Mitofusin-2 maintains mitochondrial structure and contributes to stress-induced permeability transition in cardiac myocytes

Molecular and Cellular Biology

Volumn 31, Issue 6, 2011, Pages 1309-1328

  Papanicolaou, Kyriakos N ^a   Khairallah, Ramzi J ^b   Ngoh, Gladys A ^a   Chikando, Aristide ^b   Luptak, Ivan ^a,c   O'Shea, Karen M ^b   Riley, Dushon D ^b   Lugus, Jesse J ^a   Colucci, Wilson S ^a,c   Lederer, W Jonathan ^b   Stanley, William C ^b   Walsh, Kenneth ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c BOSTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; MITOFUSIN 2; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ARTICLE; CELL DEATH; CELL STRUCTURE; CONTROLLED STUDY; HEART HYPERTROPHY; HEART MUSCLE CELL; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL PERMEABILITY; MITOCHONDRION; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY;

ANIMALS; CALCIUM; CARDIOMEGALY; CELL DEATH; CELLS, CULTURED; GENE DELETION; GTP PHOSPHOHYDROLASES; HEART; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; PERMEABILITY; RATS; REACTIVE OXYGEN SPECIES;

MUS;

EID: 79952265711     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00911-10     Document Type: Article

References (86)

1. Agah, R., et al. 1997. Gene recombination in postmitotic cells. Targeted expression of Cre recombinase provokes cardiac-restricted, site-specific rearrangement in adult ventricular muscle in vivo. J. Clin. Invest. 100:169-179.
2. Amchenkova, A. A., L. E. Bakeeva, Y. S. Chentsov, V. P. Skulachev, and D. B. Zorov. 1988. Coupling membranes as energy-transmitting cables. I. Filamentous mitochondria in fibroblasts and mitochondrial clusters in cardiomyocytes. J. Cell Biol. 107:481-495.
3. Antignani, A., and R. J. Youle. 2006. How do Bax and Bak lead to permeabilization of the outer mitochondrial membrane? Curr. Opin. Cell Biol. 18:685-689.
4. Aon, M. A., S. Cortassa, E. Marban, and B. O'Rourke. 2003. Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J. Biol. Chem. 278:44735-44744.
5. Bach, D., et al. 2003. Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism. A novel regulatory mechanism altered in obesity. J. Biol. Chem. 278:17190-17197.
6. Baines, C. P. 2010. The cardiac mitochondrion: nexus of stress. Annu. Rev. Physiol. 72:61-80.
7. Baines, C. P. 2009. The mitochondrial permeability transition pore and ischemia-reperfusion injury. Basic Res. Cardiol. 104:181-188.
8. Baines, C. P., et al. 2005. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434:658-662. (Pubitemid 40488559)
9. Baines, C. P., R. A. Kaiser, T. Sheiko, W. J. Craigen, and J. D. Molkentin. 2007. Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat. Cell Biol. 9:550-555.
10. Beraud, N., et al. 2009. Mitochondrial dynamics in heart cells: very low amplitude high frequency fluctuations in adult cardiomyocytes and flow motion in non beating Hl-1 cells. J. Bioenerg. Biomembr. 41:195-214.
11. Bereiter-Hahn, J., and M. Voth. 1994. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc. Res. Tech. 27:198-219.
12. Bernardi, P. 1992. Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by the proton electrochemical gradient. Evidence that the pore can be opened by membrane depolarization. J. Biol. Chem. 267:8834-8839.
13. Boncompagni, S., et al. 2009. Mitochondria are linked to calcium stores in striated muscle by developmentally regulated tethering structures. Mol. Biol. Cell 20:1058-1067.
14. Brady, N. R., et al. 2004. Coordinated behavior of mitochondria in both space and time: a reactive oxygen species-activated wave of mitochondrial depolarization. Biophys. J. 87:2022-2034. (Pubitemid 39167056)
15. Brady, N. R., A. Hamacher-Brady, H. V. Westerhoff, and R. A. Gottlieb. 2006. A wave of reactive oxygen species (ROS)-induced ROS release in a sea of excitable mitochondria. Antioxid. Redox Signal. 8:1651-1665.
16. Chen, H., and D. C. Chan. 2006. Critical dependence of neurons on mitochondrial dynamics. Curr. Opin. Cell Biol. 18:453-459.
17. Chen, H., A. Chomyn, and D. C. Chan. 2005. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 280:26185-26192.
18. Chen, H., et al. 2003. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160:189-200. (Pubitemid 36254953)
19. Chen, H., J. M. McCaffery, and D. C. Chan. 2007. Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 130:548-562.
20. Chen, H., et al. 2010. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 141:280-289.
21. Cipolat, S., O. Martins de Brito, B. Dal Zilio, and L. Scorrano. 2004. OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc. Natl. Acad. Sci. U. S. A. 101:15927-15932.
22. Clarke, S. J., G. P. McStay, and A. P. Halestrap. 2002. Sanglifehrin A acts as a potent inhibitor of the mitochondrial permeability transition and reperfusion injury of the heart by binding to cyclophilin-D at a different site from cyclosporin A. J. Biol. Chem. 277:34793-34799.
23. Crompton, M., S. Virji, and J. M. Ward. 1998. Cyclophilin-D binds strongly to complexes of the voltage-dependent anion channel and the adenine nucleotide translocase to form the permeability transition pore. Eur. J. Biochem. 258:729-735.
24. Dabkowski, E. R., C. L. Williamson, and J. M. Hollander. 2008. Mitochondria-specific transgenic overexpression of phospholipid hydroperoxide glutathione peroxidase (GPx4) attenuates ischemia/reperfusion-associated cardiac dysfunction. Free Radic. Biol. Med. 45:855-865.
25. Das, A., L. Xi, and R. C. Kukreja. 2005. Phosphodiesterase-5 inhibitor sildenafil preconditions adult cardiac myocytes against necrosis and apoptosis. Essential role of nitric oxide signaling. J. Biol. Chem. 280:12944-12955.
26. de Brito, O. M., and L. Scorrano. 2008. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456:605-610.
27. de Brito, O. M., and L. Scorrano. 2008. Mitofusin 2: a mitochondria-shaping protein with signaling roles beyond fusion. Antioxid. Redox Signal. 10:621-633.
28. Delettre, C., et al. 2000. Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat. Genet. 26:207-210.
29. Detmer, S. A., and D. C. Chan. 2007. Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell Biol. 8:870-879.
30. Di Lisa, F., and P. Bernardi. 2006. Mitochondria and ischemia-reperfusion injury of the heart: fixing a hole. Cardiovasc. Res. 70:191-199.
31. Elrod, J. W., et al. 2010. Cyclophilin D controls mitochondrial pore-dependent Ca(2+) exchange, metabolic flexibility, and propensity for heart failure in mice. J. Clin. Invest. 120:3680-3687.
32. Eura, Y., N. Ishihara, S. Yokota, and K. Mihara. 2003. Two mitofusin proteins, mammalian homologues of FZO, with distinct functions are both required for mitochondrial fusion. J. Biochem. 134:333-344. (Pubitemid 37288331)
33. Frezza, C., et al. 2006. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126:177-189.
34. Gaussin, V., et al. 2002. Endocardial cushion and myocardial defects after cardiac myocyte-specific conditional deletion of the bone morphogenetic protein receptor ALK3. Proc. Natl. Acad. Sci. U. S. A. 99:2878-2883.
35. Griffiths, E. J., and A. P. Halestrap. 1995. Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion. Biochem. J. 307:93-98.
36. Griparic, L., and A. M. van der Bliek. 2001. The many shapes of mitochondrial membranes. Traffic 2:235-244. (Pubitemid 32487553)
37. Gustafsson, A. B., and R. A. Gottlieb. 2008. Heart mitochondria: gates of life and death. Cardiovasc. Res. 77:334-343.
38. Halestrap, A. P. 2009. Mitochondria and reperfusion injury of the heart - a holey death but not beyond salvation. J. Bioenerg. Biomembr. 41:113-121.
39. Halestrap, A. P. 1987. The regulation of the oxidation of fatty acids and other substrates in rat heart mitochondria by changes in the matrix volume induced by osmotic strength, valinomycin and Ca2+. Biochem. J. 244:159-164. (Pubitemid 17098822)
40. Halestrap, A. P. 2009. What is the mitochondrial permeability transition pore? J. Mol. Cell. Cardiol. 46:821-831.
41. Hunter, D. R., and R. A. Haworth. 1979. The Ca2+-induced membrane transition in mitochondria. III. Transitional Ca2+ release. Arch. Biochem. Biophys. 195:468-477.
42. Imoto, M., I. Tachibana, and R. Urrutia. 1998. Identification and functional characterization of a novel human protein highly related to the yeast dynamin-like GTPase Vps1p. J. Cell Sci. 111:1341-1349. (Pubitemid 28274386)
43. Ishihara, N., Y. Eura, and K. Mihara. 2004. Mitofusin 1 and 2 play distinct roles in mitochondrial fusion reactions via GTPase activity. J. Cell Sci. 117:6535-6546. (Pubitemid 40214575)
44. Kabaeva, Z., M. Zhao, and D. E. Michele. 2008. Blebbistatin extends culture life of adult mouse cardiac myocytes and allows efficient and stable transgene expression. Am. J. Physiol. Heart Circ. Physiol. 294:H1667-H1674.
45. Karbowski, M., K. L. Norris, M. M. Cleland, S. Y. Jeong, and R. J. Youle. 2006. Role of Bax and Bak in mitochondrial morphogenesis. Nature 443:658-662.
46. Karbowski, M., and R. J. Youle. 2003. Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ. 10:870-880.
47. Khairallah, R. J., et al. 2010. Treatment with docosahexaenoic acid, but not eicosapentaenoic acid, delays Ca2+-induced mitochondria permeability transition in normal and hypertrophied myocardium. J. Pharmacol. Exp. Ther. 335:155-162.
48. King, K. L., et al. 2007. Fatty acid oxidation in cardiac and skeletal muscle mitochondria is unaffected by deletion of CD36. Arch. Biochem. Biophys. 467:234-238.
49. Kokoszka, J. E., et al. 2004. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 427:461-465. (Pubitemid 38168501)
50. Koshiba, T., et al. 2004. Structural basis of mitochondrial tethering by mitofusin complexes. Science 305:858-862. (Pubitemid 39038419)
51. Kristian, T., J. Gertsch, T. E. Bates, and B. K. Siesjo. 2000. Characteristics of the calcium-triggered mitochondrial permeability transition in nonsynaptic brain mitochondria: effect of cyclosporin A and ubiquinone O. J. Neurochem. 74:1999-2009.
52. Kroemer, G., L. Galluzzi, and C. Brenner. 2007. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87:99-163.
53. Kuznetsov, A. V., et al. 2006. Mitochondrial subpopulations and heterogeneity revealed by confocal imaging: possible physiological role? Biochim. Biophys. Acta 1757:686-691. (Pubitemid 43993850)
54. Lea, P. J., R. J. Temkin, K. B. Freeman, G. A. Mitchell, and B. H. Robinson. 1994. Variations in mitochondrial ultrastructure and dynamics observed by high resolution scanning electron microscopy (HRSEM). Microsc. Res. Tech. 27:269-277.
55. Legros, F., A. Lombes, P. Frachon, and M. Rojo. 2002. Mitochondrial fusion in human cells is efficient, requires the inner membrane potential, and is mediated by mitofusins. Mol. Biol. Cell 13:4343-4354.
56. Leung, A. W., and A. P. Halestrap. 2008. Recent progress in elucidating the molecular mechanism of the mitochondrial permeability transition pore. Biochim. Biophys. Acta 1777:946-952.
57. Luptak, I., et al. 2007. Aberrant activation of AMP-activated protein kinase remodels metabolic network in favor of cardiac glycogen storage. J. Clin. Invest. 117:1432-1439.
58. Martens, S., and H. T. McMahon. 2008. Mechanisms of membrane fusion: disparate players and common principles. Nat. Rev. Mol. Cell Biol. 9:543-556.
59. Medeiros, D. M. 2008. Assessing mitochondria biogenesis. Methods 46:288-294.
60. Nakagawa, T., et al. 2005. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434:652-658. (Pubitemid 40488558)
61. Ngoh, G. A., L. J. Watson, H. T. Facundo, W. Dillmann, and S. P. Jones. 2008. Non-canonical glycosyltransferase modulates post-hypoxic cardiac myocyte death and mitochondrial permeability transition. J. Mol. Cell. Cardiol. 45:313-325.
62. Olichon, A., et al. 2002. The human dynamin-related protein OPA1 is anchored to the mitochondrial inner membrane facing the inter-membrane space. FEBS Lett. 523:171-176. (Pubitemid 34786081)
63. Ong, S. B., et al. 2010. Inhibiting mitochondrial fission protects the heart against ischemia/reperfusion injury. Circulation 121:2012-2022.
64. O'Shea, K. M., et al. 2009. Dietary omega-3 fatty acids alter cardiac mitochondrial phospholipid composition and delay Ca2+-induced permeability transition. J. Mol. Cell. Cardiol. 47:819-827.
65. Papanicolaou, K. N., et al. 2010. Preserved heart function and maintained response to cardiac stresses in a genetic model of cardiomyocyte-targeted deficiency of cyclooxygenase-2. J. Mol. Cell. Cardiol. 49:196-209.
66. Parra, V., et al. 2008. Changes in mitochondrial dynamics during ceramide-induced cardiomyocyte early apoptosis. Cardiovasc. Res. 77:387-397.
67. Pich, S., et al. 2005. The Charcot-Marie-Tooth type 2A gene product, Mfn2, up-regulates fuel oxidation through expression of OXPHOS system. Hum. Mol. Genet. 14:1405-1415.
68. Pimentel, D. R., et al. 2001. Reactive oxygen species mediate amplitude-dependent hypertrophic and apoptotic responses to mechanical stretch in cardiac myocytes. Circ. Res. 89:453-460.
69. Ramachandran, R., and S. L. Schmid. 2008. Real-time detection reveals that effectors couple dynamin's GTP-dependent conformational changes to the membrane. EMBO J. 27:27-37.
70. Rizzuto, R., et al. 1998. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280:1763-1766. (Pubitemid 28283502)
71. Rizzuto, R., and T. Pozzan. 2006. Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol. Rev. 86:369-408.
72. Rosca, M. G., et al. 2008. Cardiac mitochondria in heart failure: decrease in respirasomes and oxidative phosphorylation. Cardiovasc. Res. 80:30-39.
73. Santel, A., et al. 2003. Mitofusin-1 protein is a generally expressed mediator of mitochondrial fusion in mammalian cells. J. Cell Sci. 116:2763-2774.
74. Santel, A., and M. T. Fuller. 2001. Control of mitochondrial morphology by a human mitofusin. J. Cell Sci. 114:867-874.
75. Shen, T., et al. 2007. Mitofusin-2 is a major determinant of oxidative stress-mediated heart muscle cell apoptosis. J. Biol. Chem. 282:23354-23361.
76. Shimada, T., K. Horita, M. Murakami, and R. Ogura. 1984. Morphological studies of different mitochondrial populations in monkey myocardial cells. Cell Tissue Res. 238:577-582. (Pubitemid 15190661)
77. Shioya, T. 2007. A simple technique for isolating healthy heart cells from mouse models. J. Physiol. Sci. 57:327-335.
78. Smirnova, E., L. Griparic, D. L. Shurland, and A. M. van der Bliek. 2001. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 12:2245-2256.
79. Suen, D. F., K. L. Norris, and R. J. Youle. 2008. Mitochondrial dynamics and apoptosis. Genes Dev. 22:1577-1590.
80. Tait, S. W., and D. R. Green. 2010. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 11:621-632.
81. Vendelin, M., et al. 2005. Mitochondrial regular arrangement in muscle cells: a "crystal-like" pattern. Am. J. Physiol. Cell Physiol. 288:C757-C767.
82. Wang, W., et al. 2008. Superoxide flashes in single mitochondria. Cell 134:279-290. (Pubitemid 352010332)
83. Wasilewski, M., and L. Scorrano. 2009. The changing shape of mitochondrial apoptosis. Trends Endocrinol. Metab. 20:287-294.
84. Yoon, Y., E. W. Krueger, B. J. Oswald, and M. A. McNiven. 2003. The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol. Cell. Biol. 23:5409-5420.
85. Zorov, D. B., C. R. Filburn, L. O. Klotz, J. L. Zweier, and S. J. Sollott. 2000. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J. Exp. Med. 192:1001-1014.
86. Zuchner, S., et al. 2004. Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat. Genet. 36:449-451.