The mitochondrial E3 ubiquitin ligase MARCH5 is required for Drp1 dependent mitochondrial division

Journal of Cell Biology

Volumn 178, Issue 1, 2007, Pages 71-84

  Karbowski, Mariusz ^a,b   Neutzner, Albert ^a   Youle, Richard J ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN I; FACTOR FOR INVERSION STIMULATION; GUANOSINE TRIPHOSPHATASE; MEMBRANE ASSOCIATED RING FINGER (C3HC4) 5 PROTEIN; MUTANT PROTEIN; RNA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CELL DIVISION; CELL ELONGATION; CELL MOTILITY; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; MITOCHONDRION; MOLECULAR INTERACTION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN INTERACTION; RNA INTERFERENCE; WILD TYPE;

GREEN FLUORESCENT PROTEINS; GTP PHOSPHOHYDROLASES; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUTATION; PROTEIN STRUCTURE, TERTIARY; RNA INTERFERENCE; UBIQUITIN-PROTEIN LIGASES;

EID: 34347398050     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200611064     Document Type: Article

References (49)

1. Bartee, E., M. Mansouri, B.T. Hovey Nerenberg, K. Gouveia, and K. Fruh. 2004. Downregulation of major histocompatibility complex class I by human ubiquitin ligases related to viral immune evasion proteins. J. Virol. 78:1109-1120.
2. Bhar, D., M.A. Karren, M. Babst, and J.M. Shaw. 2006. Dimeric Dnm1-G385D interacts with Mdv1 on mitochondria and can be stimulated to assemble into fission complexes containing Mdv1 and Fis1. J. Biol. Chem. 281:17312-17320.
3. Bleazard, W., J.M. McCaffery, E.J. King, S. Bale, A. Mozdy, Q. Tieu, J. Nunnari, and J.M. Shaw. 1999. The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat. Cell Biol. 1:298-304.
4. Bottomley, M.J., G. Stier, D. Pennacchini, G. Legube, B. Simon, A. Akhtar, M. Sattler, and G. Musco. 2005. NMR structure of the first PHD finger of autoimmune regulator protein (AIRE1). Insights into autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy (APECED) disease. J. Biol. Chem. 280:11505-11512.
5. Chan, D.C. 2006. Mitochondria: dynamic organelles in disease, aging, and development. Cell. 125:1241-1252.
6. Chen, H., S.A. Detmer, A.J. Ewald, E.E. Griffin, S.E. Fraser, and D.C. Chan. 2003. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160:189-200.
7. Escobar-Henriques, M., B. Westermann, and T. Langer. 2006. Regulation of mitochondrial fusion by the F-box protein Mdm30 involves proteasome-independent turnover of Fzo1. J. Cell Biol. 173:645-650.
8. Estaquier, J., and D. Arnoult. 2007. Inhibiting Drp1-mediated mitochondrial fission selectively prevents the release of cytochrome c during apoptosis. Cell Death Differ. 14:1086-1094.
9. Griffin, E.E., J. Graumann, and D.C. Chan. 2005. The WD40 protein Caf4p is a component of the mitochondrial fission machinery and recruits Dnm1p to mitochondria. J. Cell Biol. 170:237-248.
10. Harder, Z., R. Zunino, and H. McBride. 2004. Sumo1 conjugates mitochondrial substrates and participates in mitochondrial fission. Curr. Biol. 14:340-345.
11. Hershko, A., and A. Ciechanover. 1992. The ubiquitin system for protein degradation. Annu. Rev. Biochem. 61:761-807.
12. Hinshaw, J.E. 2000. Dynamin and its role in membrane fission. Annu. Rev. Cell Dev. Biol. 16:483-519.
13. Huang, T.T., and A.D. D'Andrea. 2006. Regulation of DNA repair by ubiquitylation. Nat. Rev. Mol. Cell Biol. 7:323-334.
14. Joazeiro, C.A., and A.M. Weissman. 2000. RING finger proteins: mediators of ubiquitin ligase activity. Cell. 102:549-552.
15. Karbowski, M., Y.J. Lee, B. Gaume, S.Y. Jeong, S. Frank, A. Nechushtan, A. Santel, M. Fuller, C.L. Smith, and R.J. Youle. 2002. Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J. Cell Biol. 159:931-938.
16. Karbowski, M., D. Arnoult, H. Chen, D.C. Chan, C.L. Smith, and R.J. Youle. 2004. Quantitation of mitochondrial dynamics by photolabeling of individual organelles shows that mitochondrial fusion is blocked during the Bax activation phase of apoptosis. J. Cell Biol. 164:493-499.
17. 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.
18. Katoh, S., C. Hong, Y. Tsunoda, K. Murata, R. Takai, E. Minami, T. Yamazaki, and E. Katoh. 2003. High precision NMR structure and function of the RING-H2 finger domain of EL5, a rice protein whose expression is increased upon exposure to pathogen-derived oligosaccharides. J. Biol. Chem. 278:15341-15348.
19. Labrousse, A.M., M.D. Zappaterra, D.A. Rube, and A.M. van der Bliek. 1999. C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol. Cell. 4:815-826.
20. 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.
21. Legesse-Miller, A., R.H. Massol, and T. Kirchhausen. 2003. Constriction and Dnm1p recruitment are distinct processes in mitochondrial fission. Mol. Biol. Cell. 14:1953-1963.
22. Li, Z., K. Okamoto, Y. Hayashi, and M. Sheng. 2004. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell. 119:873-887.
23. McBride, H.M., M. Neuspiel, and S. Wasiak. 2006. Mitochondria: more than just a powerhouse. Curr. Biol. 16:R551-R560.
24. McCormick, A.L., V.L. Smith, D. Chow, and E.S. Mocarski. 2003. Disruption of mitochondrial networks by the human cytomegalovirus UL37 gene product viral mitochondrion-localized inhibitor of apoptosis. J. Virol. 77:631-641.
25. Mozdy, A.D., J.M. McCaffery, and J.M. Shaw. 2000. Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p. J. Cell Biol. 151:367-380.
26. Nakamura, N., Y. Kimura, M. Tokuda, S. Honda, and S. Hirose. 2006. MARCH-V is a novel mitofusin 2- and Drp1-binding protein able to change mitochondrial morphology. EMBO Rep. 7:1019-1022.
27. Naylor, K., E. Ingerman, V. Okreglak, M. Marino, J.E. Hinshaw, and J. Nunnari. 2006. Mdv1 interacts with assembled dnm1 to promote mitochondrial division. J. Biol. Chem. 281:2177-2183.
28. Neutzner, A., and R.J. Youle. 2005. Instability of the mitofusin Fzo1 regulates mitochondrial morphology during the mating response of the yeast Saccharomyces cerevisiae. J. Biol. Chem. 280:18598-18603.
29. Nunnari, J., W.F. Marshall, A. Straight, A. Murray, J.W. Sedat, and P. Walter. 1997. Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA. Mol. Biol. Cell. 8:1233-1242.
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.
31. Otsuga, D., B.R. Keegan, E. Brisch, J.W. Thatcher, G.J. Hermann, W. Bleazard, and J.M. Shaw. 1998. The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast. J. Cell Biol. 143:333-349.
32. Partikian, A., B. Olveczky, R. Swaminathan, Y. Li, and A.S. Verkman. 1998. Rapid diffusion of green fluorescent protein in the mitochondrial matrix. J. Cell Biol. 140:821-829.
33. Praefcke, G.J., and H.T. McMahon. 2004. The dynamin superfamily: universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell Biol. 5:133-147.
34. Santel, A., and M.T. Fuller. 2001. Control of mitochondrial morphology by a human mitofusin. J. Cell Sci. 114:867-874.
35. Shaw, J.M., and J. Nunnari. 2002. Mitochondrial dynamics and division in budding yeast. Trends Cell Biol. 12:178-184.
36. 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.
37. Staub, O., and D. Rotin. 2006. Role of ubiquitylation in cellular membrane transport. Physiol. Rev. 86:669-707.
38. Stojanovski, D., O.S. Koutsopoulos, K. Okamoto, and M.T. Ryan. 2004. Levels of human Fis1 at the mitochondrial outer membrane regulate mitochondrial morphology. J. Cell Sci. 117:1201-1210.
39. Suzuki, M., S.Y. Jeong, M. Karbowski, R.J. Youle, and N. Tjandra. 2003. The solution structure of human mitochondria fission protein Fis1 reveals a novel TPR-like helix bundle. J. Mol. Biol. 334:445-458.
40. Szabadkai, G., A.M. Simoni, M. Chami, M.R. Wieckowski, R.J. Youle, and R. Rizzuto. 2004. Drp-1-dependent division of the mitochondrial network blocks intraorganellar Ca2+ waves and protects against Ca2+-mediated apoptosis. Mol. Cell. 16:59-68.
41. Szabadkai, G., A.M. Simoni, K. Bianchi, D. De Stefani, S. Leo, M.R. Wieckowski, and R. Rizzuto. 2006. Mitochondrial dynamics and Ca2+ signaling. Biochim. Biophys. Acta. 1763:442-449.
42. Tieu, Q., and J. Nunnari. 2000. Mdv1p is a WD repeat protein that interacts with the dynamin-related GTPase, Dnm1p, to trigger mitochondrial division. J. Cell Biol. 151:353-366.
43. Tieu, Q., V. Okreglak, K. Naylor, and J. Nunnari. 2002. The WD repeat protein, Mdv1p, functions as a molecular adaptor by interacting with Dnm1p and Fis1p during mitochondrial fission. J. Cell Biol. 158:445-452.
44. 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.
45. Welchman, R.L., C. Gordon, and R.J. Mayer. 2005. Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat. Rev. Mol. Cell Biol. 6:599-609.
46. Yonashiro, R., S. Ishido, S. Kyo, T. Fukuda, E. Goto, Y. Matsuki, M. Ohmura-Hoshino, K. Sada, H. Hotta, H. Yamamura, et al. 2006. A novel mitochondrial ubiquitin ligase plays a critical role in mitochondrial dynamics. EMBO J. 25:3618-3626.
47. Yoon, Y., K.R. Pitts, and M.A. McNiven. 2001. Mammalian dynamin-like protein DLP1 tubulates membranes. Mol. Biol. Cell. 12:2894-2905.
48. 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.
49. Youle, R.J., and M. Karbowski. 2005. Mitochondrial fission in apoptosis. Nat. Rev. Mol. Cell Biol. 6:657-663.