Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015, Article ID 891707, 12 pages
http://dx.doi.org/10.1155/2015/891707
Review Article

The Role of Cardiolipin in Cardiovascular Health

1Department of Biological Sciences, Wayne State University, Detroit, MI 48202, USA
2Department of Biochemistry, The University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390-9038, USA

Received 21 May 2015; Accepted 8 July 2015

Academic Editor: Emanuele Marzetti

Copyright © 2015 Zheni Shen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. H. De Bruijn, “Chemical structure and serological activity of natural and synthetic cardiolipin and related compounds,” British Journal of Venereal Diseases, vol. 42, no. 2, pp. 125–128, 1966. View at Google Scholar · View at Scopus
  2. M. Schlame, S. Brody, and K. Y. Hostetler, “Mitochondrial cardiolipin in diverse eukaryotes,” European Journal of Biochemistry, vol. 212, no. 3, pp. 727–733, 1993. View at Publisher · View at Google Scholar · View at Scopus
  3. A. S. Joshi, J. Zhou, V. M. Gohil, S. Chen, and M. L. Greenberg, “Cellular functions of cardiolipin in yeast,” Biochimica et Biophysica Acta, vol. 1793, no. 1, pp. 212–218, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. Q. Zhong, J. Gvozdenovic-Jeremic, P. Webster, J. Zhou, and M. L. Greenberg, “Loss of function of KRE5 suppresses temperature sensitivity of mutants lacking mitochondrial anionic lipids,” Molecular Biology of the Cell, vol. 16, no. 2, pp. 665–675, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Chen, M. Tarsio, P. M. Kane, and M. L. Greenberg, “Cardiolipin mediates cross-talk between mitochondria and the vacuole,” Molecular Biology of the Cell, vol. 19, no. 12, pp. 5047–5058, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. J. Zhou, Q. Zhong, G. Li, and M. L. Greenberg, “Loss of cardiolipin leads to longevity defects that are alleviated by alterations in stress response signaling,” The Journal of Biological Chemistry, vol. 284, no. 27, pp. 18106–18114, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Chen, D. Liu, R. L. Finley Jr., and M. L. Greenberg, “Loss of mitochondrial DNA in the yeast cardiolipin synthase crd1 mutant leads to up-regulation of the protein kinase Swe1p that regulates the G2/M transition,” The Journal of Biological Chemistry, vol. 285, no. 14, pp. 10397–10407, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. X.-X. Li, B. Tsoi, Y.-F. Li, H. Kurihara, and R.-R. He, “Cardiolipin and its different properties in mitophagy and apoptosis,” Journal of Histochemistry & Cytochemistry, vol. 63, no. 5, pp. 301–311, 2015. View at Publisher · View at Google Scholar
  9. K. Y. Hostetler, H. van den Bosch, and L. L. M. van Deenen, “The mechanism of cardiolipin biosynthesis in liver mitochondria,” Biochimica et Biophysica Acta, vol. 260, no. 3, pp. 507–513, 1972. View at Publisher · View at Google Scholar · View at Scopus
  10. H.-F. Tian, J.-M. Feng, and J.-F. Wen, “The evolution of cardiolipin biosynthesis and maturation pathways and its implications for the evolution of eukaryotes,” BMC Evolutionary Biology, vol. 12, no. 1, article 32, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. Y. Tamura, Y. Harada, S.-I. Nishikawa et al., “Tam41 is a CDP-diacylglycerol synthase required for cardiolipin biosynthesis in mitochondria,” Cell Metabolism, vol. 17, no. 5, pp. 709–718, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Kutik, M. Rissler, X. L. Guan et al., “The translocator maintenance protein Tam41 is required for mitochondrial cardiolipin biosynthesis,” Journal of Cell Biology, vol. 183, no. 7, pp. 1213–1221, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. M. R. Steiner and R. L. Lester, “In vitro studies of phospholipid biosynthesis in Saccharomyces cerevisiae,” Biochimica et Biophysica Acta (BBA)—Lipids and Lipid Metabolism, vol. 260, no. 2, pp. 222–243, 1972. View at Publisher · View at Google Scholar · View at Scopus
  14. S.-C. Chang, P. N. Heacock, C. J. Clancey, and W. Dowhan, “The PEL1 gene (renamed PGS1) encodes the phosphatidylglycerophosphate synthase of Saccharomyces cerevisiae,” The Journal of Biological Chemistry, vol. 273, no. 16, pp. 9829–9836, 1998. View at Publisher · View at Google Scholar · View at Scopus
  15. T. Hirabayashi, T. J. Larson, and W. Dowhan, “Membrane-associated phosphatidylglycerophosphate synthetase from Escherichia coli: purification by substrate affinity chromatography on cytidine 5′-Diphospho-1,2-diacyl-sn-glycerol sepharose,” Biochemistry, vol. 15, no. 24, pp. 5205–5211, 1976. View at Publisher · View at Google Scholar · View at Scopus
  16. H. van den Bosch, L. M. van Golde, and L. L. van Deenen, “Dynamics of phosphoglycerides,” Ergebnisse der Physiologie, vol. 13, pp. 13–145, 1972. View at Google Scholar · View at Scopus
  17. B. L. Kelly and M. L. Greenberg, “Characterization and regulation of phosphatidylglycerolphosphate phosphatase in Saccharomyces cerevisiae,” Biochimica et Biophysica Acta—Lipids and Lipid Metabolism, vol. 1046, no. 2, pp. 144–150, 1990. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Zhang, Z. Guan, A. N. Murphy et al., “Mitochondrial phosphatase PTPMT1 is essential for cardiolipin biosynthesis,” Cell Metabolism, vol. 13, no. 6, pp. 690–700, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Xiao, J. L. Engel, J. Zhang, M. J. Chen, G. Manning, and J. E. Dixon, “Structural and functional analysis of PTPMT1, a phosphatase required for cardiolipin synthesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 29, pp. 11860–11865, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Osman, M. Haag, F. T. Wieland, B. Brügger, and T. Langer, “A mitochondrial phosphatase required for cardiolipin biosynthesis: the PGP phosphatase Gep4,” The EMBO Journal, vol. 29, no. 12, pp. 1976–1987, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. D. Chen, X.-Y. Zhang, and Y. Shi, “Identification and functional characterization of hCLS1, a human cardiolipin synthase localized in mitochondria,” Biochemical Journal, vol. 398, no. 2, pp. 169–176, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. B. Lu, F. Y. Xu, Y. J. Jiang et al., “Cloning and characterization of a cDNA encoding human cardiolipin synthase (hCLS1),” Journal of Lipid Research, vol. 47, no. 6, pp. 1140–1145, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. R. H. Houtkooper, H. Akbari, H. van Lenthe et al., “Identification and characterization of human cardiolipin synthase,” FEBS Letters, vol. 580, no. 13, pp. 3059–3064, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. G. Tuller, C. Hrastnik, G. Achleitner, U. Schiefthaler, F. Klein, and G. Daum, “YDL142c encodes cardiolipin synthase (Cls1p) and is non-essential for aerobic growth of Saccharomyces cerevisiae,” FEBS Letters, vol. 421, no. 1, pp. 15–18, 1998. View at Publisher · View at Google Scholar · View at Scopus
  25. F. Jiang, H. S. Rizavi, and M. L. Greenberg, “Cardiolipin is not essential for the growth of Saccharomyces cerevisiae on fermentable or non-fermentable carbon sources,” Molecular Microbiology, vol. 26, no. 3, pp. 481–491, 1997. View at Publisher · View at Google Scholar · View at Scopus
  26. S.-C. Chang, P. N. Heacock, E. Mileykovskaya, D. R. Voelker, and W. Dowhan, “Isolation and characterization of the gene (CLS1) encoding cardiolipin synthase in Saccharomyces cerevisiae,” Journal of Biological Chemistry, vol. 273, no. 24, pp. 14933–14941, 1998. View at Publisher · View at Google Scholar · View at Scopus
  27. H. van den Bosch, “Phosphoglyceride metabolism,” Annual Review of Biochemistry, vol. 43, pp. 243–277, 1974. View at Publisher · View at Google Scholar · View at Scopus
  28. C. Ye, Z. Shen, and M. L. Greenberg, “Cardiolipin remodeling: a regulatory hub for modulating cardiolipin metabolism and function,” Journal of Bioenergetics and Biomembranes, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. W. E. M. Lands, “Metabolism of glycerolipids. II. The enzymatic acylation of lysolecithin,” Journal of Biological Chemistry, vol. 235, no. 8, pp. 2233–2237, 1960. View at Google Scholar · View at Scopus
  30. A. Beranek, G. Rechberger, H. Knauer, H. Wolinski, S. D. Kohlwein, and R. Leber, “Identification of a cardiolipin-specific phospholipase encoded by the gene CLD1 (YGR110W) in yeast,” The Journal of Biological Chemistry, vol. 284, no. 17, pp. 11572–11578, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. A. G. Buckland, A. R. Kinkaid, and D. C. Wilton, “Cardiolipin hydrolysis by human phospholipases A2: the multiple enzymatic activities of human cytosolic phospholipase A2,” Biochimica et Biophysica Acta—Lipids and Lipid Metabolism, vol. 1390, no. 1, pp. 65–72, 1998. View at Publisher · View at Google Scholar · View at Scopus
  32. Y.-H. Hsu, D. S. Dumlao, J. Cao, and E. A. Dennis, “Assessing phospholipase A2 activity toward cardiolipin by mass spectrometry,” PLoS ONE, vol. 8, no. 3, Article ID e59267, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. E. A. Dennis, J. Cao, Y.-H. Hsu, V. Magrioti, and G. Kokotos, “Phospholipase A2 enzymes: physical structure, biological function, disease implication, chemical inhibition, and therapeutic intervention,” Chemical Reviews, vol. 111, no. 10, pp. 6130–6185, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Bione, P. D'Adamo, E. Maestrini, A. K. Gedeon, P. A. Bolhuis, and D. Toniolo, “A novel X-linked gene, G4.5. is responsible for Barth syndrome,” Nature Genetics, vol. 12, no. 4, pp. 385–389, 1996. View at Publisher · View at Google Scholar · View at Scopus
  35. Z. Gu, F. Valianpour, S. Chen et al., “Aberrant cardiolipin metabolism in the yeast taz1 mutant: a model for Barth syndrome,” Molecular Microbiology, vol. 51, no. 1, pp. 149–158, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. F. M. Vaz, R. H. Houtkooper, F. Valianpour, P. G. Barth, and R. J. A. Wanders, “Only one splice variant of the human TAZ gene encodes a functional protein with a role in cardiolipin metabolism,” Journal of Biological Chemistry, vol. 278, no. 44, pp. 43089–43094, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Cao, Y. Liu, J. Lockwood, P. Burn, and Y. Shi, “A novel cardiolipin-remodeling pathway revealed by a gene encoding an endoplasmic reticulum-associated acyl-CoA:lysocardiolipin acyltransferase (ALCAT1) in mouse,” The Journal of Biological Chemistry, vol. 279, no. 30, pp. 31727–31734, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. W. A. Taylor and G. M. Hatch, “Identification of the human mitochondrial linoleoyl-coenzyme a monolysocardiolipin acyltransferase (MLCL AT-1),” The Journal of Biological Chemistry, vol. 284, no. 44, pp. 30360–30371, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. Y. Xu, R. I. Kelley, T. J. J. Blanck, and M. Schlame, “Remodeling of cardiolipin by phospholipid transacylation,” Journal of Biological Chemistry, vol. 278, no. 51, pp. 51380–51385, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Yamashita, T. Sugiura, and K. Waku, “Acyltransferases and transacylases involved in fatty acid remodeling of phospholipids and metabolism of bioactive lipids in mammalian cells,” Journal of Biochemistry, vol. 122, no. 1, pp. 1–16, 1997. View at Publisher · View at Google Scholar · View at Scopus
  41. P. G. Barth, H. R. Scholte, J. A. Berden et al., “An X-linked mitochondrial disease affecting cardiac muscle, skeletal muscle and neutrophil leucocytes,” Journal of the Neurological Sciences, vol. 62, no. 1–3, pp. 327–355, 1983. View at Publisher · View at Google Scholar · View at Scopus
  42. P. G. Barth, R. J. A. Wanders, and P. Vreken, “X-linked cardioskeletal myopathy and neutropenia (Barth syndrome)—MIM 302060,” Journal of Pediatrics, vol. 135, no. 3, pp. 273–276, 1999. View at Publisher · View at Google Scholar · View at Scopus
  43. F. Valianpour, R. J. A. Wanders, H. Overmars et al., “Cardiolipin deficiency in X-linked cardioskeletal myopathy and neutropenia (Barth syndrome, MIM 302060): a study in cultured skin fibroblasts,” The Journal of Pediatrics, vol. 141, no. 5, pp. 729–733, 2002. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Schlame, J. A. Towbin, P. M. Heerdt, R. Jehle, S. DiMauro, and T. J. J. Blanck, “Deficiency of tetralinoleoyl-cardiolipin in Barth syndrome,” Annals of Neurology, vol. 51, no. 5, pp. 634–637, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Schlame, R. I. Kelley, A. Feigenbaum et al., “Phospholipid abnormalities in children with Barth syndrome,” Journal of the American College of Cardiology, vol. 42, no. 11, pp. 1994–1999, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. R. Chen, T. Tsuji, F. Ichida et al., “Mutation analysis of the G4.5 gene in patients with isolated left ventricular noncompaction,” Molecular Genetics and Metabolism, vol. 77, no. 4, pp. 319–325, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. P. D'Adamo, L. Fassone, A. Gedeon et al., “The X-linked gene G4.5 is responsible for different infantile dilated cardiomyopathies,” American Journal of Human Genetics, vol. 61, no. 4, pp. 862–867, 1997. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Hijikata, K. Yura, O. Ohara, and M. Go, “Structural and functional analyses of Barth syndrome-causing mutations and alternative splicing in the tafazzin acyltransferase domain,” Meta Gene, vol. 4, pp. 92–106, 2015. View at Publisher · View at Google Scholar
  49. A. Bowron, J. Honeychurch, M. Williams et al., “Barth syndrome without tetralinoleoyl cardiolipin deficiency: a possible ameliorated phenotype,” Journal of Inherited Metabolic Disease, vol. 38, no. 2, pp. 279–286, 2015. View at Publisher · View at Google Scholar · View at Scopus
  50. S. M. Claypool, K. Whited, S. Srijumnong, X. Han, and C. M. Koehler, “Barth syndrome mutations that cause tafazzin complex lability,” Journal of Cell Biology, vol. 192, no. 3, pp. 447–462, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. R. H. Houtkooper and F. M. Vaz, “Cardiolipin, the heart of mitochondrial metabolism,” Cellular and Molecular Life Sciences, vol. 65, no. 16, pp. 2493–2506, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. H. Cheng, D. J. Mancuso, X. Jiang et al., “Shotgun lipidomics reveals the temporally dependent, highly diversified cardiolipin profile in the mammalian brain: temporally coordinated postnatal diversification of cardiolipin molecular species with neuronal remodeling,” Biochemistry, vol. 47, no. 21, pp. 5869–5880, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. M. G. Baile, M. Sathappa, Y.-W. Lu et al., “Unremodeled and remodeled cardiolipin are functionally indistinguishable in yeast,” The Journal of Biological Chemistry, vol. 289, no. 3, pp. 1768–1778, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. C. Ye, W. Lou, Y. Li et al., “Deletion of the Cardiolipin-specific Phospholipase Cld1 rescues growth and life span defects in the Tafazzin Mutant: implications for Barth Syndrome,” The Journal of Biological Chemistry, vol. 289, no. 6, pp. 3114–3125, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. D. G. Gardner and D. Shoback, Greenspan's Basic and Clinical Endocrinology, chapter 17, McGraw-Hill, New York, NY, USA, 9th edition, 2011.
  56. D. M. Nathan, “Long-term complications of diabetes mellitus,” The New England Journal of Medicine, vol. 328, no. 23, pp. 1676–1685, 1993. View at Publisher · View at Google Scholar · View at Scopus
  57. X. Han, D. R. Abendschein, J. G. Kelley, and R. W. Gross, “Diabetes-induced changes in specific lipid molecular species in rat myocardium,” Biochemical Journal, vol. 352, no. 1, pp. 79–89, 2000. View at Publisher · View at Google Scholar · View at Scopus
  58. X. Han, J. Yang, H. Cheng, K. Yang, D. R. Abendschein, and R. W. Gross, “Shotgun lipidomics identifies cardiolipin depletion in diabetic myocardium linking altered substrate utilization with mitochondrial dysfunction,” Biochemistry, vol. 44, no. 50, pp. 16684–16694, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. X. Han, J. Yang, K. Yang, Z. Zhongdan, D. R. Abendschein, and R. W. Gross, “Alterations in myocardial cardiolipin content and composition occur at the very earliest stages of diabetes: a shotgun lipidomics study,” Biochemistry, vol. 46, no. 21, pp. 6417–6428, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. H.-J. Pan, Y. Lin, Y. E. Chen, D. E. Vance, and E. H. Leiter, “Adverse hepatic and cardiac responses to rosiglitazone in a new mouse model of type 2 diabetes: relation to dysregulated phosphatidylcholine metabolism,” Vascular Pharmacology, vol. 45, no. 1, pp. 65–71, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. K. Pfeiffer, V. Gohil, R. A. Stuart et al., “Cardiolipin stabilizes respiratory chain supercomplexes,” The Journal of Biological Chemistry, vol. 278, no. 52, pp. 52873–52880, 2003. View at Publisher · View at Google Scholar · View at Scopus
  62. E. Mileykovskaya and W. Dowhan, “Cardiolipin-dependent formation of mitochondrial respiratory supercomplexes,” Chemistry and Physics of Lipids, vol. 179, pp. 42–48, 2014. View at Publisher · View at Google Scholar · View at Scopus
  63. V. Koshkin and M. L. Greenberg, “Cardiolipin prevents rate-dependent uncoupling and provides osmotic stability in yeast mitochondria,” Biochemical Journal, vol. 364, no. 1, pp. 317–322, 2002. View at Google Scholar · View at Scopus
  64. M. N. Sack, “Type 2 diabetes, mitochondrial biology and the heart,” Journal of Molecular and Cellular Cardiology, vol. 46, no. 6, pp. 842–849, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. D. L. Carden and D. N. Granger, “Pathophysiology of ischaemia-reperfusion injury,” The Journal of Pathology, vol. 190, no. 3, pp. 255–266, 2000. View at Publisher · View at Google Scholar · View at Scopus
  66. C. E. Ganote, “Contraction band necrosis and irreversible myocardial injury,” Journal of Molecular and Cellular Cardiology, vol. 15, no. 2, pp. 67–73, 1983. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Ruiz-Meana, D. Garcia-Dorado, B. Hofstaetter, H. M. Piper, and J. Soler-Soler, “Propagation of cardiomyocyte hypercontracture by passage of Na+ through gap junctions,” Circulation Research, vol. 85, no. 3, pp. 280–287, 1999. View at Publisher · View at Google Scholar · View at Scopus
  68. D. G. Allen and C. H. Orchard, “Myocardial contractile function during ischemia and hypoxia,” Circulation Research, vol. 60, no. 2, pp. 153–168, 1987. View at Publisher · View at Google Scholar · View at Scopus
  69. Y. Chandrashekhar, A. J. Prahash, S. Sen, S. Gupta, and I. S. Anand, “Cardiomyocytes from hearts with left ventricular dysfunction after ischemia-reperfusion do not manifest contractile abnormalities,” Journal of the American College of Cardiology, vol. 34, no. 2, pp. 594–602, 1999. View at Publisher · View at Google Scholar · View at Scopus
  70. A. L. Wit and M. J. Janse, “Reperfusion arrhythmias and sudden cardiac death: a century of progress toward an understanding of the mechanisms,” Circulation Research, vol. 89, no. 9, pp. 741–743, 2001. View at Google Scholar · View at Scopus
  71. W. E. Cascio, H. Yang, B. J. Muller-Borer, and T. A. Johnson, “Ischemia-induced arrhythmia: the role of connexins, gap junctions, and attendant changes in impulse propagation,” Journal of Electrocardiology, vol. 38, no. 4, supplement, pp. 55–59, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. A. V. Ghuran and A. J. Camm, “Ischaemic heart disease presenting as arrhythmias,” British Medical Bulletin, vol. 59, no. 1, pp. 193–210, 2001. View at Publisher · View at Google Scholar · View at Scopus
  73. N. Luqman, R. J. Sung, C.-L. Wang, and C.-T. Kuo, “Myocardial ischemia and ventricular fibrillation: pathophysiology and clinical implications,” International Journal of Cardiology, vol. 119, no. 3, pp. 283–290, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. I. V. Kazbanov, R. H. Clayton, M. P. Nash et al., “Effect of global cardiac ischemia on human ventricular fibrillation: insights from a multi-scale mechanistic model of the human heart,” PLoS Computational Biology, vol. 10, no. 11, Article ID e1003891, 2014. View at Publisher · View at Google Scholar · View at Scopus
  75. R. Ferrari, C. Ceconi, S. Curello et al., “Role of oxygen free radicals in ischemic and reperfused myocardium,” The American Journal of Clinical Nutrition, vol. 53, no. 1, pp. 215S–222S, 1991. View at Google Scholar · View at Scopus
  76. R. A. Kloner, K. Przyklenk, and P. Whittaker, “Deleterious effects of oxygen radicals in ischemia/reperfusion. Resolved and unresolved issues,” Circulation, vol. 80, no. 5, pp. 1115–1127, 1989. View at Publisher · View at Google Scholar · View at Scopus
  77. T. Kalogeris, Y. Bao, and R. J. Korthuis, “Mitochondrial reactive oxygen species: a double edged sword in ischemia/reperfusion vs preconditioning,” Redox Biology, vol. 2, no. 1, pp. 702–714, 2014. View at Publisher · View at Google Scholar · View at Scopus
  78. G. Paradies, G. Petrosillo, M. Pistolese, N. Di Venosa, D. Serena, and F. M. Ruggiero, “Lipid peroxidation and alterations to oxidative metabolism in mitochondria isolated from rat heart subjected to ischemia and reperfusion,” Free Radical Biology and Medicine, vol. 27, no. 1-2, pp. 42–50, 1999. View at Publisher · View at Google Scholar · View at Scopus
  79. E. J. Lesnefsky, T. J. Slabe, M. S. K. Stoll, P. E. Minkler, and C. L. Hoppel, “Myocardial ischemia selectively depletes cardiolipin in rabbit heart subsarcolemmal mitochondria,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 280, no. 6, pp. H2770–H2778, 2001. View at Google Scholar · View at Scopus
  80. G. Paradies, G. Petrosillo, M. Pistolese, N. Di Venosa, A. Federici, and F. M. Ruggiero, “Decrease in mitochondrial complex I activity in ischemic/reperfused rat heart: involvement of reactive oxygen species and cardiolipin,” Circulation Research, vol. 94, no. 1, pp. 53–59, 2004. View at Publisher · View at Google Scholar · View at Scopus
  81. G. Petrosillo, F. M. Ruggiero, N. Di Venosa, and G. Paradies, “Decreased complex III activity in mitochondria isolated from rat heart subjected to ischemia and reperfusion: role of reactive oxygen species and cardiolipin,” The FASEB Journal, vol. 17, no. 6, pp. 714–716, 2003. View at Google Scholar · View at Scopus
  82. V. E. Kagan, V. A. Tyurin, J. Jiang et al., “Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors,” Nature Chemical Biology, vol. 1, no. 4, pp. 223–232, 2005. View at Publisher · View at Google Scholar · View at Scopus
  83. Y. A. Vladimirov, E. V. Proskurnina, D. Y. Izmailov et al., “Cardiolipin activates cytochrome c peroxidase activity since it facilitates H2O2 access to heme,” Biochemistry, vol. 71, no. 9, pp. 998–1005, 2006. View at Publisher · View at Google Scholar · View at Scopus
  84. K. Nomura, H. Imai, T. Koumura, T. Kobayashi, and Y. Nakagawa, “Mitochondrial phospholipid hydroperoxide glutathione peroxidase inhibits the release of cytochrome c from mitochondria by suppressing the peroxidation of cardiolipin in hypoglycaemia-induced apoptosis,” Biochemical Journal, vol. 351, no. 1, pp. 183–193, 2000. View at Publisher · View at Google Scholar · View at Scopus
  85. M. Lutter, G. A. Perkins, and X. Wang, “The pro-apoptotic Bcl-2 family member tBid localizes to mitochondrial contact sites,” BMC Cell Biology, vol. 2, article 22, 2001. View at Publisher · View at Google Scholar · View at Scopus
  86. S. Lucken-Ardjomande, S. Montessuit, and J.-C. Martinou, “Contributions to Bax insertion and oligomerization of lipids of the mitochondrial outer membrane,” Cell Death and Differentiation, vol. 15, no. 5, pp. 929–937, 2008. View at Publisher · View at Google Scholar · View at Scopus
  87. M.-A. Sani, E. J. Dufourc, and G. Gröbner, “How does the Bax-α1 targeting sequence interact with mitochondrial membranes? The role of cardiolipin,” Biochimica et Biophysica Acta: Biomembranes, vol. 1788, no. 3, pp. 623–631, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. R. F. Epand, J.-C. Martinou, M. Fornallaz-Mulhauser, D. W. Hughes, and R. M. Epand, “The apoptotic protein tBid promotes leakage by altering membrane curvature,” The Journal of Biological Chemistry, vol. 277, no. 36, pp. 32632–32639, 2002. View at Publisher · View at Google Scholar · View at Scopus
  89. R. Ross, “The pathogenesis of atherosclerosis: a perspective for the 1990s,” Nature, vol. 362, no. 6423, pp. 801–809, 1993. View at Publisher · View at Google Scholar · View at Scopus
  90. A. Tuominen, Y. I. Miller, L. F. Hansen, Y. A. Kesäniemi, J. L. Witztum, and S. Hörkkö, “A natural antibody to oxidized cardiolipin binds to oxidized low-density lipoprotein, apoptotic cells, and atherosclerotic lesions,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 26, no. 9, pp. 2096–2102, 2006. View at Publisher · View at Google Scholar · View at Scopus
  91. H. Zhong, J. Lu, L. Xia, M. Zhu, and H. Yin, “Formation of electrophilic oxidation products from mitochondrial cardiolipin in vitro and in vivo in the context of apoptosis and atherosclerosis,” Redox Biology, vol. 2, pp. 878–883, 2014. View at Publisher · View at Google Scholar · View at Scopus
  92. I. Marai, M. Shechter, P. Langevitz et al., “Anti-cardiolipin antibodies and endothelial function in patients with coronary artery disease,” The American Journal of Cardiology, vol. 101, no. 8, pp. 1094–1097, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. O. Türkoǧlu, N. Bariş, N. Kütükçüler, Ö. Şenarslan, S. Güneri, and G. Atilla, “Evaluation of serum anti-cardiolipin and oxidized low-density lipoprotein levels in chronic periodontitis patients with essential hypertension,” Journal of Periodontology, vol. 79, no. 2, pp. 332–340, 2008. View at Publisher · View at Google Scholar · View at Scopus
  94. D. Lopez, K. Kobayashi, J. T. Merrill, E. Matsuura, and L. R. Lopez, “IgG autoantibodies against β2-glycoprotein I complexed with a lipid ligand derived from oxidized low-density lipoprotein are associated with arterial thrombosis in antiphospholipid syndrome,” Clinical and Developmental Immunology, vol. 10, no. 2–4, pp. 203–211, 2003. View at Publisher · View at Google Scholar · View at Scopus
  95. J. Su, A. G. Frostegård, X. Hua et al., “Low levels of antibodies against oxidized but not nonoxidized cardiolipin and phosphatidylserine are associated with atherosclerotic plaques in systemic lupus erythematosus,” Journal of Rheumatology, vol. 40, no. 11, pp. 1856–1864, 2013. View at Publisher · View at Google Scholar · View at Scopus
  96. V. N. Bochkov, O. V. Oskolkova, K. G. Birukov, A.-L. Levonen, C. J. Binder, and J. Stöckl, “Generation and biological activities of oxidized phospholipids,” Antioxidants & Redox Signaling, vol. 12, no. 8, pp. 1009–1059, 2010. View at Publisher · View at Google Scholar · View at Scopus
  97. A. G. Frostegård, J. Su, X. Hua, M. Vikström, U. De Faire, and J. Frostegård, “Antibodies against native and oxidized cardiolipin and phosphatidylserine and phosphorylcholine in atherosclerosis development,” PLoS ONE, vol. 9, no. 12, Article ID e111764, 2014. View at Publisher · View at Google Scholar · View at Scopus
  98. J. Su, X. Hua, M. Vikström et al., “Low levels of IgM antibodies to oxidized cardiolipin increase and high levels decrease risk of cardiovascular disease among 60-year olds: a prospective study,” BMC Cardiovascular Disorders, vol. 13, article 1, 2013. View at Publisher · View at Google Scholar · View at Scopus
  99. M. Wan, X. Hua, J. Su et al., “Oxidized but not native cardiolipin has pro-inflammatory effects, which are inhibited by Annexin A5,” Atherosclerosis, vol. 235, no. 2, pp. 592–598, 2014. View at Publisher · View at Google Scholar · View at Scopus
  100. K. M. Davey, J. S. Parboosingh, D. R. McLeod et al., “Mutation of DNAJC19, a human homologue of yeast inner mitochondrial membrane co-chaperones, causes DCMA syndrome, a novel autosomal recessive Barth syndrome-like condition,” Journal of Medical Genetics, vol. 43, no. 5, pp. 385–393, 2006. View at Publisher · View at Google Scholar · View at Scopus
  101. P. D. D'Silva, B. Schilke, W. Walter, A. Andrew, and E. A. Craig, “J protein cochaperone of the mitochondrial inner membrane required for protein import into the mitochondrial matrix,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 2, pp. 13839–13844, 2003. View at Publisher · View at Google Scholar · View at Scopus
  102. D. Mokranjac, M. Sichting, W. Neupert, and K. Hell, “Tim14, a novel key component of the import motor of the TIM23 protein translocase of mitochondria,” The EMBO Journal, vol. 22, no. 19, pp. 4945–4956, 2003. View at Publisher · View at Google Scholar · View at Scopus
  103. P. Rehling, N. Pfanner, and C. Meisinger, “Insertion of hydrophobic membrane proteins into the inner mitochondrial membrane—a guided tour,” Journal of Molecular Biology, vol. 326, no. 3, pp. 639–657, 2003. View at Publisher · View at Google Scholar · View at Scopus
  104. N. Gebert, A. S. Joshi, S. Kutik et al., “Mitochondrial cardiolipin involved in outer membrane protein biogenesis: implications for Barth syndrome,” Current Biology, vol. 19, no. 24, pp. 2133–2139, 2009. View at Publisher · View at Google Scholar · View at Scopus
  105. T. Endo, M. Eilers, and G. Schatz, “Binding of a tightly folded artificial mitochondrial precursor protein to the mitochondrial outer membrane involves a lipid-mediated conformational change,” The Journal of Biological Chemistry, vol. 264, no. 5, pp. 2951–2956, 1989. View at Google Scholar · View at Scopus
  106. T. Endo and G. Schatz, “Latent membrane perturbation activity of a mitochondrial precursor protein is exposed by unfolding,” The EMBO Journal, vol. 7, no. 4, pp. 1153–1158, 1988. View at Google Scholar · View at Scopus
  107. M. Eilers, T. Endo, and G. Schatz, “Adriamycin, a drug interacting with acidic phospholipids, blocks import of precursor proteins by isolated yeast mitochondria,” The Journal of Biological Chemistry, vol. 264, no. 5, pp. 2945–2950, 1989. View at Google Scholar · View at Scopus
  108. F. Jiang, M. T. Ryan, M. Schlame et al., “Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function,” The Journal of Biological Chemistry, vol. 275, no. 29, pp. 22387–22394, 2000. View at Publisher · View at Google Scholar · View at Scopus
  109. R. Richter-Dennerlein, A. Korwitz, M. Haag et al., “DNAJC19, a mitochondrial cochaperone associated with cardiomyopathy, forms a complex with prohibitins to regulate cardiolipin remodeling,” Cell Metabolism, vol. 20, no. 1, pp. 158–171, 2014. View at Publisher · View at Google Scholar · View at Scopus
  110. J. J. V. McMurray and M. A. Pfeffer, “Heart failure,” The Lancet, vol. 365, no. 9474, pp. 1877–1889, 2005. View at Publisher · View at Google Scholar · View at Scopus
  111. H. K. Saini-Chohan, M. G. Holmes, A. J. Chicco et al., “Cardiolipin biosynthesis and remodeling enzymes are altered during development of heart failure,” Journal of Lipid Research, vol. 50, no. 8, pp. 1600–1608, 2009. View at Publisher · View at Google Scholar · View at Scopus
  112. G. C. Sparagna, A. J. Chicco, R. C. Murphy et al., “Loss of cardiac tetralinoleoyl cardiolipin in human and experimental heart failure,” Journal of Lipid Research, vol. 48, no. 7, pp. 1559–1570, 2007. View at Publisher · View at Google Scholar · View at Scopus
  113. K. C. Chatfield, G. C. Sparagna, C. C. Sucharov et al., “Dysregulation of cardiolipin biosynthesis in pediatric heart failure,” Journal of Molecular and Cellular Cardiology, vol. 74, pp. 251–259, 2014. View at Publisher · View at Google Scholar · View at Scopus
  114. C. H. Le, C. M. Mulligan, M. A. Routh et al., “Delta-6-desaturase links polyunsaturated fatty acid metabolism with phospholipid remodeling and disease progression in heart failure,” Circulation: Heart Failure, vol. 7, no. 1, pp. 172–183, 2014. View at Publisher · View at Google Scholar · View at Scopus
  115. D. K. Reibel, B. O'Rourke, K. A. Foster, H. Hutchinson, C. E. Uboh, and R. L. Kent, “Altered phospholipid metabolism in pressure-overload hypertrophied hearts,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 250, no. 1, pp. H1–H6, 1986. View at Google Scholar · View at Scopus
  116. M. Rosca, P. Minkler, and C. L. Hoppel, “Cardiac mitochondria in heart failure: normal cardiolipin profile and increased threonine phosphorylation of complex IV,” Biochimica et Biophysica Acta: Bioenergetics, vol. 1807, no. 11, pp. 1373–1382, 2011. View at Publisher · View at Google Scholar · View at Scopus
  117. D. S. Fredrickson, “The inheritance of high density lipoprotein deficiency (Tangier disease),” The Journal of Clinical Investigation, vol. 43, pp. 228–236, 1964. View at Publisher · View at Google Scholar · View at Scopus
  118. J. F. Oram, “Tangier disease and ABCA1,” Biochimica et Biophysica Acta (BBA)—Molecular and Cell Biology of Lipids, vol. 1529, no. 1–3, pp. 321–330, 2000. View at Publisher · View at Google Scholar · View at Scopus
  119. S. Rust, M. Rosier, H. Funke et al., “Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1,” Nature Genetics, vol. 22, no. 4, pp. 352–355, 1999. View at Publisher · View at Google Scholar · View at Scopus
  120. B. L. Knight, “ATP-binding cassette transporter A1: regulation of cholesterol efflux,” Biochemical Society Transactions, vol. 32, no. 1, pp. 124–127, 2004. View at Publisher · View at Google Scholar · View at Scopus
  121. N. Wang, D. L. Silver, C. Thiele, and A. R. Tall, “ATP-binding cassette transporter A1 (ABCA1) functions as a cholesterol efflux regulatory protein,” The Journal of Biological Chemistry, vol. 276, no. 26, pp. 23742–23747, 2001. View at Publisher · View at Google Scholar · View at Scopus
  122. M. Fobker, R. Voss, H. Reinecke, C. Crone, G. Assmann, and M. Walter, “Accumulation of cardiolipin and lysocardiolipin in fibroblasts from Tangier disease subjects,” FEBS Letters, vol. 500, no. 3, pp. 157–162, 2001. View at Publisher · View at Google Scholar · View at Scopus
  123. C. Maack and B. O'Rourke, “Excitation-contraction coupling and mitochondrial energetics,” Basic Research in Cardiology, vol. 102, no. 5, pp. 369–392, 2007. View at Publisher · View at Google Scholar · View at Scopus
  124. M.-S. Beaudoin, C. G. R. Perry, A. M. Arkell et al., “Impairments in mitochondrial palmitoyl-CoA respiratory kinetics that precede development of diabetic cardiomyopathy are prevented by resveratrol in ZDF rats,” The Journal of Physiology, vol. 592, no. 12, pp. 2519–2533, 2014. View at Publisher · View at Google Scholar · View at Scopus
  125. D. Montaigne, X. Marechal, A. Coisne et al., “Myocardial contractile dysfunction is associated with impaired mitochondrial function and dynamics in type 2 diabetic but not in obese patients,” Circulation, vol. 130, no. 7, pp. 554–564, 2014. View at Publisher · View at Google Scholar · View at Scopus
  126. N. S. Dhalla, S. Rangi, S. Zieroth, and Y.-J. Xu, “Alterations in sarcoplasmic reticulum and mitochondrial functions in diabetic cardiomyopathy,” Experimental & Clinical Cardiology, vol. 17, no. 3, pp. 115–120, 2012. View at Google Scholar · View at Scopus
  127. M. Zhang, J. Wei, H. Shan et al., “Calreticulin-STAT3 signaling pathway modulates mitochondrial function in a rat model of furazolidone-induced dilated cardiomyopathy,” PLoS ONE, vol. 8, no. 6, Article ID e66779, 2013. View at Publisher · View at Google Scholar · View at Scopus
  128. X. Wang, M. Bathina, J. Lynch et al., “Deletion of MCL-1 causes lethal cardiac failure and mitochondrial dysfunction,” Genes & Development, vol. 27, no. 12, pp. 1351–1364, 2013. View at Publisher · View at Google Scholar · View at Scopus
  129. D. Hayashi, S. Ohshima, S. Isobe et al., “Increased 99mTc-sestamibi washout reflects impaired myocardial contractile and relaxation reserve during dobutamine stress due to mitochondrial dysfunction in dilated cardiomyopathy patients,” Journal of the American College of Cardiology, vol. 61, no. 19, pp. 2007–2017, 2013. View at Publisher · View at Google Scholar · View at Scopus
  130. C. Jung, A. S. Martins, E. Niggli, and N. Shirokova, “Dystrophic cardiomyopathy: amplification of cellular damage by Ca2+ signalling and reactive oxygen species-generating pathways,” Cardiovascular Research, vol. 77, no. 4, pp. 766–773, 2008. View at Publisher · View at Google Scholar · View at Scopus
  131. Y. Burelle, M. Khairallah, A. Ascah et al., “Alterations in mitochondrial function as a harbinger of cardiomyopathy: lessons from the dystrophic heart,” Journal of Molecular and Cellular Cardiology, vol. 48, no. 2, pp. 310–321, 2010. View at Publisher · View at Google Scholar · View at Scopus
  132. E. T. Chouchani, C. Methner, G. Buonincontri et al., “Complex I deficiency due to selective loss of Ndufs4 in the mouse heart results in severe hypertrophic cardiomyopathy,” PLoS ONE, vol. 9, no. 4, Article ID e94157, 2014. View at Publisher · View at Google Scholar · View at Scopus
  133. C. M. Hagen, F. H. Aidt, P. L. Hedley et al., “Mitochondrial haplogroups modify the risk of developing hypertrophic cardiomyopathy in a Danish population,” PLoS ONE, vol. 8, no. 8, Article ID e71904, 2013. View at Publisher · View at Google Scholar · View at Scopus
  134. X. Liu, B. Ye, S. Miller et al., “Ablation of ALCAT1 mitigates hypertrophic cardiomyopathy through effects on oxidative stress and mitophagy,” Molecular and Cellular Biology, vol. 32, no. 21, pp. 4493–4504, 2012. View at Publisher · View at Google Scholar · View at Scopus
  135. L. Lin, V. K. Sharma, and S.-S. Sheu, “Mechanisms of reduced mitochondrial Ca2+ accumulation in failing hamster heart,” Pflügers Archi—European Journal of Physiology, vol. 454, no. 3, pp. 395–402, 2007. View at Publisher · View at Google Scholar · View at Scopus
  136. G. Karamanlidis, C. F. Lee, L. Garcia-Menendez et al., “Mitochondrial complex I deficiency increases protein acetylation and accelerates heart failure,” Cell Metabolism, vol. 18, no. 2, pp. 239–250, 2013. View at Publisher · View at Google Scholar · View at Scopus
  137. S. Boudina and E. D. Abel, “Diabetic cardiomyopathy revisited,” Circulation, vol. 115, no. 25, pp. 3213–3223, 2007. View at Publisher · View at Google Scholar · View at Scopus
  138. M. Fry and D. E. Green, “Cardiolipin requirement for electron transfer in complex I and III of the mitochondrial respiratory chain,” The Journal of Biological Chemistry, vol. 256, no. 4, pp. 1874–1880, 1981. View at Google Scholar · View at Scopus
  139. M. Zhang, E. Mileykovskaya, and W. Dowhan, “Gluing the respiratory chain together: cardiolipin is required for supercomplex formation in the inner mitochondrial membrane,” The Journal of Biological Chemistry, vol. 277, no. 46, pp. 43553–43556, 2002. View at Publisher · View at Google Scholar · View at Scopus
  140. M. Zhang, E. Mileykovskaya, and W. Dowhan, “Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria,” The Journal of Biological Chemistry, vol. 280, no. 33, pp. 29403–29408, 2005. View at Publisher · View at Google Scholar · View at Scopus
  141. V. M. Gohil, P. Hayes, S. Matsuyama, H. Schägger, M. Schlame, and M. L. Greenberg, “Cardiolipin biosynthesis and mitochondrial respiratory chain function are interdependent,” The Journal of Biological Chemistry, vol. 279, no. 41, pp. 42612–42618, 2004. View at Publisher · View at Google Scholar · View at Scopus
  142. A. Ranieri, D. Millo, G. Di Rocco et al., “Immobilized cytochrome c bound to cardiolipin exhibits peculiar oxidation state-dependent axial heme ligation and catalytically reduces dioxygen,” Journal of Biological Inorganic Chemistry, vol. 20, no. 3, pp. 531–540, 2015. View at Publisher · View at Google Scholar · View at Scopus
  143. K. Beyer and M. Klingenberg, “ADP/ATP carrier protein from beef heart mitochondria has high amounts of tightly bound cardiolipin, as revealed by 31P nuclear magnetic resonance,” Biochemistry, vol. 24, no. 15, pp. 3821–3826, 1985. View at Publisher · View at Google Scholar · View at Scopus
  144. G. Paradies and F. M. Ruggiero, “The effect of doxorubicin on the transport of pyruvate in rat-heart mitochondria,” Biochemical and Biophysical Research Communications, vol. 156, no. 3, pp. 1302–1307, 1988. View at Publisher · View at Google Scholar · View at Scopus
  145. B. Kadenbach, P. Mende, H. V. J. Kolbe, I. Stipani, and F. Palmieri, “The mitochondrial phosphate carrier has an essential requirement for cardiolipin,” FEBS Letters, vol. 139, no. 1, pp. 109–112, 1982. View at Publisher · View at Google Scholar · View at Scopus
  146. G. Paradies, G. Petrosillo, M. Pistolese, and F. M. Ruggiero, “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 Letters, vol. 466, no. 2-3, pp. 323–326, 2000. View at Publisher · View at Google Scholar · View at Scopus
  147. A. Musatov, “Contribution of peroxidized cardiolipin to inactivation of bovine heart cytochrome c oxidase,” Free Radical Biology and Medicine, vol. 41, no. 2, pp. 238–246, 2006. View at Publisher · View at Google Scholar · View at Scopus
  148. H. Schägger and K. Pfeiffer, “Supercomplexes in the respiratory chains of yeast and mammalian mitochondria,” The EMBO Journal, vol. 19, no. 8, pp. 1777–1783, 2000. View at Publisher · View at Google Scholar · View at Scopus
  149. M. McKenzie, M. Lazarou, D. R. Thorburn, and M. T. Ryan, “Mitochondrial respiratory chain supercomplexes are destabilized in barth syndrome patients,” Journal of Molecular Biology, vol. 361, no. 3, pp. 462–469, 2006. View at Publisher · View at Google Scholar · View at Scopus
  150. T. A. Ajith and T. G. Jayakumar, “Mitochondria-targeted agents: future perspectives of mitochondrial pharmaceutics in cardiovascular diseases,” World Journal of Cardiology, vol. 6, no. 10, pp. 1091–1099, 2014. View at Publisher · View at Google Scholar
  151. K. Zhao, G.-M. Zhao, D. Wu et al., “Cell-permeable peptide antioxidants targeted to inner mitochondrial membrane inhibit mitochondrial swelling, oxidative cell death, and reperfusion injury,” Journal of Biological Chemistry, vol. 279, no. 33, pp. 34682–34690, 2004. View at Publisher · View at Google Scholar · View at Scopus
  152. J. Cho, K. Won, D. Wu et al., “Potent mitochondria-targeted peptides reduce myocardial infarction in rats,” Coronary Artery Disease, vol. 18, no. 3, pp. 215–220, 2007. View at Publisher · View at Google Scholar · View at Scopus
  153. H. H. Szeto, “Mitochondria-targeted cytoprotective peptides for ischemia-reperfusion injury,” Antioxidants & Redox Signaling, vol. 10, no. 3, pp. 601–619, 2008. View at Publisher · View at Google Scholar · View at Scopus
  154. G. F. Kelso, A. Maroz, H. M. Cochemé et al., “A mitochondria-targeted macrocyclic Mn(II) superoxide dismutase mimetic,” Chemistry & Biology, vol. 19, no. 10, pp. 1237–1246, 2012. View at Publisher · View at Google Scholar · View at Scopus
  155. R. A. J. Smith, C. M. Porteous, C. V. Coulter, and M. P. Murphy, “Selective targeting of an antioxidant to mitochondria,” European Journal of Biochemistry, vol. 263, no. 3, pp. 709–716, 1999. View at Publisher · View at Google Scholar · View at Scopus
  156. G. F. Kelso, C. M. Porteous, C. V. Coulter et al., “Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties,” The Journal of Biological Chemistry, vol. 276, no. 7, pp. 4588–4596, 2001. View at Publisher · View at Google Scholar · View at Scopus
  157. S. E. Brown, M. F. Ross, A. Sanjuan-Pla, A.-R. B. Manas, R. A. J. Smith, and M. P. Murphy, “Targeting lipoic acid to mitochondria: synthesis and characterization of a triphenylphosphonium-conjugated α-lipoyl derivative,” Free Radical Biology and Medicine, vol. 42, no. 12, pp. 1766–1780, 2007. View at Publisher · View at Google Scholar · View at Scopus
  158. A. Sickmann, J. Reinders, Y. Wagner et al., “The proteome of Saccharomyces cerevisiae mitochondria,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 23, pp. 13207–13212, 2003. View at Publisher · View at Google Scholar · View at Scopus
  159. U. Nair and D. J. Klionsky, “Molecular mechanisms and regulation of specific and nonspecific autophagy pathways in yeast,” The Journal of Biological Chemistry, vol. 280, no. 51, pp. 41785–41788, 2005. View at Publisher · View at Google Scholar · View at Scopus
  160. K. Okamoto, “Organellophagy: eliminating cellular building blocks via selective autophagy,” The Journal of Cell Biology, vol. 205, no. 4, pp. 435–445, 2014. View at Publisher · View at Google Scholar · View at Scopus
  161. K. Wang and D. J. Klionsky, “Mitochondria removal by autophagy,” Autophagy, vol. 7, no. 3, pp. 297–300, 2011. View at Publisher · View at Google Scholar · View at Scopus
  162. A. G. Moyzis, J. Sadoshima, and Å. B. Gustafsson, “Mending a broken heart: the role of mitophagy in cardioprotection,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 308, no. 3, pp. H183–H192, 2015. View at Publisher · View at Google Scholar
  163. A. Nakai, O. Yamaguchi, T. Takeda et al., “The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress,” Nature Medicine, vol. 13, no. 5, pp. 619–624, 2007. View at Publisher · View at Google Scholar · View at Scopus
  164. P.-J. Linton, M. Gurney, D. Sengstock, R. M. Mentzer Jr., and R. A. Gottlieb, “This old heart: cardiac aging and autophagy,” Journal of Molecular and Cellular Cardiology, vol. 83, pp. 44–54, 2015. View at Publisher · View at Google Scholar · View at Scopus
  165. H. D. Sybers, J. Ingwall, and M. DeLuca, “Autophagy in cardiac myocytes,” Recent Advances in Studies on Cardiac Structure and Metabolism, vol. 26-29, no. 12, pp. 453–463, 1976. View at Google Scholar · View at Scopus
  166. L. Yan, D. E. Vatner, S.-J. Kim et al., “Autophagy in chronically ischemic myocardium,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 39, pp. 13807–13812, 2005. View at Publisher · View at Google Scholar · View at Scopus
  167. A. Hamacher-Brady, N. R. Brady, S. E. Logue et al., “Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy,” Cell Death and Differentiation, vol. 14, no. 1, pp. 146–157, 2007. View at Publisher · View at Google Scholar · View at Scopus
  168. C. Huang, S. Yitzhaki, C. N. Perry et al., “Autophagy induced by ischemic preconditioning is essential for cardioprotection,” Journal of Cardiovascular Translational Research, vol. 3, no. 4, pp. 365–373, 2010. View at Publisher · View at Google Scholar · View at Scopus
  169. L. Valentim, K. M. Laurence, P. A. Townsend et al., “Urocortin inhibits Beclin1-mediated autophagic cell death in cardiac myocytes exposed to ischaemia/reperfusion injury,” Journal of Molecular and Cellular Cardiology, vol. 40, no. 6, pp. 846–852, 2006. View at Publisher · View at Google Scholar · View at Scopus
  170. Y. Matsui, H. Takagi, X. Qu et al., “Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and beclin 1 in mediating autophagy,” Circulation Research, vol. 100, no. 6, pp. 914–922, 2007. View at Publisher · View at Google Scholar · View at Scopus
  171. L.-T. Wang, B.-L. Chen, C.-T. Wu, K.-H. Huang, C.-K. Chiang, and S. H. Liu, “Protective role of AMP-activated protein kinase-evoked autophagy on an in vitro model of ischemia/reperfusion-induced renal tubular cell injury,” PLoS ONE, vol. 8, no. 11, Article ID e79814, 2013. View at Publisher · View at Google Scholar · View at Scopus
  172. R. Guo and J. Ren, “Deficiency in AMPK attenuates ethanol-induced cardiac contractile dysfunction through inhibition of autophagosome formation,” Cardiovascular Research, vol. 94, no. 3, pp. 480–491, 2012. View at Publisher · View at Google Scholar · View at Scopus
  173. M. A. Paiva, Z. Rutter-Locher, L. M. Gonçalves et al., “Enhancing AMPK activation during ischemia protects the diabetic heart against reperfusion injury,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 300, no. 6, pp. H2123–H2134, 2011. View at Publisher · View at Google Scholar · View at Scopus
  174. C. Huang, W. Liu, C. N. Perry et al., “Autophagy and protein kinase C are required for cardioprotection by sulfaphenazole,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 298, no. 2, pp. H570–H579, 2010. View at Publisher · View at Google Scholar · View at Scopus
  175. R. S. Decker and K. Wildenthal, “Lysosomal alterations in hypoxic and reoxygenated hearts. I. Ultrastructural and cytochemical changes,” The American Journal of Pathology, vol. 98, no. 2, pp. 425–444, 1980. View at Google Scholar · View at Scopus
  176. X. Ma, H. Liu, S. R. Foyil et al., “Impaired autophagosome clearance contributes to cardiomyocyte death in ischemia/reperfusion injury,” Circulation, vol. 125, no. 25, pp. 3170–3181, 2012. View at Publisher · View at Google Scholar · View at Scopus
  177. C. T. Chu, J. Ji, R. K. Dagda et al., “Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells,” Nature Cell Biology, vol. 15, no. 10, pp. 1197–1205, 2013. View at Publisher · View at Google Scholar · View at Scopus
  178. C. T. Chu, H. Bayir, and V. E. Kagan, “LC3 binds externalized cardiolipin on injured mitochondria to signal mitophagy in neurons: implications for Parkinson disease,” Autophagy, vol. 10, no. 2, pp. 376–378, 2014. View at Publisher · View at Google Scholar · View at Scopus
  179. L. Wang, X. Liu, J. Nie et al., “ALCAT1 controls mitochondrial etiology of fatty liver diseases, linking defective mitophagy to steatosis,” Hepatology, vol. 61, no. 2, pp. 486–496, 2015. View at Publisher · View at Google Scholar · View at Scopus
  180. W. Huang, W. Choi, W. Hu et al., “Crystal structure and biochemical analyses reveal Beclin 1 as a novel membrane binding protein,” Cell Research, vol. 22, no. 3, pp. 473–489, 2012. View at Publisher · View at Google Scholar · View at Scopus
  181. H. Mellor and P. J. Parker, “The extended protein kinase C superfamily,” Biochemical Journal, vol. 332, part 2, pp. 281–292, 1998. View at Google Scholar · View at Scopus
  182. S. P. Marso and D. M. Stern, Diabetes and Cardiovascular Disease: Integrating Science and Clinical Medicine, Lippincott Williams & Wilkins, 2003.
  183. D. R. Meldrum, J. C. Cleveland Jr., X. Meng et al., “Protein kinase C isoform diversity in preconditioning,” Journal of Surgical Research, vol. 69, no. 1, pp. 183–187, 1997. View at Publisher · View at Google Scholar · View at Scopus
  184. M. Munakata, C. Stamm, I. Friehs et al., “Protective effects of protein kinase C during myocardial ischemia require activation of phosphatidyl-inositol specific phospholipase C,” Annals of Thoracic Surgery, vol. 73, no. 4, pp. 1236–1245, 2002. View at Publisher · View at Google Scholar · View at Scopus
  185. W. Jiang, L. Bian, L.-J. Ma, R.-Z. Tang, S. Xun, and Y.-W. He, “Hyperthermia-induced apoptosis in Tca8113 cells is inhibited by heat shock protein 27 through blocking phospholipid scramblase 3 phosphorylation,” International Journal of Hyperthermia, vol. 26, no. 6, pp. 523–537, 2010. View at Publisher · View at Google Scholar · View at Scopus
  186. Y. He, J. Liu, D. Grossman et al., “Phosphorylation of mitochondrial phospholipid scramblase 3 by protein kinase C-δ induces its activation and facilitates mitochondrial targeting of tBid,” Journal of Cellular Biochemistry, vol. 101, no. 5, pp. 1210–1221, 2007. View at Publisher · View at Google Scholar · View at Scopus
  187. J. E. Kowalczyk, M. Beresewicz, B. Gajkowska, and B. Zabłocka, “Association of protein kinase C delta and phospholipid scramblase 3 in hippocampal mitochondria correlates with neuronal vulnerability to brain ischemia,” Neurochemistry International, vol. 55, no. 1–3, pp. 157–163, 2009. View at Publisher · View at Google Scholar · View at Scopus
  188. Q. Zhong, G. Li, J. Gvozdenovic-Jeremic, and M. L. Greenberg, “Up-regulation of the cell integrity pathway in Saccharomyces cerevisiae suppresses temperature sensitivity of the pgs1Δ mutant,” Journal of Biological Chemistry, vol. 282, no. 22, pp. 15946–15953, 2007. View at Publisher · View at Google Scholar · View at Scopus
  189. S. Nomoto, Y. Watanabe, J. Ninomiya-Tsuji et al., “Functional analyses of mammalian protein kinase C isozymes in budding yeast and mammalian fibroblasts,” Genes to Cells, vol. 2, no. 10, pp. 601–614, 1997. View at Google Scholar · View at Scopus
  190. W. Korytowski, L. V. Basova, A. Pilat, R. M. Kernstock, and A. W. Girotti, “Permeabilization of the mitochondrial outer membrane by bax/truncated Bid (tBid) proteins as sensitized by cardiolipin hydroperoxide translocation: mechanistic implications for the intrinsic pathway of oxidative apoptosis,” The Journal of Biological Chemistry, vol. 286, no. 30, pp. 26334–26343, 2011. View at Publisher · View at Google Scholar · View at Scopus