Drp1-dependent mitochondrial fission via MiD49/51 is essential for apoptotic cristae remodeling

Journal of Cell Biology

Volumn 212, Issue 5, 2016, Pages 531-544

  Otera, Hidenori ^a   Miyata, Non ^b   Kuge, Osamu ^b   Mihara, Katsuyoshi ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C; DRP1 PROTEIN; DRP1 RECEPTOR MFF; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE OPA1; MID49 PROTEIN; MID51 PROTEIN; PROTEIN BAK; PROTEIN BAX; RECEPTOR; REGULATOR PROTEIN; UNCLASSIFIED DRUG; DNM1L PROTEIN, HUMAN; ELONGATION FACTOR; MICROTUBULE ASSOCIATED PROTEIN; MIEF1 PROTEIN, HUMAN; MIEF2 PROTEIN, HUMAN; MITOCHONDRIAL PROTEIN;

APOPTOSIS; APOPTOTIC CRISTAE REMODELING; ARTICLE; CELL DIVISION; CELL FRACTIONATION; CELL FUSION; COMPARATIVE STUDY; CONTROLLED STUDY; CRISPR CAS SYSTEM; ENZYME RELEASE; FEMALE; HCT116 CELL LINE; HELA CELL LINE; HUMAN; HUMAN CELL; MITOCHONDRIAL FISSION; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN STRUCTURE; CYTOPLASM; DEFICIENCY; METABOLISM; TUMOR CELL CULTURE;

APOPTOSIS; CYTOCHROMES C; CYTOPLASM; GTP PHOSPHOHYDROLASES; HELA CELLS; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PEPTIDE ELONGATION FACTORS; TUMOR CELLS, CULTURED;

EID: 84960428273     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201508099     Document Type: Article

References (43)

1. Anand, R., T. Wai, M.J. Baker, N. Kladt, A.C. Schauss, E. Rugarli, and T. Langer. 2014. The i-AAA protease YME1L and OMA1 cleave OPA1 to balance mitochondrial fusion and fission. J. Cell Biol. 204:919-929. http://dx.doi.org/10.1083/jcb.201308006
2. Baines, C.P., R.A. Kaiser, N.H. Purcell, N.S. Blair, H. Osinska, M.A. Hambleton, E.W. Brunskill, M.R. Sayen, R.A. Gottlieb, G.W. Dorn, et al. 2005. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature. 434:658-662. http://dx.doi.org/10.1038/nature03434
3. Bhuvanendran, S., K. Salka, K. Rainey, S.C. Sreetama, E. Williams, M. Leeker, V. Prasad, J. Boyd, G.H. Patterson, J.K. Jaiswal, and A.M. Colberg-Poley. 2014. Superresolution imaging of human cytomegalovirus vMIA localization in sub-mitochondrial compartments. Viruses. 6:1612-1636. http://dx.doi.org/10.3390/v6041612
4. Chipuk, J.E., G.P. McStay, A. Bharti, T. Kuwana, C.J. Clarke, L.J. Siskind, L.M. Obeid, and D.R. Green. 2012. Sphingolipid metabolism cooperates with BAK and BAX to promote the mitochondrial pathway of apoptosis. Cell. 148:988-1000. http://dx.doi.org/10.1016/j.cell.2012.01.038
5. Detmer, S.A., and D.C. Chan. 2007. Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell Biol. 8:870-879. http://dx.doi.org/10.1038/nrm2275
6. Elgass, K.D., E.A. Smith, M.A. LeGros, C.A. Larabell, and M.T. Ryan. 2015. Analysis of ER-mitochondria contacts using correlative fluorescence microscopy and soft X-ray tomography of mammalian cells. J. Cell Sci. 128:2795-2804. http://dx.doi.org/10.1242/jcs.169136
7. Frank, S., B. Gaume, E.S. Bergmann-Leitner, W.W. Leitner, E.G. Robert, F. Catez, C.L. Smith, and R.J. Youle. 2001. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell. 1:515-525. http://dx.doi.org/10.1016/S1534-5807(01)00055-7
8. 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
9. 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
10. Gandre-Babbe, S., and A.M. van der Bliek. 2008. The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells. Mol. Biol. Cell. 19:2402-2412. http://dx.doi.org/10.1091/mbc.E07-12-1287
11. Germain, M., J.P. Mathai, H.M. McBride, and G.C. Shore. 2005. Endoplasmic reticulum BIK initiates DRP1-regulated remodelling of mitochondrial cristae during apoptosis. EMBO J. 24:1546-1556. http://dx.doi.org/10.1038/sj.emboj.7600592
12. Guarani, V., E.M. McNeill, J.A. Paulo, E.L. Huttlin, F. Fröhlich, S.P. Gygi, D. Van Vactor, and J.W. Harper. 2015. QIL1 is a novel mitochondrial protein required for MIC OS complex stability and cristae morphology. eLife. 4:1-23. http://dx.doi.org/10.7554/eLife.06265
13. Huber, N., S. Guimaraes, M. Schrader, U. Suter, and A. Niemann. 2013. Charcot-Marie-Tooth disease-associated mutants of GDAP1 dissociate its roles in peroxisomal and mitochondrial fission. EMBO Rep. 14:545-552. http://dx.doi.org/10.1038/embor.2013.56
14. 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
15. James, D.I., and J.C. Martinou. 2008. Mitochondrial dynamics and apoptosis: a painful separation. Dev. Cell. 15:341-343. http://dx.doi.org/10.1016/j.devcel.2008.08.011
16. Jiang, X., H. Jiang, Z. Shen, and X. Wang. 2014. Activation of mitochondrial protease OMA1 by Bax and Bak promotes cytochrome c release during apoptosis. Proc. Natl. Acad. Sci. USA. 111:14782-14787. http://dx.doi.org/10.1073/pnas.1417253111
17. John, G.B., Y. Shang, L. Li, C. Renken, C.A. Mannella, J.M. Selker, L. Rangell, M.J. Bennett, and J. Zha. 2005. The mitochondrial inner membrane protein mitofilin controls cristae morphology. Mol. Biol. Cell. 16:1543-1554. http://dx.doi.org/10.1091/mbc.E04-08-0697
18. Koirala, S., Q. Guo, R. Kalia, H.T. Bui, D.M. Eckert, A. Frost, and J.M. Shaw. 2013. Interchangeable adaptors regulate mitochondrial dynamin assembly for membrane scission. Proc. Natl. Acad. Sci. USA. 110:E1342-E1351. http://dx.doi.org/10.1073/pnas.1300855110
19. Liu, T., R. Yu, S.B. Jin, L. Han, U. Lendahl, J. Zhao, and M. Nistér. 2013. The mitochondrial elongation factors MIEF1 and MIEF2 exert partially distinct functions in mitochondrial dynamics. Exp. Cell Res. 319:2893-2904. http://dx.doi.org/10.1016/j.yexcr.2013.07.010
20. Losón, O.C., Z. Song, H. Chen, and D.C. Chan. 2013. Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol. Biol. Cell. 24:659-667. http://dx.doi.org/10.1091/mbc.E12-10-0721
21. Losón, O.C., R. Liu, M.E. Rome, S. Meng, J.T. Kaiser, S.O. Shan, and D.C. Chan. 2014. The mitochondrial fission receptor MiD51 requires ADP as a cofactor. Structure. 22:367-377. http://dx.doi.org/10.1016/j.str.2014.01.001
22. Lucken-Ardjomande, S., S. Montessuit, and J.C. Martinou. 2008. Contributions to Bax insertion and oligomerization of lipids of the mitochondrial outer membrane. Cell Death Differ. 15:929-937. http://dx.doi.org/10.1038/cdd.2008.9
23. 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
24. Montessuit, S., S.P. Somasekharan, O. Terrones, S. Lucken-Ardjomande, S. Herzig, R. Schwarzenbacher, D.J. Manstein, E. Bossy-Wetzel, G. Basañez, P. Meda, and J.-C. Martinou. 2010. Membrane remodeling induced by the dynamin-related protein Drp1 stimulates Bax oligomerization. Cell. 142:889-901. http://dx.doi.org/10.1016/j.cell.2010.08.017
25. Nakagawa, T., S. Shimizu, T. Watanabe, O. Yamaguchi, K. Otsu, H. Yamagata, H. Inohara, T. Kubo, and Y. Tsujimoto. 2005. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature. 434:652-658. http://dx.doi.org/10.1038/nature03317
26. Norton, M., A.C. Ng, S. Baird, A. Dumoulin, T. Shutt, N. Mah, M.A. Andrade-Navarro, H.M. McBride, and R.A. Screaton. 2014. ROMO1 is an essential redox-dependent regulator of mitochondrial dynamics. Sci. Signal. 7:ra10. http://dx.doi.org/10.1126/scisignal.2004374
27. 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
28. Otera, H., C. Wang, M.M. Cleland, K. Setoguchi, S. Yokota, R.J. Youle, and K. Mihara. 2010. Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J. Cell Biol. 191:1141-1158. http://dx.doi.org/10.1083/jcb.201007152
29. 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
30. Palmer, C.S., K.D. Elgass, R.G. Parton, L.D. Osellame, D. Stojanovski, and M.T. Ryan. 2013. Adaptor proteins MiD49 and MiD51 can act independently of Mff and Fis1 in Drp1 recruitment and are specific for mitochondrial fission. J. Biol. Chem. 288:27584-27593. http://dx.doi.org/10.1074/jbc.M113.479873
31. Patten, D.A., J. Wong, M. Khacho, V. Soubannier, R.J. Mailloux, K. Pilon-Larose, J.G. MacLaurin, D.S. Park, H.M. McBride, L. Trinkle-Mulcahy, et al. 2014. OPA1-dependent cristae modulation is essential for cellular adaptation to metabolic demand. EMBO J. 33:2676-2691. http://dx.doi.org/10.15252/embj.201488349
32. Prudent, J., R. Zunino, A. Sugiura, S. Mattie, G.C. Shore, and H.M. McBride. 2015. MAPL SUMOylation of Drp1 Stabilizes an ER/Mitochondrial Platform Required for Cell Death. Mol. Cell. 59:941-955. http://dx.doi.org/10.1016/j.molcel.2015.08.001
33. Richter, V., C.S. Palmer, L.D. Osellame, A.P. Singh, K. Elgass, D.A. Stroud, H. Sesaki, M. Kvansakul, and M.T. Ryan. 2014. Structural and functional analysis of MiD51, a dynamin receptor required for mitochondrial fission. J. Cell Biol. 204:477-486. http://dx.doi.org/10.1083/jcb.201311014
34. Scorrano, L. 2009. Opening the doors to cytochrome c: changes in mitochondrial shape and apoptosis. Int. J. Biochem. Cell Biol. 41:1875-1883. http://dx.doi.org/10.1016/j.biocel.2009.04.016
35. Sesaki, H., S.M. Southard, M.P. Yaffe, and R.E. Jensen. 2003. Mgm1p, a dynamin-related GTPase, is essential for fusion of the mitochondrial outer membrane. Mol. Biol. Cell. 14:2342-2356. http://dx.doi.org/10.1091/mbc.E02-12-0788
36. Setoguchi, K., H. Otera, and K. Mihara. 2006. Cytosolic factor- and TOMindependent import of C-tail-anchored mitochondrial outer membrane proteins. EMBO J. 25:5635-5647. http://dx.doi.org/10.1038/sj.emboj.7601438
37. Suen, D.F., K.L. Norris, and R.J. Youle. 2008. Mitochondrial dynamics and apoptosis. Genes Dev. 22:1577-1590. http://dx.doi.org/10.1101/gad.1658508
38. 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. http://dx.doi.org/10.1038/nrm2952
39. Varanita, T., M.E. Soriano, V. Romanello, T. Zaglia, R. Quintana-Cabrera, M. Semenzato, R. Menabò, V. Costa, G. Civiletto, P. Pesce, et al. 2015. The OPA1-dependent mitochondrial cristae remodeling pathway controls atrophic, apoptotic, and ischemic tissue damage. Cell Metab. 21:834-844. http://dx.doi.org/10.1016/j.cmet.2015.05.007
40. Wasiak, S., R. Zunino, and H.M. McBride. 2007. Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J. Cell Biol. 177:439-450. http://dx.doi.org/10.1083/jcb.200610042
41. Yagita, Y., T. Hiromasa, and Y. Fujiki. 2013. Tail-anchored PEX26 targets peroxisomes via a PEX19-dependent and TRC40-independent class I pathway. J. Cell Biol. 200:651-666. http://dx.doi.org/10.1083/jcb.201211077
42. Yang, R.F., G.W. Zhao, S.T. Liang, Y. Zhang, L.H. Sun, H.Z. Chen, and D.P. Liu. 2012. Mitofilin regulates cytochrome c release during apoptosis by controlling mitochondrial cristae remodeling. Biochem. Biophys. Res. Commun. 428:93-98. http://dx.doi.org/10.1016/j.bbrc.2012.10.012
43. 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