Central role of mitofusin 2 in autophagosome-lysosome fusion in cardiomyocytes

Journal of Biological Chemistry

Volumn 287, Issue 28, 2012, Pages 23615-23625

  Zhao, Ting ^a   Huang, Xiaohu ^a   Han, Liang ^a   Wang, Xianhua ^a   Cheng, Hongqiang ^b   Zhao, Yungang ^a   Chen, Quan ^c   Chen, Ju ^b   Cheng, Heping ^a   Xiao, Ruiping ^a   Zheng, Ming ^a  

^a PEKING UNIVERSITY   (China)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c INSTITUTE OF ZOOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGIC DEGRADATION; AUTOPHAGOSOMES; AUTOPHAGY; CARDIOMYOCYTES; CARDIOPROTECTION; CELLULAR METABOLISM; CRITICAL STEPS; DYNAMIC PROTEINS; FUNCTIONAL DEFECTS; HEART FAILURE; ISCHEMIA REPERFUSION; KNOCKOUT MICE; OUTER MEMBRANE PROTEIN;

BIOLOGICAL MEMBRANES; CELL DEATH; DEGRADATION;

HEART;

MITOFUSIN 2; RAB7 PROTEIN; SHORT HAIRPIN RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL FUSION; CELL METABOLISM; CELL STRESS; CONTROLLED STUDY; GENE; GENE DELETION; GENE SILENCING; HEART DISEASE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; IMMUNOPRECIPITATION; LYSOSOME; MFN2 GENE; MITOCHONDRIAL RESPIRATION; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANIMALS; ANIMALS, NEWBORN; AUTOPHAGY; BLOTTING, WESTERN; CELLS, CULTURED; DNA, MITOCHONDRIAL; ECHOCARDIOGRAPHY; GTP PHOSPHOHYDROLASES; HEART; IMMUNOPRECIPITATION; LYSOSOMES; MEMBRANE FUSION; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA, HEART; MYOCARDIUM; MYOCYTES, CARDIAC; PHAGOSOMES; PROTEIN BINDING; RAB GTP-BINDING PROTEINS; REPERFUSION INJURY; RNA INTERFERENCE;

MUS;

EID: 84863613170     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.379164     Document Type: Article

References (60)

1. Santel, A., Frank, S., Gaume, B., Herrler, M., Youle, R. J., and Fuller, M. T. (2003) Mitofusin-1 protein is a generally expressed mediator of mitochondrial fusion in mammalian cells. J. Cell Sci. 116, 2763-2774 (Pubitemid 36857227)
2. Rojo, M., Legros, F., Chateau, D., and Lombès, A. (2002) Membrane topology and mitochondrial targeting of mitofusins, ubiquitous mammalian homologs of the transmembrane GTPase Fzo. J. Cell Sci. 115, 1663-1674 (Pubitemid 34520596)
3. Misaka, T., Miyashita, T., and Kubo, Y. (2002) Primary structure of a dynamin-related mouse mitochondrial GTPase and its distribution in brain, subcellular localization, and effect on mitochondrial morphology. J. Biol. Chem. 277, 15834-15842 (Pubitemid 34967862)
4. Liesa, M., Palacín, M., and Zorzano, A. (2009) Mitochondrial dynamics in mammalian health and disease. Physiol. Rev. 89, 799-845
5. Cipolat, S., Martins de Brito, O., Dal Zilio, B., and Scorrano, L. (2004) OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc. Natl. Acad. Sci. U.S.A. 101, 15927-15932 (Pubitemid 39507904)
6. Twig, G., Elorza, A., Molina, A. J., Mohamed, H., Wikstrom, J. D., Walzer, G., Stiles, L., Haigh, S. E., Katz, S., Las, G., Alroy, J., Wu, M., Py, B. F., Yuan, J., Deeney, J. T., Corkey, B. E., and Shirihai, O. S. (2008) Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 27, 433-446 (Pubitemid 351161653)
7. Gomes, L. C., and Scorrano, L. (2008) High levels of Fis1, a pro-fission mitochondrial protein, trigger autophagy. Biochim. Biophys. Acta 1777, 860-866
8. Gomes, L. C., Di Benedetto, G., and Scorrano, L. (2011) During autophagy mitochondria elongates are spared from degradation and sustain cell viability. Nat. Cell Biol. 13, 589-598
9. Narendra, D., Tanaka, A., Suen, D. F., and Youle, R. J. (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183, 795-803
10. Hailey, D. W., Rambold, A. S., Satpute-Krishnan, P., Mitra, K., Sougrat, R., Kim, P. K., and Lippincott-Schwartz, J. (2010) Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 141, 656-667
11. Bing, R. J., Siegel, A., Ungar, I., and Gilbert, M. (1954) Metabolism of the human heart. II. Studies on fat, ketone, and amino acid metabolism. Am. J. Med. 16, 504-515
12. Suzuki, S. W., Onodera, J., and Ohsumi, Y. (2011) Starvation-induced cell death in autophagy-defective yeast mutants is caused by mitochondria dysfunction. PLoS One 6, e17412
13. Chan, D. C. (2006) Mitochondria. Dynamic organelles in disease, aging, and development. Cell 125, 1241-1252
14. Karbowski, M., and Youle, R. J. (2003) Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ. 10, 870-880 (Pubitemid 36939697)
15. Yaffe, M. P. (1999) The machinery of mitochondrial inheritance and behavior. Science 283, 1493-1497
16. Birkedal, R., Shiels, H. A., and Vendelin, M. (2006) Three-dimensional mitochondrial arrangement in ventricular myocytes. From chaos to order. Am. J. Physiol. Cell Physiol. 291, C1148-C1158 (Pubitemid 44878585)
17. Kijima, K., Numakura, C., Izumino, H., Umetsu, K., Nezu, A., Shiiki, T., Ogawa, M., Ishizaki, Y., Kitamura, T., Shozawa, Y., and Hayasaka, K. (2005) Mitochondrial GTPase mitofusin 2 mutation in Charcot-Marie-Tooth neuropathy type 2A. Hum. Genet. 116, 23-27 (Pubitemid 40057912)
18. Züchner, S., Mersiyanova, I. V., Muglia, M., Bissar-Tadmouri, N., Rochelle, J., Dadali, E. L., Zappia, M., Nelis, E., Patitucci, A., Senderek, J., Parman, Y., Evgrafov, O., Jonghe, P. D., Takahashi, Y., Tsuji, S., Pericak-Vance, M. A., Quattrone, A., Battaloglu, E., Polyakov, A. V., Timmerman, V., Schröder, J. M., Vance, J. M., and Battologlu, E. (2004) Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat. Genet. 36, 449-451 (Pubitemid 38620027)
19. de Brito, O. M., and Scorrano, L. (2008) Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456, 605-610
20. Bach, D., Pich, S., Soriano, F. X., Vega, N., Baumgartner, B., Oriola, J., Daugaard, J. R., Lloberas, J., Camps, M., Zierath, J. R., Rabasa-Lhoret, R., Wallberg-Henriksson, H., Laville, M., Palacín, M., Vidal, H., Rivera, F., Brand, M., and Zorzano, A. (2003) Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism. A novel regulatory mechanism altered in obesity. J. Biol. Chem. 278, 17190-17197 (Pubitemid 36799599)
21. Chen, H., Vermulst, M., Wang, Y. E., Chomyn, A., Prolla, T. A., McCaffery, J. M., and Chan, D. C. (2010) Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 141, 280-289
22. Chen, K. H., Guo, X., Ma, D., Guo, Y., Li, Q., Yang, D., Li, P., Qiu, X., Wen, S., Xiao, R. P., and Tang, J. (2004) Dysregulation of HSG triggers vascular proliferative disorders. Nat. Cell Biol. 6, 872-883 (Pubitemid 39207252)
23. Shen, T., Zheng, M., Cao, C., Chen, C., Tang, J., Zhang, W., Cheng, H., Chen, K. H., and Xiao, R. P. (2007) Mitofusin-2 is a major determinant of oxidative stress-mediated heart muscle cell apoptosis. J. Biol. Chem. 282, 23354-23361 (Pubitemid 47311963)
24. Chen, H., Detmer, S. A., Ewald, A. J., Griffin, E. E., Fraser, S. E., and Chan, D. C. (2003) Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160, 189-200 (Pubitemid 36254953)
25. Chen, Y., Liu, Y., and Dorn, G. W., 2nd (2011) Mitochondrial fusion is essential for organelle function and cardiac homeostasis. Circ. Res. 109, 1327-1331
26. Papanicolaou, K. N., Khairallah, R. J., Ngoh, G. A., Chikando, A., Luptak, I., O'Shea, K. M., Riley, D. D., Lugus, J. J., Colucci, W. S., Lederer, W. J., Stanley, W. C., and Walsh, K. (2011) Mitofusin-2 maintains mitochondrial structure and contributes to stress-induced permeability transition in cardiac myocytes. Mol. Cell. Biol. 31, 1309-1328
27. Guo, X., Chen, K. H., Guo, Y., Liao, H., Tang, J., and Xiao, R. P. (2007) Mitofusin 2 triggers vascular smooth muscle cell apoptosis via mitochondrial death pathway. Circ. Res. 101, 1113-1122 (Pubitemid 350146437)
28. Zheng, M., and Xiao, R. P. (2010) Role of mitofusin 2 in cardiovascular oxidative injury. J. Mol. Med. 88, 987-991
29. Zheng, M., Cheng, H., Li, X., Zhang, J., Cui, L., Ouyang, K., Han, L., Zhao, T., Gu, Y., Dalton, N. D., Bang, M. L., Peterson, K. L., and Chen, J. (2009) Cardiac specific ablation of Cypher leads to a severe form of dilated cardiomyopathy with premature death. Hum. Mol. Genet. 18, 701-713
30. Cheng, H., Lederer, W. J., and Cannell, M. B. (1993) Calcium sparks. Elementary events underlying excitation-contraction coupling in heart muscle. Science 262, 740-744 (Pubitemid 23350693)
31. Amiott, E. A., Lott, P., Soto, J., Kang, P. B., McCaffery, J. M., DiMauro, S., Abel, E. D., Flanigan, K. M., Lawson, V. H., and Shaw, J. M. (2008) Mitochondrial fusion and function in Charcot-Marie-Tooth type 2A patient fibroblasts with mitofusin 2 mutations. Exp. Neurol. 211, 115-127
32. Tanhauser, S. M., and Laipis, P. J. (1995) Multiple deletions are detectable in mitochondrial DNA of aging mice. J. Biol. Chem. 270, 24769-24775
33. Wallace, D. C. (1999) Mitochondrial diseases in man and mouse. Science 283, 1482-1488
34. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., and Yoshimori, T. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728
35. Klionsky, D. J., Abeliovich, H., Agostinis, P., Agrawal, D. K., Aliev, G., Askew, D. S., Baba, M., Baehrecke, E. H., Bahr, B. A., Ballabio, A., Bamber, B. A., Bassham, D. C., Bergamini, E., Bi, X., Biard-Piechaczyk, M., Blum, J. S., Bredesen, D. E., Brodsky, J. L., Brumell, J. H., Brunk, U. T., Bursch, W., Camougrand, N., Cebollero, E., Cecconi, F., Chen, Y., Chin, L. S., Choi, A., Chu, C. T., Chung, J., Clarke, P. G., Clark, R. S., Clarke, S. G., Clavé, C., Cleveland, J. L., Codogno, P., Colombo, M. I., Coto-Montes, A., Cregg, J. M., Cuervo, A. M., Debnath, J., Demarchi, F., Dennis, P. B., Dennis, P. A., Deretic, V., Devenish, R. J., Di Sano, F., Dice, J. F., Difiglia, M., Dinesh-Kumar, S., Distelhorst, C. W., Djavaheri-Mergny, M., Dorsey, F. C., Droge, W., Dron, M., Dunn, W. A., Jr., Duszenko, M., Eissa, N. T., Elazar, Z., Esclatine, A., Eskelinen, E. L., Fesus, L., Finley, K. D., Fuentes, J. M., Fueyo, J., Fujisaki, K., Galliot, B., Gao, F. B., Gewirtz, D. A., Gibson, S. B., Gohla, A., Goldberg, A. L., Gonzalez, R., Gonzalez-Estevez, C., Gorski, S., Gottlieb, R. A., Haussinger, D., He, Y. W., Heidenreich, K., Hill, J. A., Hoyer-Hansen, M., Hu, X., Huang, W. P., Iwasaki, A., Jaattela, M., Jackson, W. T., Jiang, X., Jin, S., Johansen, T., Jung, J. U., Kadowaki, M., Kang, C., Kelekar, A., Kessel, D. H., Kiel, J. A., Kim, H. P., Kimchi, A., Kinsella, T. J., Kiselyov, K., Kitamoto, K., Knecht, E., Komatsu, M., Kominami, E., Kondo, S., Kovacs, A. L., Kroemer, G., Kuan, C. Y., Kumar, R., Kundu, M., Landry, J., Laporte, M., Le, W., Lei, H. Y., Lenardo, M. J., Levine, B., Lieberman, A., Lim, K. L., Lin, F. C., Liou, W., Liu, L. F., Lopez-Berestein, G., Lopez-Otin, C., Lu, B., Macleod, K. F., Malorni, W., Martinet, W., Matsuoka, K., Mautner, J., Meijer, A. J., Melendez, A., Michels, P., Miotto, G., Mistiaen, W. P., Mizushima, N., Mograbi, B., Monastyrska, I., Moore, M. N., Moreira, P. I., Moriyasu, Y., Motyl, T., Munz, C., Murphy, L. O., Naqvi, N. I., Neufeld, T. P., Nishino, I., Nixon, R. A., Noda, T., Nurnberg, B., Ogawa, M., Oleinick, N. L., Olsen, L. J., Ozpolat, B., Paglin, S., Palmer, G. E., Papassideri, I., Parkes, M., Perlmutter, D. H., Perry, G., Piacentini, M., Pinkas-Kramarski, R., Prescott, M., Proikas-Cezanne, T., Raben, N., Rami, A., Reggiori, F., Rohrer, B., Rubinsztein, D. C., Ryan, K. M., Sadoshima, J., Sakagami, H., Sakai, Y., Sandri, M., Sasakawa, C., Sass, M., Schneider, C., Seglen, P. O., Seleverstov, O., Settleman, J., Shacka, J. J., Shapiro, I. M., Sibirny, A., Silva-Zacarin, E. C., Simon, H. U., Simone, C., Simonsen, A., Smith, M. A., Spanel-Borowski, K., Srinivas, V., Steeves, M., Stenmark, H., Stromhaug, P. E., Subauste, C. S., Sugimoto, S., Sulzer, D., Suzuki, T., Swanson, M. S., Tabas, I., Takeshita, F., Talbot, N. J., Talloczy, Z., Tanaka, K., Tanida, I., Taylor, G. S., Taylor, J. P., Terman, A., Tettamanti, G., Thompson, C. B., Thumm, M., Tolkovsky, A. M., Tooze, S. A., Truant, R., Tumanovska, L. V., Uchiyama, Y., Ueno, T., Uzcategui, N. L., van der Klei, I., Vaquero, E. C., Vellai, T., Vogel, M. W., Wang, H. G., Webster, P., Wiley, J. W., Xi, Z., Xiao, G., Yahalom, J., Yang, J. M., Yap, G., Yin, X. M., Yoshimori, T., Yu, L., Yue, Z., Yuzaki, M., Zabirnyk, O., Zheng, X., Zhu, X., and Deter, R. L. (2008) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4, 151-175
36. Yorimitsu, T., and Klionsky, D. J. (2005) Autophagy. Molecular machinery for self-eating. Cell Death Differ. 12, Suppl. 2, 1542-1552
37. Bjørkøy, G., Lamark, T., Brech, A., Outzen, H., Perander, M., Overvatn, A., Stenmark, H., and Johansen, T. (2005) p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 171, 603-614 (Pubitemid 41668720)
38. Hamacher-Brady, A., Brady, N. R., Logue, S. E., Sayen, M. R., Jinno, M., Kirshenbaum, L. A., Gottlieb, R. A., and Gustafsson, A. B. (2007) Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ. 14, 146-157 (Pubitemid 44911902)
39. Ganley, I. G., Wong, P. M., Gammoh, N., and Jiang, X. (2011) Distinct autophagosomal-lysosomal fusion mechanism revealed by thapsigargin-induced autophagy arrest. Mol. Cell 42, 731-743
40. Gutierrez, M. G., Munafó, D. B., Berón, W., and Colombo, M. I. (2004) Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J. Cell Sci. 117, 2687-2697 (Pubitemid 38997252)
41. Jäger, S., Bucci, C., Tanida, I., Ueno, T., Kominami, E., Saftig, P., and Eskelinen, E. L. (2004) Role for Rab7 in maturation of late autophagic vacuoles. J. Cell Sci. 117, 4837-4848 (Pubitemid 39433449)
42. Pankiv, S., Alemu, E. A., Brech, A., Bruun, J. A., Lamark, T., Overvatn, A., Bjørkøy, G., and Johansen, T. (2010) FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport. J. Cell Biol. 188, 253-269
43. Rabinowitz, J. D., and White, E. (2010) Autophagy and metabolism. Science 330, 1344-1348
44. Singh, R., Kaushik, S., Wang, Y., Xiang, Y., Novak, I., Komatsu, M., Tanaka, K., Cuervo, A. M., and Czaja, M. J. (2009) Autophagy regulates lipid metabolism. Nature 458, 1131-1135
45. Inuzuka, Y., Okuda, J., Kawashima, T., Kato, T., Niizuma, S., Tamaki, Y., Iwanaga, Y., Yoshida, Y., Kosugi, R., Watanabe-Maeda, K., Machida, Y., Tsuji, S., Aburatani, H., Izumi, T., Kita, T., and Shioi, T. (2009) Suppression of phosphoinositide 3-kinase prevents cardiac aging in mice. Circulation 120, 1695-1703
46. Stroikin, Y., Dalen, H., Lööf, S., and Terman, A. (2004) Inhibition of autophagy with 3-methyladenine results in impaired turnover of lysosomes and accumulation of lipofuscin-like material. Eur. J. Cell Biol. 83, 583-590 (Pubitemid 40123822)
47. Terman, A., Dalen, H., Eaton, J. W., Neuzil, J., and Brunk, U. T. (2004) Aging of cardiac myocytes in culture. Oxidative stress, lipofuscin accumulation, and mitochondrial turnover. Ann. N.Y. Acad. Sci. 1019, 70-77 (Pubitemid 38951288)
48. Wang, X., Xie, W., Zhang, Y., Lin, P., Han, L., Han, P., Wang, Y., Chen, Z., Ji, G., Zheng, M., Weisleder, N., Xiao, R. P., Takeshima, H., Ma, J., and Cheng, H. (2010) Cardioprotection of ischemia/reperfusion injury by cholesterol-dependent MG53-mediated membrane repair. Circ. Res. 107, 76-83
49. Axe, E. L., Walker, S. A., Manifava, M., Chandra, P., Roderick, H. L., Habermann, A., Griffiths, G., and Ktistakis, N. T. (2008) Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J. Cell Biol. 182, 685-701
50. Hayashi-Nishino, M., Fujita, N., Noda, T., Yamaguchi, A., Yoshimori, T., and Yamamoto, A. (2009) A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat. Cell Biol. 11, 1433-1437
51. McEwan, D. G., and Dikic, I. (2010) Not all autophagy membranes are created equal. Cell 141, 564-566
52. Koshiba, T., Detmer, S. A., Kaiser, J. T., Chen, H., McCaffery, J. M., and Chan, D. C. (2004) Structural basis of mitochondrial tethering by mitofusin complexes. Science 305, 858-862 (Pubitemid 39038419)
53. Detmer, S. A., and Chan, D. C. (2007) Complementation between mouse Mfn1 and Mfn2 protects mitochondrial fusion defects caused by CMT2A disease mutations. J. Cell Biol. 176, 405-414
54. Papanicolaou, K. N., Ngoh, G. A., Dabkowski, E. R., O'Connell, K. A., Ribeiro, R. F., Stanley, W. C., and Walsh, K. (2011) Am. J. Physiol. Heart Circ. Physiol. 302, H167-H179
55. Agah, R., Frenkel, P. A., French, B. A., Michael, L. H., Overbeek, P. A., and Schneider, M. D. (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 (Pubitemid 27311255)
56. Minamisawa, S., Gu, Y., Ross, J., Jr., Chien, K. R., and Chen, J. (1999) A post-transcriptional compensatory pathway in heterozygous ventricular myosin light chain 2-deficient mice results in lack of gene dosage effect during normal cardiac growth or hypertrophy. J. Biol. Chem. 274, 10066-10070
57. Pich, S., Bach, D., Briones, P., Liesa, M., Camps, M., Testar, X., Palacín, M., and Zorzano, A. (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 (Pubitemid 40823451)
58. Matsui, Y., Takagi, H., Qu, X., Abdellatif, M., Sakoda, H., Asano, T., Levine, B., and Sadoshima, J. (2007) Distinct roles of autophagy in the heart during ischemia and reperfusion. Roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ. Res. 100, 914-922 (Pubitemid 46555697)
59. Sciarretta, S., Hariharan, N., Monden, Y., Zablocki, D., and Sadoshima, J. (2011) Is autophagy in response to ischemia and reperfusion protective or detrimental for the heart? Pediatr. Cardiol. 32, 275-281
60. Tanaka, Y., Guhde, G., Suter, A., Eskelinen, E. L., Hartmann, D., Lüllmann-Rauch, R., Janssen, P. M., Blanz, J., von Figura, K., and Saftig, P. (2000) Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature 406, 902-906 (Pubitemid 30664267)