295.
  • 70
    Hoppel, C. L., Tandler, B., Parland, W., Turkaly, J. S., Albers, L. D., Hamster cardiomyopathy. A defect in oxidative phosphorylation in the cardiac interfibrillar mitochondria. J. Biol. Chem. 1982, 257, 1540–1548.
  • 71
    Wolkowicz, P. E., McMillin-Wood, J., Respiration-dependent calcium ion uptake by two preparations of cardiac mitochondria. Effects of palmitoyl-coenzyme A and palmitoylcarnitine on calcium ion cycling and nicotinamide nucleotide reduction state. Biochem. J. 1980, 186, 257–266.
  • 72
    Di Lisa, F., Menabo, R., Canton, M., Barile, M., Bernardi, P., Opening of the mitochondrial permeability transition pore causes depletion of mitochondrial and cytosolic NAD+ and is a causative event in the death of myocytes in postischemic reperfusion of the heart. J. Biol. Chem. 2001, 276, 2571–2575.
  • 73
    Da Cruz, S., Xenarios, I., Langridge, J., Vilbois, F. et al., Proteomic analysis of the mouse liver mitochondrial inner membrane. J. Biol. Chem. 2003, 278, 41566–41571.
  • 74
    Fountoulakis, M., Berndt, P., Langen, H., Suter, L., The rat liver mitochondrial proteins. Electrophoresis 2002, 23, 311–328.
    Direct Link:
  • 75
    Fountoulakis, M., Schlaeger, E. J., The mitochondrial proteins of the neuroblastoma cell line IMR-32. Electrophoresis 2003, 24, 260–275.
    Direct Link:
  • 76
    Kim, N., Lee, Y., Kim, H., Joo, H. et al., Potential biomarkers for ischemic heart damage identified in mitochondrial proteins by comparative proteomics. Proteomics 2006, 6, 1237–1249.
    Direct Link:
  • 77
    Mootha, V. K., Bunkenborg, J., Olsen, J. V., Hjerrild, M. et al., Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 2003, 115, 629–640.
  • 78
    Rabilloud, T., Kieffer, S., Procaccio, V., Louwagie, M. et al., Two-dimensional electrophoresis of human placental mitochondria and protein identification by mass spectrometry: toward a human mitochondrial proteome. Electrophoresis 1998, 19, 1006–1014.
    Direct Link:
  • 79
    Scheffler, N. K., Miller, S. W., Carroll, A. K., Anderson, C. et al., Two-dimensional electrophoresis and mass spectrometric identification of mitochondrial proteins from an SH-SY5Y neuroblastoma cell line. Mitochondrion 2001, 1, 161–179.
  • 80
    Schilling, B., Murray, J., Yoo, C. B., Row, R. H. et al., Proteomic analysis of succinate dehydrogenase and ubiquinol-cytochrome c reductase (Complex II and III) isolated by immunoprecipitation from bovine and mouse heart mitochondria. Biochim. Biophys. Acta 2006, 1762, 213–222.
  • 81
    Taylor, S. W., Warnock, D. E., Glenn, G. M., Zhang, B. et al., An alternative strategy to determine the mitochondrial proteome using sucrose gradient fractionation and 1D PAGE on highly purified human heart mitochondria. J. Proteome Res. 2002, 1, 451–458.
  • 82
    Taylor, S. W., Fahy, E., Zhang, B., Glenn, G. M. et al., Characterization of the human heart mitochondrial proteome. Nat. Biotechnol. 2003, 21, 281–286.
  • 83
    Kane, L. A., Yung, C. K., Agnetti, G., Neverova, I., Van Eyk, J. E., Optimization of paper bridge loading for 2-DE analysis in the basic pH region: Application to the mitochondrial subproteome. Proteomics 2006.
    Direct Link:
  • 84
    McDonald, T., Sheng, S., Stanley, B., Chen, D. et al., Expanding the subproteome of the inner mitochondria using protein separation technologies: one- and two-dimensional liquid chromatography and two-dimensional gel electrophoresis. Mol. Cell. Proteomics 2006, 5, 2392–2411.
  • 85
    Pedersen, P. L., Greenawalt, J. W., Reynafarje, B., Hullihen, J. et al., Preparation and characterization of mitochondria and submitochondrial particles of rat liver and liver-derived tissues. Methods Cell Biol. 1978, 20, 411–481.
  • 86
    Lopez, M. F., Kristal, B. S., Chernokalskaya, E., Lazarev, A. et al., High-throughput profiling of the mitochondrial proteome using affinity fractionation and automation. Electrophoresis 2000, 21, 3427–3440.
    Direct Link:
  • 87
    Foster, D. B., Noguchi, T., VanBuren, P., Murphy, A. M., Van Eyk, J. E., C-terminal truncation of cardiac troponin I causes divergent effects on ATPase and force: implications for the pathophysiology of myocardial stunning. Circ. Res. 2003, 93, 917–924.
  • 88
    White, M. Y., Cordwell, S. J., McCarron, H. C., Tchen, A. S. et al., Modifications of myosin-regulatory light chain correlate with function of stunned myocardium. J. Mol. Cell. Cardiol. 2003, 35, 833–840.
  • 89
    Yuan, C., Ravi, R., Murphy, A. M., Discovery of disease-induced post-translational modifications in cardiac contractile proteins. Curr. Opin. Mol. Ther. 2005, 7, 234–239.
  • 90
    Veitch, K., Hombroeckx, A., Caucheteux, D., Pouleur, H., Hue, L., Global ischaemia induces a biphasic response of the mitochondrial respiratory chain. Anoxic pre-perfusion protects against ischaemic damage. Biochem. J. 1992, 281, 709–715.
  • 91
    Sadek, H. A., Humphries, K. M., Szweda, P. A., Szweda, L. I., Selective inactivation of redox-sensitive mitochondrial enzymes during cardiac reperfusion. Arch. Biochem. Biophys. 2002, 406, 222–228.
  • 92
    Lucas, D. T., Szweda, L. I., Declines in mitochondrial respiration during cardiac reperfusion: age-dependent inactivation of alpha-ketoglutarate dehydrogenase. Proc. Natl. Acad. Sci. USA 1999, 96, 6689–6693.
  • 93
    Hardy, L., Clark, J. B., Darley-Usmar, V. M., Smith, D. R., Stone, D., Reoxygenation-dependent decrease in mitochondrial NADH:CoQ reductase (Complex I) activity in the hypoxic/reoxygenated rat heart. Biochem. J. 1991, 274, 133–137.
  • 94
    White, M. Y., Cordwell, S. J., McCarron, H. C., Prasan, A. M. et al., Proteomics of ischemia/reperfusion injury in rabbit myocardium reveals alterations to proteins of essential functional systems. Proteomics 2005, 5, 1395–1410.
    Direct Link:
  • 95
    Zhang, Y., Marcillat, O., Giulivi, C., Ernster, L., Davies, K. J., The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J. Biol. Chem. 1990, 265, 16330–16336.
  • 96
    Malis, C. D., Bonventre, J. V., Mechanism of calcium potentiation of oxygen free radical injury to renal mitochondria. A model for post-ischemic and toxic mitochondrial damage. J. Biol. Chem. 1986, 261, 14201–14208.
  • 97
    Borutaite, V., Budriunaite, A., Brown, G. C., Reversal of nitric oxide-, peroxynitrite- and S-nitrosothiol-induced inhibition of mitochondrial respiration or complex I activity by light and thiols. Biochim. Biophys. Acta 2000, 1459, 405–412.
  • 98
    Murray, J., Taylor, S. W., Zhang, B., Ghosh, S. S., Capaldi, R. A., Oxidative damage to mitochondrial complex I due to peroxynitrite: identification of reactive tyrosines by mass spectrometry. J. Biol. Chem. 2003, 278, 37223–37230.
  • 99
    Paradies, G., Petrosillo, G., Pistolese, M., Ruggiero, F. M., Reactive oxygen species affect mitochondrial electron transport complex I activity through oxidative cardiolipin damage. Gene 2002, 286, 135–141.
  • 100
    Taylor, S. W., Fahy, E., Murray, J., Capaldi, R. A., Ghosh, S. S., Oxidative post-translational modification of tryptophan residues in cardiac mitochondrial proteins. J. Biol. Chem. 2003, 278, 19587–19590.
  • 101
    Jekabsone, A., Ivanoviene, L., Brown, G. C., Borutaite, V., Nitric oxide and calcium together inactivate mitochondrial complex I and induce cytochrome c release. J. Mol. Cell. Cardiol. 2003, 35, 803–809.
  • 102
    Sadek, H. A., Szweda, P. A., Szweda, L. I., Modulation of mitochondrial complex I activity by reversible Ca 2+ and NADH mediated superoxide anion dependent inhibition. Biochemistry 2004, 43, 8494–8502.
  • 103
    Pocsfalvi, G., Cuccurullo, M., Schlosser, G., Cacace, G. et al., Shotgun proteomics for the characterization of subunit composition of mitochondrial complex I. Biochim. Biophys. Acta 2006, 1757, 1438–1450.
  • 104
    Carroll, J., Fearnley, I. M., Shannon, R. J., Hirst, J., Walker, J. E., Analysis of the subunit composition of complex I from bovine heart mitochondria. Mol. Cell. Proteomics 2003, 2, 117–126.
  • 105
    Fearnley, I. M., Carroll, J., Walker, J. E., Proteomic analysis of the subunit composition of complex I (NADH:ubiquinone oxidoreductase) from bovine heart mitochondria. Methods Mol. Biol. 2007, 357, 103–125.
  • 106
    Tompkins, A. J., Burwell, L. S., Digerness, S. B., Zaragoza, C. et al., Mitochondrial dysfunction in cardiac ischemia-reperfusion injury: ROS from complex I, without inhibition. Biochim. Biophys. Acta 2006, 1762, 223–231.
  • 107
    Robinson, N. C., Functional binding of cardiolipin to cytochrome c oxidase. J. Bioenerg. Biomembr. 1993, 25, 153–163.
  • 108
    De Windt, L. J., Reneman, R. S., Van der Vusse, G. J., Van Bilsen, M., Phospholipase A2-mediated hydrolysis of cardiac phospholipids: the use of molecular and transgenic techniques. Mol. Cell. Biochem. 1998, 180, 65–73.
  • 109
    Paradies, G., Ruggiero, F. M., Petrosillo, G., Quagliariello, E., Peroxidative damage to cardiac mitochondria: cytochrome oxidase and cardiolipin alterations. FEBS Lett. 1998, 424, 155–158.
  • 110
    Paradies, G., Petrosillo, G., Pistolese, M., Di Venosa, N. et al., Lipid peroxidation and alterations to oxidative metabolism in mitochondria isolated from rat heart subjected to ischemia and reperfusion. Free Radic. Biol. Med. 1999, 27, 42–50.
  • 111
    Lesnefsky, E. J., Slabe, T. J., Stoll, M. S., Minkler, P. E., Hoppel, C. L., Myocardial ischemia selectively depletes cardiolipin in rabbit heart subsarcolemmal mitochondria. Am. J. Physiol. Heart Circ. Physiol. 2001, 280, H2770–H2778.
  • 112
    Paradies, G., Petrosillo, G., Pistolese, M., Ruggiero, F. M., The effect of reactive oxygen species generated from the mitochondrial electron transport chain on the cytochrome c oxidase activity and on the cardiolipin content in bovine heart submitochondrial particles. FEBS Lett. 2000, 466, 323–326.
  • 113
    Chen, J., Henderson, G. I., Freeman, G. L., Role of 4-hydroxynonenal in modification of cytochrome c oxidase in ischemia/reperfused rat heart. J. Mol. Cell. Cardiol. 2001, 33, 1919–1927.
  • 114
    Adibhatla, R. M., Hatcher, J. F., Dempsey, R. J., Phospholipase A2, hydroxyl radicals, and lipid peroxidation in transient cerebral ischemia. Antioxid. Redox Signal. 2003, 5, 647–654.
  • 115
    McLean, L. R., Hagaman, K. A., Davidson, W. S., Role of lipid structure in the activation of phospholipase A2 by peroxidized phospholipids. Lipids 1993, 28, 505–509.
  • 116
    Chicco, A. J., Sparagna, G. C., Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am. J. Physiol., Cell Physiol. 2007, 292, C33–44.
  • 117
    Schlame, M., Rua, D., Greenberg, M. L., The biosynthesis and functional role of cardiolipin. Prog. Lipid Res. 2000, 39, 257–288.
  • 118
    Hoch, F. L., Cardiolipins and biomembrane function. Biochim. Biophys. Acta 1992, 1113, 71–133.
  • 119
    Mileykovskaya, E., Zhang, M., Dowhan, W., Cardiolipin in energy transducing membranes. Biochemistry (Mosc) 2005, 70, 154–158.
  • 120
    Benderdour, M., Charron, G., DeBlois, D., Comte, B., Des Rosiers, C., Cardiac mitochondrial NADP+-isocitrate dehydrogenase is inactivated through 4-hydroxynonenal adduct formation: an event that precedes hypertrophy development. J. Biol. Chem. 2003, 278, 45154–45159.
  • 121
    Benderdour, M., Charron, G., Comte, B., Ayoub, R. et al., Decreased cardiac mitochondrial NADP+-isocitrate dehydrogenase activity and expression: a marker of oxidative stress in hypertrophy development. Am. J. Physiol. Heart Circ. Physiol. 2004, 287, H2122–2131.
  • 122
    Baines, C. P., Cohen, M. V., Downey, J. M., Signal transduction in ischemic preconditioning: the role of kinases and mitochondrial K(ATP) channels. J. Cardiovasc. Electrophysiol. 1999, 10, 741–754.
    Direct Link:
  • 123
    Halestrap, A. P., Clarke, S. J., Khaliulin, I., The role of mitochondria in protection of the heart by preconditioning. Biochim. Biophys. Acta 2007, 1767, 1007–1031.
  • 124
    Seddon, M., Looi, Y. H., Shah, A. M., Oxidative stress and redox signaling in cardiac hypertrophy and heart failure. Heart 2007, 93, 903–907.
  • 125
    Barford, D., The role of cysteine residues as redox-sensitive regulatory switches. Curr. Opin. Struct. Biol. 2004, 14, 679–686.
  • 126
    Salmeen, A., Andersen, J. N., Myers, M. P., Meng, T. C. et al., Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 2003, 423, 769–773.
  • 127
    van Montfort, R. L., Congreve, M., Tisi, D., Carr, R., Jhoti, H., Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 2003, 423, 773–777.
  • 128
    Takeishi, Y., Jalili, T., Ball, N. A., Walsh, R. A., Responses of cardiac protein kinase C isoforms to distinct pathological stimuli are differentially regulated. Circ. Res. 1999, 85, 264–271.
  • 129
    Murriel, C. L., Mochly-Rosen, D., Opposing roles of delta and epsilonPKC in cardiac ischemia and reperfusion: targeting the apoptotic machinery. Arch. Biochem. Biophys. 2003, 420, 246–254.
  • 130
    Baines, C. P., Goto, M., Downey, J. M., Oxygen radicals released during ischemic preconditioning contribute to cardioprotection in the rabbit myocardium. J. Mol. Cell. Cardiol. 1997, 29, 207–216.
  • 131
    Forbes, R. A., Steenbergen, C., Murphy, E., Diazoxide-induced cardioprotection requires signaling through a redox-sensitive mechanism. Circ. Res. 2001, 88, 802–809.
  • 132
    Oldenburg, O., Qin, Q., Krieg, T., Yang, X. M. et al., Bradykinin induces mitochondrial ROS generation via NO, cGMP, PKG, and mitoKATP channel opening and leads to cardioprotection. Am. J. Physiol. Heart Circ. Physiol. 2004, 286, H468–H476.
  • 133
    Yao, Z., Tong, J., Tan, X., Li, C. et al., Role of reactive oxygen species in acetylcholine-induced preconditioning in cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 1999, 277, H2504–H2509.
  • 134
    Penna, C., Cappello, S., Mancardi, D., Raimondo, S. et al., 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. 2006, 101, 168–179.
  • 135
    Sabri, A., Steinberg, S. F., Protein kinase C isoform-selective signals that lead to cardiac hypertrophy and the progression of heart failure. Mol. Cell. Biochem. 2003, 251, 97–101.
  • 136
    Ping, P., Zhang, J., Qiu, Y., Tang, X. L. et al., Ischemic preconditioning induces selective translocation of protein kinase C isoforms epsilon and eta in the heart of conscious rabbits without subcellular redistribution of total protein kinase C activity. Circ. Res. 1997, 81, 404–414.
  • 137
    Ping, P., Zhang, J., Cao, X., Li, R. C. et al., PKC-dependent activation of p44/p42 MAPKs during myocardial ischemia-reperfusion in conscious rabbits. Am. J. Physiol. Heart Circ. Physiol. 1999, 276, H1468–H1481.
  • 138
    Ping, P., Song, C., Zhang, J., Guo, Y. et al., Formation of protein kinase C(epsilon)-Lck signaling modules confers cardioprotection. J. Clin. Invest. 2002, 109, 499–507.
  • 139
    Ping, P., Zhang, J., Pierce, W. M., Jr., Bolli, R., Functional proteomic analysis of protein kinase C epsilon signaling complexes in the normal heart and during cardioprotection. Circ. Res. 2001, 88, 59–62.
  • 140
    Pain, T., Yang, X. M., Critz, S. D., Yue, Y. et al., Opening of mitochondrial K(ATP) channels triggers the preconditioned state by generating free radicals. Circ. Res. 2000, 87, 460–466.
  • 141
    Budas, G. R., Jovanovic, S., Crawford, R. M., Jovanovic, A., Hypoxia-induced preconditioning in adult stimulated cardiomyocytes is mediated by the opening and trafficking of sarcolemmal KATP channels. FASEB J. 2004, 18, 1046–1048.
  • 142
    Gross, G. J., Fryer, R. M., Sarcolemmal versus mitochondrial ATP-sensitive K+ channels and myocardial preconditioning. Circ. Res. 1999, 84, 973–979.
  • 143
    Gross, G. J., Peart, J. N., KATP channels and myocardial preconditioning: an update. Am. J. Physiol. Heart Circ. Physiol. 2003, 285, H921–H930.
  • 144
    Obal, D., Dettwiler, S., Favoccia, C., Scharbatke, H. et al., The influence of mitochondrial KATP-channels in the cardioprotection of preconditioning and postconditioning by sevoflurane in the rat in vivo. Anesth. Analg. 2005, 101, 1252–1260.
  • 145
    Holmuhamedov, E. L., Wang, L., Terzic, A., ATP-sensitive K+ channel openers prevent Ca2+ overload in rat cardiac mitochondria. J. Physiol. 1999, 519, 347–360.
    Direct Link:
  • 146
    Dos Santos, P., Kowaltowski, A. J., Laclau, M. N., Seetharaman, S. et al., Mechanisms by which opening the mitochondrial ATP- sensitive K(+) channel protects the ischemic heart. Am. J. Physiol. Heart Circ. Physiol. 2002, 283, H284–H295.
  • 147
    O'Rourke, B., Evidence for mitochondrial K+ channels and their role in cardioprotection. Circ. Res. 2004, 94, 420–432.
  • 148
    Vanden Hoek, T., Becker, L. B., Shao, Z. H., Li, C. Q., Schumacker, P. T., Preconditioning in cardiomyocytes protects by attenuating oxidant stress at reperfusion. Circ. Res. 2000, 86, 541–548.
  • 149
    Jaburek, M., Costa, A. D., Burton, J. R., Costa, C. L., Garlid, K. D., Mitochondrial PKC epsilon and mitochondrial ATP-sensitive K+ channel copurify and coreconstitute to form a functioning signaling module in proteoliposomes. Circ. Res. 2006, 99, 878–883.
  • 150
    Hu, K., Huang, C. S., Jan, Y. N., Jan, L. Y., ATP-sensitive potassium channel traffic regulation by adenosine and protein kinase C. Neuron 2003, 38, 417–432.
  • 151
    Garlid, K. D., Paucek, P., Mitochondrial potassium transport: the K(+) cycle. Biochim. Biophys. Acta 2003, 1606, 23–41.
  • 152
    Ferranti, R., da Silva, M. M., Kowaltowski, A. J., Mitochondrial ATP-sensitive K+ channel opening decreases reactive oxygen species generation. FEBS Lett. 2003, 536, 51–55.
  • 153
    Layland, J., Solaro, R. J., Shah, A. M., Regulation of cardiac contractile function by troponin I phosphorylation. Cardiovasc. Res. 2005, 66, 12–21.
  • 154
    Goldspink, P. H., Montgomery, D. E., Walker, L. A., Urboniene, D. et al., Protein kinase Cepsilon overexpression alters myofilament properties and composition during the progression of heart failure. Circ. Res. 2004, 95, 424–432.
  • 155
    Robinson, N. E., Robinson, A. B., Deamidation of human proteins. Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 12409–12413.
  • 156
    Robinson, N. E., Robinson, A. B., Molecular clocks. Proc. Natl. Acad. Sci. USA 2001, 98, 944–949.
  • 157
    Robinson, N. E., Protein deamidation. Proc. Natl. Acad. Sci. USA 2002, 99, 5283–5288.
  • 158
    Van Kleef, S. M., Willems-Thijssen, W., Hoenders, H. J., Intracellular degradation and deamidation of alpha-crystalline subunits. Eur. J. Biochem. 1976, 66, 477–483.
    Direct Link:
  • 159
    Groenen, P. J., van Dongen, M. J., Voorter, C. E., Bloemendal, H., de Jong, W. W., Age-dependent deamidation of alpha B-crystalline. FEBS Lett. 1993, 322, 69–72.
  • 160
    White, M. Y., Hambly, B. D., Jeremy, R. W., Cordwell, S. J., Ischemia-specific phosphorylation and myofilament translocation of heat shock protein 27 precedes alpha B-crystalline and occurs independently of reactive oxygen species in rabbit myocardium. J. Mol. Cell. Cardiol. 2006, 40, 761–774.
  • 161
    Sarioglu, H., Lottspeich, F., Walk, T., Jung, G., Eckerskorn, C., Deamidation as a widespread phenomenon in two-dimensional polyacrylamide gel electrophoresis of human blood plasma proteins. Electrophoresis 2000, 21, 2209–2218.
    Direct Link:
  • 162
    Wright, H. T., Sequence and structure determinants of the nonenzymatic deamidation of asparagine and glutamine residues in proteins. Protein Eng. 1991, 4, 283–294.
  • 163
    Walker, J. E., Fearnley, I. M., Gay, N. J., Gibson, B. W. et al., Primary structure and subunit stoichiometry of F1-ATPase from bovine mitochondria. J. Mol. Biol. 1985, 184, 677–701.
  • 164
    Gottlieb, R. A., Burleson, K. O., Kloner, R. A., Babior, B. M., Engler, R. L., Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J. Clin. Invest. 1994, 94, 1621–1628.
  • 165
    Olivetti, G., Quaini, F., Sala, R., Lagrasta, C. et al., Acute myocardial infarction in humans is associated with activation of programmed myocyte cell death in the surviving portion of the heart. J. Mol. Cell. Cardiol. 1996, 28, 2005–2016.
  • 166
    Narula, J., Pandey, P., Arbustini, E., Haider, N. et al., Apoptosis in heart failure: release of cytochrome c from mitochondria and activation of caspase-3 in human cardiomyopathy. Proc. Natl. Acad. Sci. USA 1999, 96, 8144–8149.
  • 167
    Steenbergen, C., Afshari, C. A., Petranka, J. G., Collins, J. et al., Alterations in apoptotic signaling in human idiopathic cardiomyopathic hearts in failure. Am. J. Physiol. Heart Circ. Physiol. 2003, 284, H268–276.
  • 168
    Guerra, S., Leri, A., Wang, X., Finato, N. et al., Myocyte death in the failing human heart is gender dependent. Circ. Res. 1999, 85, 856–866.
  • 169
    Eskes, R., Antonsson, B., Osen-Sand, A., Montessuit, S. et al., Bax-induced cytochrome C release from mitochondria is independent of the permeability transition pore but highly dependent on Mg 2+ ions. J. Cell Biol. 1998, 143, 217–224.
  • 170
    Finucane, D. M., Bossy-Wetzel, E., Waterhouse, N. J., Cotter, T. G., Green, D. R., Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xL. J. Biol. Chem. 1999, 274, 2225–2233.
  • 171
    Jürgensmeier, J. M., Xie, Z., Deveraux, Q., Ellerby, L. et al., Bax directly induces release of cytochrome c from isolated mitochondria. Proc. Natl. Acad. Sci. USA 1998, 95, 4997–5002.
  • 172
    Marzo, I., Brenner, C., Zamzami, N., Jurgensmeier, J. M. et al., Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 1998, 281, 2027–2031.
  • 173
    Narita, M., Shimizu, S., Ito, T., Chittenden, T. et al., Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc. Natl. Acad. Sci. USA 1998, 95, 14681–14686.
  • 174
    Pastorino, J. G., Tafani, M., Rothman, R. J., Marcinkeviciute, A. et al., Functional consequences of the sustained or transient activation by Bax of the mitochondrial permeability transition pore. J. Biol. Chem. 1999, 274, 31734–31739.
  • 175
    Shimizu, S., Tsujimoto, Y., Proapoptotic BH3-only Bcl-2 family members induce cytochrome c release, but not mitochondrial membrane potential loss, and do not directly modulate voltage-dependent anion channel activity. Proc. Natl. Acad. Sci. USA 2000, 97, 577–582.
  • 176
    Guo, Y., Srinivasula, S. M., Druilhe, A., Fernandes-Alnemri, T., Alnemri, E. S., Caspase-2 induces apoptosis by releasing proapoptotic proteins from mitochondria. J. Biol. Chem. 2002, 277, 13430–13437.
  • 177
    Jugdutt, B. I., Idikio, H. A., Apoptosis and oncosis in acute coronary syndromes: assessment and implications. Mol. Cell. Biochem. 2005, 270, 177–200.
  • 178
    Cheng, E. H., Kirsch, D. G., Clem, R. J., Ravi, R. et al., Conversion of Bcl-2 to a Bax-like death effector by caspases. Science 1997, 278, 1966–1968.
  • 179
    Clem, R. J., Cheng, E. H., Karp, C. L., Kirsch, D. G. et al., Modulation of cell death by Bcl-XL through caspase interaction. Proc. Natl. Acad. Sci. USA 1998, 95, 554–559.
  • 180
    Heiskanen, K. M., Bhat, M. B., Wang, H. W., Ma, J., Nieminen, A. L., Mitochondrial depolarization accompanies cytochrome c release during apoptosis in PC6 cells. J. Biol. Chem. 1999, 274, 5654–5658.
  • 181
    Argaud, L., Gateau-Roesch, O., Raisky, O., Loufouat, J. et al., Postconditioning inhibits mitochondrial permeability transition. Circulation 2005, 111, 194–197.
  • 182
    Crompton, M., The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 1999, 341, 233–249.
  • 183
    Crompton, M., Costi, A., Hayat, L., Evidence for the presence of a reversible Ca2+-dependent pore activated by oxidative stress in heart mitochondria. Biochem. J. 1987, 245, 915–918.
  • 184
    Hunter, D. R., Haworth, R. A., The Ca2+-induced membrane transition in mitochondria. III. Transitional Ca 2+ release. Arch. Biochem. Biophys. 1979, 195, 468–477.
  • 185
    Akao, M., O'Rourke, B., Teshima, Y., Seharaseyon, J., Marban, E., Mechanistically distinct steps in the mitochondrial death pathway triggered by oxidative stress in cardiac myocytes. Circ. Res. 2003, 92, 186–194.
  • 186
    Baines, C. P., Kaiser, R. A., Purcell, N. H., Blair, N. S. et al., Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005, 434, 658–662.
  • 187
    Baines, C. P., Kaiser, R. A., Sheiko, T., Craigen, W. J., Molkentin, J. D., Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat. Cell Biol. 2007, 9, 550–555.
  • 188
    Lochner, A., Genade, S., Tromp, E., Podzuweit, T., Moolman, J. A., Ischemic preconditioning and the beta-adrenergic signal transduction pathway. Circulation 1999, 100, 958–966.
  • 189
    Sanada, S., Asanuma, H., Tsukamoto, O., Minamino, T. et al., Protein kinase A as another mediator of ischemic preconditioning independent of protein kinase C. Circulation 2004, 110, 51–57.
  • 190
    Marks, A. R., Cardiac intracellular calcium release channels: role in heart failure. Circ. Res. 2000, 87, 8–11.
  • 191
    Reiken, S., Gaburjakova, M., Guatimosim, S., Gomez, A. M. et al., Protein kinase A phosphorylation of the cardiac calcium release channel (ryanodine receptor) in normal and failing hearts. Role of phosphatases and response to isoproterenol. J. Biol. Chem. 2003, 278, 444–453.
  • 192
    Papa, S., Sardanelli, A. M., Scacco, S., Technikova-Dobrova, Z., cAMP-dependent protein kinase and phosphoproteins in mammalian mitochondria. An extension of the cAMP-mediated intracellular signal transduction. FEBS Lett. 1999, 444, 245–249.
  • 193
    Pawson, T., Scott, J. D., Signaling through scaffold, anchoring, and adaptor proteins. Science 1997, 278, 2075–2080.
  • 194
    Burgess, J. W., Yamada, E. W., cAMP-dependent protein kinase isozymes with preference for histone H2B as substrate in mitochondria of bovine heart. Biochem. Cell Biol. 1987, 65, 137–143.
  • 195
    Papa, S., Sardanelli, A. M., Cocco, T., Speranza, F. et al., The nuclear-encoded 18 kDa (IP) AQDQ subunit of bovine heart complex I is phosphorylated by the mitochondrial cAMP-dependent protein kinase. FEBS Lett. 1996, 379, 299–301.
  • 196
    Sardanelli, A. M., Technikova-Dobrova, Z., Scacco, S. C., Speranza, F., Papa, S., Characterization of proteins phosphorylated by the cAMP-dependent protein kinase of bovine heart mitochondria. FEBS Lett. 1995, 377, 470–474.
  • 197
    Technikova-Dobrova, Z., Sardanelli, A. M., Papa, S., Phosphorylation of mitochondrial proteins in bovine heart. Characterization of kinases and substrates. FEBS Lett. 1993, 322, 51–55.
  • 198
    Technikova-Dobrova, Z., Sardanelli, A. M., Stanca, M. R., Papa, S., cAMP-dependent protein phosphorylation in mitochondria of bovine heart. FEBS Lett. 1994, 350, 187–191.
  • 199
    Sardanelli, A. M., Technikova-Dobrova, Z., Speranza, F., Mazzocca, A. et al., Topology of the mitochondrial cAMP-dependent protein kinase and its substrates. FEBS Lett. 1996, 396, 276–278.
  • 200
    Larsen, M. R., Thingholm, T. E., Jensen, O. N., Roepstorff, P., Jorgensen, T. J., Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell. Proteomics 2005, 4, 873–886.
  • 201
    Palmisano, G., Sardanelli, A. M., Signorile, A., Papa, S., Larsen, M. R., The phosphorylation pattern of bovine heart complex I subunits. Proteomics 2007, 7, 1575–1583.
    Direct Link:
  • 202
    Pocsfalvi, G., Cuccurullo, M., Schlosser, G., Scacco, S. et al., Phosphorylation of B14.5a subunit from bovine heart complex I identified by titanium dioxide selective enrichment and shotgun proteomics. Mol. Cell. Proteomics 2007, 6, 231–237.
  • 203
    Chang, C. R., Blackstone, C., Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology. J. Biol. Chem. 2007, 282, 21583–21587.
  • 204
    Chan, D. C., Mitochondria: dynamic organelles in disease, aging, and development. Cell 2006, 125, 1241–1252.
  • 205
    Chan, D. C., Mitochondrial dynamics in disease. N. Engl. J. Med. 2007, 356, 1707–1709.
  • 206
    Matsumoto-Ida, M., Akao, M., Takeda, T., Kato, M., Kita, T., Real-time 2-photon imaging of mitochondrial function in perfused rat hearts subjected to ischemia/reperfusion. Circulation 2006, 114, 1497–1503.
  • 207
    Kuznetsov, A. V., Usson, Y., Leverve, X., Margreiter, R., Subcellular heterogeneity of mitochondrial function and dysfunction: evidence obtained by confocal imaging. Mol. Cell. Biochem. 2004, 256-257, 359–365.
  • 208
    Kuznetsov, A. V., Troppmair, J., Sucher, R., Hermann, M. et al., Mitochondrial subpopulations and heterogeneity revealed by confocal imaging: possible physiological role? Biochim. Biophys. Acta 2006, 1757, 686–691.
  • 209
    Murry, C. E., Richard, V. J., Reimer, K. A., Jennings, R. B., Ischemic preconditioning slows energy metabolism and delays ultrastructural damage during a sustained ischemic episode. Circ. Res. 1990, 66, 913–931.
  • 210
    Mannella, C. A., The relevance of mitochondrial membrane topology to mitochondrial function. Biochim. Biophys. Acta 2006, 1762, 140–147.
  • 211
    Hackenbrock, C. R., Ultrastructural bases for metabolically linked mechanical activity in mitochondria. I. Reversible ultrastructural changes with change in metabolic steady state in isolated liver mitochondria. J. Cell Biol. 1966, 30, 269–297.
  • 212
    Skulachev, V. P., Mitochondrial filaments and clusters as intracellular power-transmitting cables. Trends Biochem. Sci. 2001, 26, 23–29.
  • 213
    Kuznetsov, A. V., Schneeberger, S., Renz, O., Meusburger, H. et al., Functional heterogeneity of mitochondria after cardiac cold ischemia and reperfusion revealed by confocal imaging. Transplantation 2004, 77, 754–756.
  • 214
    Lesnefsky, E. J., Tandler, B., Ye, J., Slabe, T. J. et al., Myocardial ischemia decreases oxidative phosphorylation through cytochrome oxidase in subsarcolemmal mitochondria. Am. J. Physiol. Heart Circ. Physiol. 1997, 273, H1544–H1554.
  • 215
    Akar, F. G., Aon, M. A., Tomaselli, G. F., O'Rourke, B., The mitochondrial origin of postischemic arrhythmias. J. Clin. Invest. 2005, 115, 3527–3535.
  • 216
    Aon, M. A., Cortassa, S., Akar, F. G., O'Rourke, B., Mitochondrial criticality: a new concept at the turning point of life or death. Biochim. Biophys. Acta 2006, 1762, 232–240.
  • 217
    Anmann, T., Guzun, R., Beraud, N., Pelloux, S. et al., Different kinetics of the regulation of respiration in permeabilized cardiomyocytes and in HL-1 cardiac cells. Importance of cell structure/organization for respiration regulation. Biochim. Biophys. Acta 2006, 1757, 1597–1606.
  • 218
    Chan, D. C., Mitochondrial fusion and fission in mammals. Annu. Rev. Cell Dev. Biol. 2006, 22, 79–99.
  • 219
    Rojo, M., Legros, F., Chateau, D., Lombes, A., Membrane topology and mitochondrial targeting of mitofusins, ubiquitous mammalian homologs of the transmembrane GTPase Fzo. J. Cell. Sci. 2002, 115, 1663–1674.
  • 220
    Santel, A., Fuller, M. T., Control of mitochondrial morphology by a human mitofusin. J. Cell. Sci. 2001, 114, 867–874.
  • 221
    Smirnova, E., Griparic, L., Shurland, D. L., van der Bliek, A. M., Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 2001, 12, 2245–2256.
  • 222
    Caprioli, R. M., Farmer, T. B., Gile, J., Molecular imaging of biological samples: localization of peptides and proteins using MALDI-TOF MS. Anal. Chem. 1997, 69, 4751–4760.
  • 223
    Stoeckli, M., Chaurand, P., Hallahan, D. E., Caprioli, R. M., Imaging mass spectrometry: a new technology for the analysis of protein expression in mammalian tissues. Nat. Med. 2001, 7, 493–496.
  • 224
    Lemaire, R., Desmons, A., Tabet, J. C., Day, R. et al., Direct analysis and MALDI imaging of formalin-fixed, paraffin-embedded tissue sections. J. Proteome Res. 2007, 6, 1295–1305.
  • 225
    Chaurand, P., Stoeckli, M., Caprioli, R. M., Direct profiling of proteins in biological tissue sections by MALDI mass spectrometry. Anal. Chem. 1999, 71, 5263–5270.
  • 226
    Caldwell, R. L., Caprioli, R. M., Tissue profiling by mass spectrometry: a review of methodology and applications. Mol. Cell. Proteomics 2005, 4, 394–401.
  • 227
    Lemaire, R., Menguellet, S. A., Stauber, J., Marchaudon, V. et al., Specific MALDI Imaging and Profiling for Biomarker Hunting and Validation: Fragment of the 11S Proteasome Activator Complex, Reg Alpha Fragment, Is a New Potential Ovary Cancer Biomarker. J. Proteome Res. 2007, 6, 4127–4134.
  • 228
    Zheng, Y., Xu, Y., Ye, B., Lei, J. et al., Prostate carcinoma tissue proteomics for biomarker discovery. Cancer 2003, 98, 2576–2582.
    Direct Link:
  • 229
    Drexler, D. M., Garrett, T. J., Cantone, J. L., Diters, R. W. et al., Utility of imaging mass spectrometry (IMS) by matrix-assisted laser desorption ionization (MALDI) on an ion trap mass spectrometer in the analysis of drugs and metabolites in biological tissues. J. Pharmacol. Toxicol. Methods 2007, 55, 279–288.
  • 230
    Uhlen, M., Ponten, F., Antibody-based proteomics for human tissue profiling. Mol. Cell. Proteomics 2005, 4, 384–393.
  • 231
    Bengtsson, S., Krogh, M., Szigyarto, C. A., Uhlen, M. et al., Large-scale proteomics analysis of human ovarian cancer for biomarkers. J. Proteome Res. 2007, 6, 1440–1450.
Get PDF (355K)