Drp1, Mff, Fis1, and MiD51 are coordinated to mediate mitochondrial fission during UV irradiation-induced apoptosis

FASEB Journal

Volumn 30, Issue 1, 2016, Pages 466-476

  Zhang, Zhenzhen ^a   Liu, Lei ^a   Wu, Shengnan ^a   Xing, Da ^a  

^a SOUTH CHINA NORMAL UNIVERSITY   (China)

Author keywords

Bax; GTP binding; MIEF1; Mitochondrial fragmentation; Oligomerization

Indexed keywords

COMPLEMENTARY DNA; DYNAMIN RELATED PROTEIN 1; MITOCHONDRIAL DYNAMICS OF 51 KDA PROTEIN; MITOCHONDRIAL FISSION FACTOR; MITOCHONDRIAL FISSION PROTEIN 1; OUTER MEMBRANE PROTEIN; SERINE; UNCLASSIFIED DRUG; DYNAMIN; ELONGATION FACTOR; FIS1 PROTEIN, HUMAN; MEMBRANE PROTEIN; MIEF1 PROTEIN, HUMAN; MITOCHONDRIAL PROTEIN; PROTEIN BINDING;

APOPTOSIS; ARTICLE; CELL FRACTIONATION; CELLULAR DISTRIBUTION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CROSS LINKING; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL FISSION; MITOCHONDRION; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; ULTRAVIOLET IRRADIATION; WESTERN BLOTTING; GENETICS; METABOLISM; PHOSPHORYLATION; RADIATION RESPONSE; TUMOR CELL LINE; ULTRAVIOLET RADIATION;

APOPTOSIS; CELL LINE, TUMOR; DYNAMINS; HUMANS; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; PEPTIDE ELONGATION FACTORS; PHOSPHORYLATION; PROTEIN BINDING; ULTRAVIOLET RAYS;

EID: 84973449037     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-274258     Document Type: Article

References (45)

1. Chan, D. C. (2006) Mitochondria: dynamic organelles in disease, aging, and development. Cell 125, 1241-1252
2. Youle, R. J., and van der Bliek, A. M. (2012) Mitochondrial fission, fusion, and stress. Science 337, 1062-1065
3. Chan, D. C. (2012) Fusion and fission: interlinked processes critical for mitochondrial health. Annu. Rev. Genet. 46, 265-287
4. Archer, S. L. (2013) Mitochondrial dynamics: mitochondrial fission and fusion in human diseases. N. Engl. J. Med. 369, 2236-2251
5. Liesa, M., Palacín, M., and Zorzano, A. (2009) Mitochondrial dynamics in mammalian health and disease. Physiol. Rev. 89, 799-845
6. James, D. I., Parone, P. A., Mattenberger, Y., and Martinou, J. C. (2003) hFis1, a novel component of the mammalian mitochondrial fission machinery. J. Biol. Chem. 278, 36373-36379
7. Stojanovski, D., Koutsopoulos, O. S., Okamoto, K., and Ryan, M. T. (2004) Levels of human Fis1 at the mitochondrial outer membrane regulate mitochondrial morphology. J. Cell Sci. 117, 1201-1210
8. Yoon, Y., Krueger, E. W., Oswald, B. J., and McNiven, M. A. (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
9. Gandre-Babbe, S., and van der Bliek, A. M. (2008) The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells. Mol. Biol. Cell 19, 2402-2412
10. Otera, H., Wang, C., Cleland, M. M., Setoguchi, K., Yokota, S., Youle, R. J., and Mihara, K. (2010) Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J. Cell Biol. 191, 1141-1158
11. Zhao, J., Liu, T., Jin, S., Wang, X., Qu, M., Uhlén, P., Tomilin, N., Shupliakov, O., Lendahl, U., and Nistér, M. (2011) Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission. EMBO J. 30, 2762-2778
12. Palmer, C. S., Osellame, L. D., Laine, D., Koutsopoulos, O. S., Frazier, A. E., and Ryan, M. T. (2011) MiD49 and MiD51, new components of the mitochondrial fission machinery. EMBO Rep. 12, 565-573
13. Hoppins, S., Lackner, L., and Nunnari, J. (2007) The machines that divide and fuse mitochondria. Annu. Rev. Biochem. 76, 751-780
14. Yu, T., Fox, R. J., Burwell, L. S., and Yoon, Y. (2005) Regulation of mitochondrial fission and apoptosis by the mitochondrial outer membrane protein hFis1. J. Cell Sci. 118, 4141-4151
15. Lee, Y. J., Jeong, S. Y., Karbowski, M., Smith, C. L., and Youle, R. J. (2004) Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol. Biol. Cell 15, 5001-5011
16. Losón, O. C., Song, Z., Chen, H., and Chan, D. C. (2013) Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol. Biol. Cell 24, 659-667
17. Losón, O. C., Liu, R., Rome, M. E., Meng, S., Kaiser, J. T., Shan, S. O., and Chan, D. C. (2014) The mitochondrial fission receptor MiD51 requires ADP as a cofactor. Structure 22, 367-377
18. Palmer, C. S., Elgass, K. D., Parton, R. G., Osellame, L. D., Stojanovski, D., and Ryan, M. T. (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
19. Cribbs, J. T., and Strack, S. (2007) Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep. 8, 939-944
20. Taguchi, N., Ishihara, N., Jofuku, A., Oka, T., and Mihara, K. (2007) Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J. Biol. Chem. 282, 11521-11529
21. Cereghetti, G. M., Stangherlin, A., Martins de Brito, O., Chang, C. R., Blackstone, C., Bernardi, P., and Scorrano, L. (2008) Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc. Natl. Acad. Sci. USA 105, 15803-15808
22. Wasiak, S., Zunino, R., and McBride, H. M. (2007) Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J. Cell Biol. 177, 439-450
23. Karbowski, M., Neutzner, A., and Youle, R. J. (2007) The mitochondrial E3 ubiquitin ligase MARCH5 is required for Drp1 dependent mitochondrial division. J. Cell Biol. 178, 71-84
24. Wang, H., Song, P., Du, L., Tian, W., Yue, W., Liu, M., Li, D., Wang, B., Zhu, Y., Cao, C., Zhou, J., and Chen, Q. (2011) Parkin ubiquitinates Drp1 for proteasome-dependent degradation: implication of dysregulated mitochondrial dynamics in Parkinson disease. J. Biol. Chem. 286, 11649-11658
25. Suen, D. F., Norris, K. L., and Youle, R. J. (2008) Mitochondrial dynamics and apoptosis. Genes Dev. 22, 1577-1590
26. Brooks, C., Wei, Q., Feng, L., Dong, G., Tao, Y., Mei, L., Xie, Z. J., and Dong, Z. (2007) Bak regulates mitochondrial morphology and pathology during apoptosis by interacting with mitofusins. Proc. Natl. Acad. Sci. USA 104, 11649-11654
27. Karbowski, M., Norris, K. L., Cleland, M. M., Jeong, S. Y., and Youle, R. J. (2006) Role of Bax and Bak in mitochondrial morphogenesis. Nature 443, 658-662
28. Frank, S., Gaume, B., Bergmann-Leitner, E. S., Leitner, W. W., Robert, E. G., Catez, F., Smith, C. L., and Youle, R. J. (2001) The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 1, 515-525
29. Karbowski, M., Lee, Y. J., Gaume, B., Jeong, S. Y., Frank, S., Nechushtan, A., Santel, A., Fuller, M., Smith, C. L., and Youle, R. J. (2002) Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J. Cell Biol. 159, 931-938
30. Cassidy-Stone, A., Chipuk, J. E., Ingerman, E., Song, C., Yoo, C., Kuwana, T., Kurth, M. J., Shaw, J. T., Hinshaw, J. E., Green, D. R., and Nunnari, J. (2008) Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev. Cell 14, 193-204
31. Montessuit, S., Somasekharan, S. P., Terrones, O., Lucken-Ardjomande, S., Herzig, S., Schwarzenbacher, R., Manstein, D. J., Bossy-Wetzel, E., Basañez, G., Meda, P., and Martinou, J. C. (2010) Membrane remodeling induced by the dynamin-related protein Drp1 stimulates Bax oligomerization. Cell 142, 889-901
32. Roucou, X., Montessuit, S., Antonsson, B., and Martinou, J. C. (2002) Bax oligomerization in mitochondrial membranes requires tBid (caspase-8-cleaved Bid) and a mitochondrial protein. Biochem. J. 368, 915-921
33. Wang, X., Xing, D., Liu, L., and Chen, W. R. (2009) BimL directly neutralizes Bcl-xL to promote Bax activation during UV-induced apoptosis. FEBS Lett. 583, 1873-1879
34. Zhang, Y., Xing, D., and Liu, L. (2009) PUMA promotes Bax translocation by both directly interacting with Bax and by competitive binding to Bcl-X L during UV-induced apoptosis. Mol. Biol. Cell 20, 3077-3087
35. Koopman, W. J., Distelmaier, F., Esseling, J. J., Smeitink, J. A., and Willems, P. H. (2008) Computer-assisted live cell analysis of mitochondrial membrane potential, morphology and calcium handling. Methods 46, 304-311
36. Li, Q., Lau, A., Morris, T. J., Guo, L., Fordyce, C. B., and Stanley, E. F. (2004) A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J. Neurosci. 24, 4070-4081
37. Zhu, P. P., Patterson, A., Stadler, J., Seeburg, D. P., Sheng, M., and Blackstone, C. (2004) Intra- and intermolecular domain interactions of the C-terminal GTPase effector domain of the multimeric dynamin-like GTPase Drp1. J. Biol. Chem. 279, 35967-35974
38. Hájek, P., Chomyn, A., and Attardi, G. (2007) Identification of a novel mitochondrial complex containing mitofusin 2 and stomatin-like protein 2. J. Biol. Chem. 282, 5670-5681
39. Wang, J. X., Li, Q., and Li, P. F. (2009) Apoptosis repressor with caspase recruitment domain contributes to chemotherapy resistance by abolishing mitochondrial fission mediated by dynamin-related protein-1. Cancer Res. 69, 492-500
40. Liu, L., Zhang, Z., and Xing, D. (2011) Cell death via mitochondrial apoptotic pathway due to activation of Bax by lysosomal photodamage. Free Radic. Biol. Med. 51, 53-68
41. Sheridan, C., Delivani, P., Cullen, S. P., and Martin, S. J. (2008) Baxor Bak-induced mitochondrial fission can be uncoupled from cytochrome C release. Mol. Cell 31, 570-585
42. Wu, S., Zhou, F., Zhang, Z., and Xing, D. (2011) Bax is essential for Drp1-mediated mitochondrial fission but not for mitochondrial outer membrane permeabilization caused by photodynamic therapy. J. Cell. Physiol. 226, 530-541
43. Wakabayashi, J., Zhang, Z., Wakabayashi, N., Tamura, Y., Fukaya, M., Kensler, T. W., Iijima, M., and Sesaki, H. (2009) The dynamin-related GTPase Drp1 is required for embryonic and brain development in mice. J. Cell Biol. 186, 805-816
44. Rappold, P. M., Cui, M., Grima, J. C., Fan, R. Z., de Mesy-Bentley, K. L., Chen, L., Zhuang, X., Bowers, W. J., and Tieu, K. (2014) Drp1 inhibition attenuates neurotoxicity and dopamine release deficits in vivo. Nat. Commun. 5, 5244
45. Otera, H., Ishihara, N., and Mihara, K. (2013) New insights into the function and regulation of mitochondrial fission. Biochim. Biophys. Acta 1833, 1256-1268