Two Mitofusin Proteins, Mammalian Homologues of FZO, with Distinct Functions Are Both Required for Mitochondrial Fusion

Journal of Biochemistry

Volumn 134, Issue 3, 2003, Pages 333-344

  Eura, Yuka ^a   Ishihara, Naotada ^a   Yokota, Sadaki ^b   Mihara, Katsuyoshi ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b UNIVERSITY OF YAMANASHI   (Japan)

Author keywords

GTPase; Membrane fusion; Mitochondria; Organelle morphology; RNAi

Indexed keywords

FZO PROTEIN; GUANOSINE TRIPHOSPHATASE; ISOPROTEIN; MITOFUSIN; MITOFUSIN 1; MITOFUSIN 2; MUTANT PROTEIN; OUTER MEMBRANE PROTEIN; RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL FUSION; CELL LABELING; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HELA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; MAMMAL CELL; MEMBRANE FUSION; MICROTUBULE; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTER MEMBRANE; PARAINFLUENZA VIRUS 1; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SEQUENCE HOMOLOGY; TECHNIQUE; TISSUE DISTRIBUTION;

ANIMALS; DROSOPHILA PROTEINS; GTP PHOSPHOHYDROLASES; HELA CELLS; HUMANS; MEMBRANE FUSION; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MORPHOGENESIS; MUTATION; PROTEIN ISOFORMS; RATS; RNA, SMALL INTERFERING; SENDAI VIRUS; TISSUE DISTRIBUTION; TRANSFECTION;

ANIMALIA; HUMAN PARAINFLUENZA VIRUS 1; MAMMALIA;

EID: 0142058391     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/jb/mvg150     Document Type: Article

References (46)

1. Hermann, G.J. and Shaw, J.M. (1998) Mitochondrial dynamics in yeast. Annu. Rev. Cell. Dev. Biol. 14, 265-303
2. Yaffe, M.P. (1999) The machinery of mitochondrial inheritance and behavior. Science 283, 1493-1497
3. Jensen, R.E., Hobbs, A.E., Cerveny, K.L., and Sesaki, H. (2000) Yeast mitochondrial dynamics: fusion, division, segregation, and shape. Microsc. Res. Tech. 51, 573-583
4. McConnell, S.J. and Yaffe, M.P. (1993) Intermediate filament formation by a yeast protein essential for organelle inheritance. Science 260, 687-689
5. Sesaki, H. and Jensen, R.E. (1999) Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J. Cell Biol. 147, 699-706
6. Shaw, J.M. and Nunnari, J. (2002) Mitochondrial dynamics and division in budding yeast. Trends Cell Biol. 12, 178-184
7. Otsuga, D., Keegan, B.R., Brisch, E., Thatcher, J.W., Hermann, G.J., Bleazard, W., and Shaw, J.M. (1998) The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast. J. Cell Biol. 143, 333-349
8. Bleazard, W., McCaffery, J.M., King, E.J., Bale, S., Mozdy, A., Tieu, Q., Nunnari, J., and Shaw, J.M. (1999) The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat. Cell Biol. 1, 298-304
9. Jones, B.A. and Fangman, W.L. (1992) Mitochondrial DNA maintenance in yeast requires a protein containing a region related to the GTP-binding domain of dynamin. Genes Dev. 6, 380-389
10. Guan, K., Farh, L., Marshall, T.K., and Deschenes, R.J. (1993) Normal mitochondrial structure and genome maintenance in yeast requires the dynamin-like product of the MGM1 gene. Curr. Genet. 24, 141-148
11. Shepard, K.A. and Yaffe, M.P. (1999) The yeast dynamin-like protein, Mgm1p, functions on the mitochondrial outer membrane to mediate mitochondrial inheritance. J. Cell Biol. 144, 711-720
12. Pelloquin, L., Belenguer, P., Menon, Y., Gas, N., and Ducommun, B. (1999) Fission yeast Msp1 is a mitochondrial dynamin-related protein. J. Cell Sci. 112, 4151-4161
13. Wong, E.D., Wagner, J.A., Gorsich, S.W., McCaffery, J.M., Shaw, J.M., and Nunnari, J. (2000) The dynamin-related GTPase, Mgm1p, is an intermembrane space protein required for maintenance of fusion competent mitochondria. J. Cell Biol. 151, 341-352.
14. Hales, K.G. and Fuller, M.T. (1997) Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell 90, 121-129
15. Hermann, G.J., Thatcher, J.W., Mills, J.P., Hales, K.G., Fuller, M.T., Nunnari, J., and Shaw, J.M. (1998) Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. J. Cell Biol. 143, 359-373
16. Rapaport, D., Brunner, M., Neupert, W., and Westermann, B. (1998) Fzo1p is a mitochondrial outer membrane protein essential for the biogenesis of functional mitochondria in Saccharomyces cerevisiae. J. Biol. Chem. 273, 20150-20155
17. Fritz, S., Rapaport, D., Klanner, E., Neupert, W., and Westermann, B. (2001) Connection of the mitochondrial outer and inner membranes by Fzo1 is critical for organellar fusion. J. Cell Biol. 152, 683-692
18. Shin, H.W., Shinotsuka, C., Torii, S., Murakami, K., and Nakayama, K. (1997) Identification and subcellular localization of a novel mammalian dynamin-related protein homologous to yeast Vps1p and Dnm1p. J. Biochem. (Tokyo) 122, 525-530
19. Imoto, M., Tachibana, I., and Urrutia, R. (1998) Identification and functional characterization of a novel human protein highly related to the yeast dynamin-like GTPase Vpslp. J. Cell Sci. 111, 1341-1349
20. Kamimoto, T., Nagai, Y., Onogi, H., Muro, Y., Wakabayashi, T., and Hagiwara, M. (1998) Dymple, a novel dynamin-like high molecular weight GTPase lacking a proline-rich carboxyl-terminal domain in mammalian cells. J. Biol. Chem. 273, 1044-1051
21. Yoon, Y., Pitts, K.R., Dahan, S., and McNiven, M.A. (1998) A novel dynamin-like protein associates with cytoplasmic vesicles and tubules of the endoplasmic reticulum in mammalian cells. J. Cell Biol. 140, 779-793
22. Smirnova, E., Shurland, D.L., Ryazantsev, S.N., and van der Bliek, A.M. (1998) A human dynamin-related protein controls the distribution of mitochondria. J. Cell Biol. 143, 351-358
23. Pitts, K.R., Yoon, Y., Krueger, E.W., and McNiven, M.A. (1999) The dynamin-like protein DLP1 is essential for normal distribution and morphology of the endoplasmic reticulum and mitochondria in mammalian cells. Mol. Biol. Cell 10, 4403-4417
24. Smirnova, E., Griparic, L., Shurland, D.L., and van Der Bliek, A.M. (2001) Dynamin-related protein drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 12, 2245-2256
25. Yoon, Y., Pitts, K.R., and McNiven, M.A. (2001) Mammalian dynamin-like protein dlp1 tubulates membranes. Mol. Biol. Cell 12, 2894-2905
26. Frank, S., Gaume, B., Bergmann-Leitner, E., Leitner, W., Robert, E., Catez, F., Smith, C., and Youle, R. (2001) The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 4, 515-525
27. Alexander, C., Votruba, M., Pesch, U.E., Thiselton, D.L., Mayer, S., Moore, A., Rodriguez, M., Kellner, U., Leo-Kottler, B., Auburger, G., Bhattacharya, S.S., and Wissinger, B. (2000) OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat. Genet. 26, 211-215
28. Delettre, C., Lenaers, G., Griffoin, J.M., Gigarel, N., Lorenzo, C., Belenguer, P., Pelloquin, L., Grosgeorge, J., Turc-Carel, C., Perret, E., Astarie-Dequeker, C., Lasquellec, L., Arnaud, B., Ducommun, B., Kaplan, J., and Hamel, C.P. (2000) Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat. Genet. 26, 207-210
29. Santel, A. and Fuller, M.T. (2001) Control of mitochondrial morphology by a human mitofusin. J. Cell Sci. 114, 867-874
30. Rojo, M., Legros, F., Chateau, D., and Lombes, A. (2002) Membrane topology and mitochondrial targeting of mitofusins, ubiquitous mammalian homologs of the transmembrane GTPase Fzo. J. Cell Sci. 115, 1663-1674
31. Mihara, K. (1990) Structure and regulation of rat liver microsomal stearoyl-CoA desaturase gene. J. Biochem. (Tokyo) 108, 1022-1029
32. Suzuki, H., Okazawa, Y., Komiya, T., Saeki, K., Mekada, E., Kitada, S., Ito, A., and Mihara, K. (2000) Characterization of rat TOM40, a central component of the preprotein translocase of the mitochondrial outer membrane. J. Biol. Chem. 275, 37930-37936
33. Suzuki, H., Maeda, M., and Mihara, K. (2002) Characterization of rat TOM70 as a receptor of the preprotein translocase of the mitochondrial outer membrane. J. Cell Sci. 115, 1895-1905
34. Ishihara, N. and Mihara, K. (1998) Identification of the protein import components of the rat mitochondrial inner membrane, rTIM17, rTIM23, and rTIM44. J. Biochem. (Tokyo) 123, 722-732
35. Saeki, K., Suzuki, H., Tsuneoka, M., Maeda, M., Iwamoto, R., Hasuwa, H., Shida, S., Takahashi, T., Sakaguchi, M., Endo, T., Miura, Y., Mekada, E., and Mihara, K. (2000) Identification of mammalian TOM22 as a subunit of the preprotein translocase of the mitochondrial outer membrane. J. Biol. Chem. 275, 31996-32002
36. Kose, S., Imamoto, N., Tachibana, T., Yoshida, M., and Yoneda, Y. (1999) beta-subunit of nuclear pore-targeting complex (importin-beta) can be exported from the nucleus in a Ran-independent manner. J. Biol. Chem. 274, 3946-3952
37. Ukaji, K., Ariyoshi, N., Sakaguchi, M., Hamasaki, N., and Mihara, K. (2002) Membrane topogenesis of the three amino-terminal transmembrane segments of Glucose-6-phosphatase on endoplasmic reticulum. Biochem. Biophys. Res. Commun. 292, 153-160
38. Ungermann, C., Neupert, W., and Cyr, D.M. (1994) The role of Hsp70 in conferring unidirectionality on protein translocation into mitochondria. Science 266, 1250-1253
39. Ishihara, N., Yamashina, S., Sakaguchi, M., Mihara, K., and Omura, T. (1995) Malfolded cytochrome P-450(M1) localized in unusual membrane structures of the endoplasmic reticulum in cultured animal cells. J. Biochem. (Tokyo) 118, 397-404
40. Yokota, S., Kamijo, K., and Oda, T. (2000) Aggregate formation and degradation of overexpressed wild-type and mutant urate oxidase proteins. Quality control of organelle-destined proteins by endoplasmic reticulum. Histochem. Cell Biol. 114, 433-446
41. Elbashir, S.M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., and Tuschl, T. (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411, 494-498
42. Ishihara, N., Jofuku, A., Eura, Y., and Mihara, K. (2003) Regulation of mitochondrial morphology by membrane potential and DRP1-dependent division and FZO1-dependent fusion reaction in mammalian cells. Biochem. Biophys. Res. Commun. 301, 891-898
43. Legros, F., Lombes, A., Frachon, P., and Rojo, M. (2002) Mitochondrial fusion in human cells is efficient, requires the inner membrane potential, and is mediated by mitofusins. Mol. Biol. Cell 13, 4343-4354
44. Kanaji, S., Iwahashi, J., Kida, Y., Sakaguchi, M., and Mihara, K. (2000) Characterization of the signal that directs Tom20 to the mitochondrial outer membrane. J. Cell Biol. 151, 277-288
45. Yano, M., Kanazawa, M., Terada, K., Namchai, C., Yamaizumi, M., Hanson, B., Hoogenraad, N., and Mori, M. (1997) Visualization of mitochondrial protein import in cultured mammalian cells with green fluorescent protein and effects of overexpression of the human import receptor Tom20. J. Biol. Chem. 272, 8459-8465
46. Chen, H., Detmer, S., Ewald, A., Griffin, E., Fraser, S., and Chan, D. (2003) Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160, 189-200