The i-AAA protease YME1L and OMA1 cleave OPA1 to balance mitochondrial fusion and fission

Journal of Cell Biology

Volumn 204, Issue 6, 2014, Pages 919-929

  Anand, Ruchika ^a   Wai, Timothy ^a   Baker, Michael J ^a   Kladt, Nikolay ^b   Schauss, Astrid C ^b   Rugarli, Elena ^a,b   Langer, Thomas ^a,b,c  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ISOPROTEIN; OMA1 ENZYME; OPA1 ENZYME; PROTEINASE; UNCLASSIFIED DRUG; YME1L ENZYME;

ANIMAL CELL; APOPTOTIC RESISTANCE; ARTICLE; CELL DIVISION; CELL ULTRASTRUCTURE; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CONTROLLED STUDY; CRISTAE MORPHOGENESIS; EMBRYO; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOCHONDRIAL FISSION; MITOCHONDRIAL FRAGMENTATION; MITOCHONDRIAL FUSION; MITOCHONDRIAL TUBULATION; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING;

ANIMALS; APOPTOSIS; GTP PHOSPHOHYDROLASES; HEK293 CELLS; HUMANS; METALLOENDOPEPTIDASES; METALLOPROTEASES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; MITOCHONDRIAL SIZE; ORGANELLE SHAPE; PROTEIN SUBUNITS; PROTEIN TRANSPORT;

EID: 84896264348     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201308006     Document Type: Article

References (52)

1. Alexander, C., M. Votruba, U.E. Pesch, D.L. Thiselton, S. Mayer, A. Moore, M. Rodriguez, U. Kellner, B. Leo-Kottler, G. Auburger, et al. 2000. OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat. Genet. 26:211-215. http://dx.doi.org/10.1038/79944
2. Baricault, L., B. Ségui, L. Guégand, A. Olichon, A. Valette, F. Larminat, and G. Lenaers. 2007. OPA1 cleavage depends on decreased mitochondrial ATP level and bivalent metals. Exp. Cell Res. 313:3800-3808. http://dx.doi .org/10.1016/j.yexcr.2007.08.008
3. Cagalinec, M., D. Safiulina, M. Liiv, J. Liiv, V. Choubey, P. Wareski, V. Veksler, and A. Kaasik. 2013. Principles of the mitochondrial fusion and fission cycle in neurons. J. Cell Sci. 126:2187-2197. http://dx.doi .org/10.1242/jcs.118844
4. Chan, D.C. 2012. Fusion and fission: interlinked processes critical for mitochondrial health. Annu. Rev. Genet. 46:265-287. http://dx.doi.org/10 .1146/annurev-genet-110410-132529
5. 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. USA. 101:15927-15932. http://dx.doi.org/10.1073/pnas.0407043101
6. Cipolat, S., T. Rudka, D. Hartmann, V. Costa, L. Serneels, K. Craessaerts, K. Metzger, C. Frezza, W. Annaert, L. D'Adamio, et al. 2006. Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling. Cell. 126:163-175. http://dx.doi.org/10 .1016/j.cell.2006.06.021
7. Delettre, C., G. Lenaers, J.M. Griffoin, N. Gigarel, C. Lorenzo, P. Belenguer, L. Pelloquin, J. Grosgeorge, C. Turc-Carel, E. Perret, et al. 2000. Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat. Genet. 26:207-210. http://dx.doi .org/10.1038/79936
8. Delettre, C., J.M. Griffoin, J. Kaplan, H. Dollfus, B. Lorenz, L. Faivre, G. Lenaers, P. Belenguer, and C.P. Hamel. 2001. Mutation spectrum and splicing variants in the OPA1 gene. Hum. Genet. 109:584-591. http:// dx.doi.org/10.1007/s00439-001-0633-y
9. DeVay, R.M., L. Dominguez-Ramirez, L.L. Lackner, S. Hoppins, H. Stahlberg, and J. Nunnari. 2009. Coassembly of Mgm1 isoforms requires cardiolipin and mediates mitochondrial inner membrane fusion. J. Cell Biol. 186:793-803. http://dx.doi.org/10.1083/jcb.200906098
10. Duvezin-Caubet, S., R. Jagasia, J. Wagener, S. Hofmann, A. Trifunovic, A. Hansson, A. Chomyn, M.F. Bauer, G. Attardi, N.G. Larsson, et al. 2006. Proteolytic processing of OPA1 links mitochondrial dysfunction to alterations in mitochondrial morphology. J. Biol. Chem. 281:37972-37979. http://dx.doi.org/10.1074/jbc.M606059200
11. Ehses, S., I. Raschke, G. Mancuso, A. Bernacchia, S. Geimer, D. Tondera, J.-C. Martinou, B. Westermann, E.I. Rugarli, and T. Langer. 2009. Regulation of OPA1 processing and mitochondrial fusion by m-AAA protease isoenzymes and OMA1. J. Cell Biol. 187:1023-1036. http://dx.doi.org/10 .1083/jcb.200906084
12. Escobar-Henriques, M., and F. Anton. 2013. Mechanistic perspective of mitochondrial fusion: tubulation vs. fragmentation. Biochim. Biophys. Acta. 1833:162-175. http://dx.doi.org/10.1016/j.bbamcr.2012.07.016
13. Frezza, C., S. Cipolat, O. Martins de Brito, M. Micaroni, G.V. Beznoussenko, T. Rudka, D. Bartoli, R.S. Polishuck, N.N. Danial, B. De Strooper, and L. Scorrano. 2006. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell. 126:177-189. http://dx.doi.org/ 10.1016/j.cell.2006.06.025
14. Friedman, J.R., L.L. Lackner, M. West, J.R. DiBenedetto, J. Nunnari, and G.K. Voeltz. 2011. ER tubules mark sites of mitochondrial division. Science. 334:358-362. http://dx.doi.org/10.1126/science.1207385
15. Griparic, L., T. Kanazawa, and A.M. van der Bliek. 2007. Regulation of the mitochondrial dynamin-like protein Opa1 by proteolytic cleavage. J. Cell Biol. 178:757-764. http://dx.doi.org/10.1083/jcb.200704112
16. Guillery, O., F. Malka, T. Landes, E. Guillou, C. Blackstone, A. Lombès, P. Belenguer, D. Arnoult, and M. Rojo. 2008. Metalloprotease-mediated OPA1 processing is modulated by the mitochondrial membrane potential. Biol. Cell. 100:315-325. http://dx.doi.org/10.1042/BC20070110
17. Head, B., L. Griparic, M. Amiri, S. Gandre-Babbe, and A.M. van der Bliek. 2009. Inducible proteolytic inactivation of OPA1 mediated by the OMA1 protease in mammalian cells. J. Cell Biol. 187:959-966. http://dx.doi .org/10.1083/jcb.200906083
18. Ishihara, N., Y. Fujita, T. Oka, and K. Mihara. 2006. Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J. 25:2966-2977. http://dx.doi.org/10.1038/sj.emboj.7601184
19. Itoh, K., K. Nakamura, M. Iijima, and H. Sesaki. 2013. Mitochondrial dynamics in neurodegeneration. Trends Cell Biol. 23:64-71. http://dx.doi.org/10 .1016/j.tcb.2012.10.006
20. Knott, A.B., and E. Bossy-Wetzel. 2008. Impairing the mitochondrial fission and fusion balance: a new mechanism of neurodegeneration. Ann. N. Y. Acad. Sci. 1147:283-292. http://dx.doi.org/10.1196/annals.1427.030
21. Lee, Y.J., S.Y. Jeong, M. Karbowski, C.L. Smith, and R.J. Youle. 2004. Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol. Biol. Cell. 15:5001-5011. http://dx.doi.org/ 10.1091/mbc.E04-04-0294
22. Liesa, M., and O.S. Shirihai. 2013. Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab. 17:491-506. http://dx.doi.org/10.1016/j.cmet.2013.03.002
23. Liu, X., D. Weaver, O. Shirihai, and G. Hajnóczky. 2009. Mitochondrial 'kiss-andrun': interplay between mitochondrial motility and fusion-fission dynamics. EMBO J. 28:3074-3089. http://dx.doi.org/10.1038/emboj.2009.255
24. Meeusen, S., R. DeVay, J. Block, A. Cassidy-Stone, S. Wayson, J.M. McCaffery, and J. Nunnari. 2006. Mitochondrial inner-membrane fusion and crista maintenance requires the dynamin-related GTPase Mgm1. Cell. 127:383-395. http://dx.doi.org/10.1016/j.cell.2006.09.021
25. Merkwirth, C., S. Dargazanli, T. Tatsuta, S. Geimer, B. Löwer, F.T. Wunderlich, J.C. von Kleist-Retzow, A. Waisman, B. Westermann, and T. Langer. 2008. Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev. 22:476-488. http://dx.doi.org/10.1101/gad.460708
26. Müller-Rischart, A.K., A. Pilsl, P. Beaudette, M. Patra, K. Hadian, M. Funke, R. Peis, A. Deinlein, C. Schweimer, P.H. Kuhn, et al. 2013. The E3 ligase parkin maintains mitochondrial integrity by increasing linear ubiquitination of NEMO. Mol. Cell. 49:908-921. http://dx.doi.org/10.1016/j.molcel .2013.01.036
27. Murley, A., L.L. Lackner, C. Osman, M. West, G.K. Voeltz, P. Walter, and J. Nunnari. 2013. ER-associated mitochondrial division links the distribution of mitochondria and mitochondrial DNA in yeast. Elife. 2:e00422. http://dx.doi.org/10.7554/eLife.00422
28. Nunnari, J., and A. Suomalainen. 2012. Mitochondria: in sickness and in health. Cell. 148:1145-1159. http://dx.doi.org/10.1016/j.cell.2012.02.035
29. Olichon, A., L. Baricault, N. Gas, E. Guillou, A. Valette, P. Belenguer, and G. Lenaers. 2003. Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis. J. Biol. Chem. 278:7743-7746. http://dx.doi.org/10.1074/jbc .C200677200
30. Olichon, A., G. Elachouri, L. Baricault, C. Delettre, P. Belenguer, and G. Lenaers. 2007. OPA1 alternate splicing uncouples an evolutionary conserved function in mitochondrial fusion from a vertebrate restricted function in apoptosis. Cell Death Differ. 14:682-692. http://dx.doi.org/10 .1038/sj.cdd.4402048
31. Otera, H., N. Ishihara, and K. Mihara. 2013. New insights into the function and regulation of mitochondrial fission. Biochim. Biophys. Acta. 1833:1256-1268. http://dx.doi.org/10.1016/j.bbamcr.2013.02.002
32. Palmer, C.S., L.D. Osellame, D. Laine, O.S. Koutsopoulos, A.E. Frazier, and M.T. Ryan. 2011. MiD49 and MiD51, new components of the mitochondrial fission machinery. EMBO Rep. 12:565-573. http://dx.doi.org/10 .1038/embor.2011.54
33. Quirós, P.M., A.J. Ramsay, D. Sala, E. Fernández-Vizarra, F. Rodríguez, J.R. Peinado, M.S. Fernández-García, J.A. Vega, J.A. Enríquez, A. Zorzano, and C. López-Otín. 2012. Loss of mitochondrial protease OMA1 alters processing of the GTPase OPA1 and causes obesity and defective thermogenesis in mice. EMBO J. 31:2117-2133. http://dx.doi.org/ 10.1038/emboj.2012.70
34. + memory T cells is prone to accelerated apoptosis that is prevented by interleukin-15 (IL-15). Cell Death Differ. 8:395-402. http://dx.doi.org/10.1038/sj.cdd.4400825
35. Ruan, Y., H. Li, K. Zhang, F. Jian, J. Tang, and Z. Song. 2013. Loss of Yme1L perturbates mitochondrial dynamics. Cell Death Dis. 4:e896. http://dx .doi.org/10.1038/cddis.2013.414
36. Schneider, C.A., W.S. Rasband, and K.W. Eliceiri. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods. 9:671-675. http://dx.doi.org/ 10.1038/nmeth.2089
37. Sesaki, H., and R.E. Jensen. 1999. Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J. Cell Biol. 147:699-706. http://dx.doi.org/10.1083/jcb.147.4.699
38. 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. http://dx.doi.org/10.1091/ mbc.12.8.2245
39. Song, Z., H. Chen, M. Fiket, C. Alexander, and D.C. Chan. 2007. OPA1 processing controls mitochondrial fusion and is regulated by mRNA splicing, membrane potential, and Yme1L. J. Cell Biol. 178:749-755. http://dx .doi.org/10.1083/jcb.200704110
40. Stiburek, L., J. Cesnekova, O. Kostkova, D. Fornuskova, K. Vinsova, L. Wenchich, J. Houstek, and J. Zeman. 2012. YME1L controls the accumulation of respiratory chain subunits and is required for apoptotic resistance, cristae morphogenesis, and cell proliferation. Mol. Biol. Cell. 23:1010-1023. http://dx.doi.org/10.1091/mbc.E11-08-0674
41. Tamura, Y., K. Itoh, and H. Sesaki. 2011. SnapShot: Mitochondrial dynamics. Cell. 145:1158-1158: e1. http://dx.doi.org/10.1016/j.cell.2011.06.018
42. Tondera, D., S. Grandemange, A. Jourdain, M. Karbowski, Y. Mattenberger, S. Herzig, S. Da Cruz, P. Clerc, I. Raschke, C. Merkwirth, et al. 2009. SLP-2 is required for stress-induced mitochondrial hyperfusion. EMBO J. 28:1589-1600. http://dx.doi.org/10.1038/emboj.2009.89
43. Twig, G., A. Elorza, A.J. Molina, H. Mohamed, J.D. Wikstrom, G. Walzer, L. Stiles, S.E. Haigh, S. Katz, G. Las, et al. 2008. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 27:433-446. http://dx.doi.org/10.1038/sj.emboj.7601963
44. van der Bliek, A.M., Q. Shen, and S. Kawajiri. 2013. Mechanisms of mitochondrial fission and fusion. Cold Spring Harb. Perspect. Biol. 5:a011072. http://dx.doi.org/10.1101/cshperspect.a011072
45. Wakabayashi, J., Z. Zhang, N. Wakabayashi, Y. Tamura, M. Fukaya, T.W. Kensler, M. Iijima, and H. Sesaki. 2009. The dynamin-related GTPase Drp1 is required for embryonic and brain development in mice. J. Cell Biol. 186:805-816. http://dx.doi.org/10.1083/jcb.200903065
46. Wang, S., W. Xiao, S. Shan, C. Jiang, M. Chen, Y. Zhang, S. Lü, J. Chen, C. Zhang, Q. Chen, and M. Long. 2012. Multi-patterned dynamics of mitochondrial fission and fusion in a living cell. PLoS ONE. 7:e19879. http:// dx.doi.org/10.1371/journal.pone.0019879
47. Westermann, B. 2010. Mitochondrial fusion and fission in cell life and death. Nat. Rev. Mol. Cell Biol. 11:872-884. http://dx.doi.org/10.1038/nrm3013
48. Yamaguchi, R., L. Lartigue, G. Perkins, R.T. Scott, A. Dixit, Y. Kushnareva, T. Kuwana, M.H. Ellisman, and D.D. Newmeyer. 2008. Opa1-mediated cristae opening is Bax/Bak and BH3 dependent, required for apoptosis, and independent of Bak oligomerization. Mol. Cell. 31:557-569. http:// dx.doi.org/10.1016/j.molcel.2008.07.010
49. Youle, R.J., and A.M. van der Bliek. 2012. Mitochondrial fission, fusion, and stress. Science. 337:1062-1065. http://dx.doi.org/10.1126/science .1219855
50. Zhao, J., T. Liu, S. Jin, X. Wang, M. Qu, P. Uhlén, N. Tomilin, O. Shupliakov, U. Lendahl, and M. Nistér. 2011. Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission. EMBO J. 30:2762-2778. http://dx.doi.org/10.1038/ emboj.2011.198
51. Zick, M., S. Duvezin-Caubet, A. Schäfer, F. Vogel, W. Neupert, and A.S. Reichert. 2009. Distinct roles of the two isoforms of the dynamin-like GTPase Mgm1 in mitochondrial fusion. FEBS Lett. 583:2237-2243. http://dx.doi.org/10.1016/j.febslet.2009.05.053
52. Zunino, R., A. Schauss, P. Rippstein, M. Andrade-Navarro, and H.M. McBride. 2007. The SUMO protease SENP5 is required to maintain mitochondrial morphology and function. J. Cell Sci. 120:1178-1188. http://dx.doi.org/ 10.1242/jcs.03418