Mgm1p, a dynamin-related GTPase, is essential for fusion of the mitochondrial outer membrane

Molecular Biology of the Cell

Volumn 14, Issue 6, 2003, Pages 2342-2356

  Sesaki, Hiromi ^a   Southard, Sheryl M ^a   Yaffe, Michael P ^b   Jensen, Robert E ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN; GUANOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; MUTANT PROTEIN; PROTEIN FZO1P; PROTEIN MGM1P; PROTEIN UGO1P; UNCLASSIFIED DRUG;

ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE; MGM1 GENE; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; WILD TYPE; ZYGOTE;

DNA, MITOCHONDRIAL; GTP PHOSPHOHYDROLASES; GTP-BINDING PROTEINS; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0038376024     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-12-0788     Document Type: Article

References (63)

1. Adams, A., Gottschling, D., Kaiser, C., and Stearns, T. (1997). Methods in Yeast Genetics. Plainview, NY: Cold Spring Harbor Laboratory Press.
2. Alexander, C. 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.
3. Azpiroz, R., and Butow, R.A. (1995). Mitochondrial inheritance in yeast. Methods Enzymol. 260, 453-465.
4. Bereiter-Hahn, J., and Voth, M. (1994). Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc. Res. Tech. 27, 198-219.
5. 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.
6. Bomer, U., Pfanner, N., and Dietmeier, K. (1996). Identification of a third yeast mitochondrial Tom protein with tetratrico peptide repeats. FEBS Lett. 382, 153-158.
7. Brachmann, C.B., Davies, A., Cost, G.J., Caputo, E., Li, J., Hieter, P., and Boeke, J.D. (1998). Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132.
8. Burgess, S.M., Delannoy, M., and Jensen, R.E. (1994). MMM1 encodes a mitochondrial outer membrane protein essential for establishing and maintaining the structure of yeast mitochondria. J. Cell Biol. 126, 1375-1391.
9. Cerveny, K.L., McCaffery, J.M., and Jensen, R.E. (2001). Division of mitochondria requires a novel DMN1-interacting protein, Net2p. Mol. Biol. Cell 12, 309-321.
10. Damke, H., Binns, D.D., Ueda, H., Schmid, S.L., and Baba, T. (2001). Dynamin GTPase domain mutants block endocytic vesicle formation at morphologically distinct stages. Mol. Biol. Cell 12, 2578-2589.
11. Daum, G., Böhni, P.C., and Schatz, G. (1982). Import of proteins into mitochondria. Cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J. Cell Biol. 257, 13028-13033.
12. Delettre, C. et al. (2000). Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat. Genet. 26, 207-210.
13. Delettre, C., Lenaers, G., Pelloquin, L., Belenguer, P., and Hamel, C.P. (2002). OPA1 (Kjer type) dominant optic atrophy: a novel mitochondrial disease. Mol. Genet. Metab. 75, 97-107.
14. Emtage, J.L., and Jensen, R.E. (1993). MAS6 encodes an essential inner membrane component of the yeast mitochondrial protein import pathway. J. Cell Biol. 122, 1003-1012.
15. Evan, G.I., Lewis, G.K., Ramsay, G., and Bishop, J.M. (1985). Isolation of monoclonal antibodies specific for human c-myc protooncogene product. Mol Cell Biol. 5, 3610-3616.
16. Fekkes, P., Shepard, K.A., and Yaffe, M.P. (2000). Gag3p, an outer membrane protein required for fission of mitochondrial tubules. J. Cell Biol. 151, 333-340.
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. Gammie, A.E., Kurihara, L.J., Vallee, R.B., and Rose, M.D. (1995). DNM1, a dynamin-related gene, participates in endosomal trafficking in yeast. J. Cell Biol. 130, 553-566.
19. Gratzer, S. et al. (1995). Mas37p, a novel receptor subunit for protein import into mitochondria. J. Cell Biol. 129, 25-34.
20. Grote, E., Carr, C.M., and Novick, P.J. (2000). Ordering the final events in yeast exocytosis. J. Cell Biol. 151, 439-452.
21. Gu, X., and Verma, D.P. (1996). Phragmoplastin, a dynamin-like protein associated with cell plate formation in plants. EMBO J. 15, 695-704.
22. 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.
23. Hales, K.G., and Fuller, M.T. (1997). Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell 90, 121-129.
24. Hermann, G.J., and Shaw, J.M. (1998). Mitochondrial dynamics in yeast. Annu. Rev. Cell Dev. Biol. 14, 265-303.
25. 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.
26. Hobbs, A.E., Srinivasan, M., McCaffery, J.M., and Jensen, R.E. (2001). Mmm1p, a mitochondrial outer membrane protein, is connected to mitochondrial DNA (mtDNA) nucleoids and required for mtDNA stability. J. Cell Biol. 152, 401-410.
27. Hoffman, C.S., and Winston, F. (1987). A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation into Escherichia coli. Gene 57, 267-272.
28. Hwa, J.J., Hiller, M.A., Fuller, M.T., and Santel, A. (2002). Differential expression of the Drosophila mitofusin genes fuzzy onions (fzo) and dmfn. Mech. Dev. 116, 213-216.
29. 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.
30. 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.
31. Labrousse, A.M., Zappaterra, M.D., Rube, D.A., and van der Bliek, A.M. (1999). C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol. Cell 4, 815-826.
32. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
33. Marks, B., Stowell, M.H., Vallis, Y., Mills, I.G., Gibson, A., Hopkins, C.R., and McMahon, H.T. (2001). GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410, 231-235.
34. McNiven, M.A. (1998). Dynamin: a molecular motor with pinchase action. Cell 94, 151-154.
35. Nigro, J.M., Sikorski, R., Reed, S.I., and Vogelstein, B. (1992). Human p53 and CDC2Hs genes combine to inhibit the proliferation of Saccharomyces cerevisiae. Mol. Cell. Biol. 12, 1357-1365.
36. Niman, H.L., Houghten, R.A., Walker, L.E., Reisfeld, R.A., Wilson, I.A., Hogle, J.M., and Lerner, R.A. (1983). Generation of protein-reactive antibodies by short peptides is an event of high frequency: implications for the structural basis of immune recognition. Proc. Natl. Acad. Sci. USA 80, 4949-4953.
37. Nunnari, J., Marshall, W.F., Straight, A., Murray, A., Sedat, J.W., and Walter, P. (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.
38. Okamoto, K., Perlman, P.S., and Butow, R.A. (1998). The sorting of mitochondrial DNA and mitochondrial proteins in zygotes: preferential transmission of mitochondrial DNA to the medial bud. J. Cell Biol. 142, 613-623.
39. Oldenburg, K.R., Vo, K.T., Michaelis, S., and Paddon, C. (1997). Recombination-mediated PCR-directed plasmid construction in vivo in yeast. Nucleic Acids Res. 25, 451-452.
40. Paumard, P., Vaillier, J., Coulary, B., Schaeffer, J., Soubannier, V., Mueller, D.M., Brethes, D., di Rago, J.P., and Velours, J. (2002). The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 21, 221-230.
41. 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, 20150-20455.
42. 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.
43. Ryan, K.R., Menold, M.M., Garrett, S., and Jensen, R.E. (1994). SMS1, a high-copy suppressor of the yeast mas6 mutant, encodes an essential inner membrane protein required for mitochondrial protein import. Mol. Biol. Cell 5, 529-538.
44. Santel, A., and Fuller, M.T. (2001). Control of mitochondrial morphology by a human mitofusin. J. Cell Sci. 114, 867-874.
45. Schlossmann, J., Lill, R., Neupert, W., and Court, D.A. (1996). Tom71, a novel homologue of the mitochondrial preprotein receptor Tom70. J. Biol. Chem. 271, 17890-17895.
46. Schmid, S.L., McNiven, M.A., and De Camilli, P. (1998). Dynamin and its partners: a progress report. Curr. Opin. Cell Biol. 10, 504-512.
47. Sesaki, H., and Jensen, R.E. (1999). Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J. Cell Biol. 147, 699-706.
48. Sesaki, H., and Jensen, R.E. (2001). UGO1 encodes an outer membrane protein required for mitochondnal fusion. J. Cell Biol. 152, 1123-1134.
49. Sever, S., Damke, H., and Schmid, S.L. (2000a). Dynamin:GTP controls the formation of constricted coated pits, the rate limiting step in clathrin-mediated endocytosis. J. Cell Biol. 150, 1137-1148.
50. Sever, S., Damke, H., and Schmid, S.L. (2000b). Garrotes, springs, ratchets, and whips: putting dynamin models to the test. Traffic 1, 385-392.
51. Sever, S., Muhlberg, A.B., and Schmid, S.L. (1999). Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature 398, 481-486.
52. Shaw, J.M., and Nunnari, J. (2002). Mitochondrial dynamics and division in budding yeast. Trends Cell Biol. 12, 178-184.
53. Shepard, K.A., and Yaffe, M.P. (1999). The yeast dynamin-like protein, mgm1p, functions on the mitochondrial outer membrane to mediate mitochondrial inheritance [In Process Citation]. J. Cell Biol. 144, 711-720.
54. Sikorski, R., and Hieter, P. (1989). A system of shuttle vectors and host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-28.
55. Sweitzer, S.M., and Hinshaw, J.E. (1998). Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93, 1021-1029.
56. Takei, K., McPherson, P.S., Schmid, S.L., and De Camilli, P. (1995). Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature 374, 186-190.
57. Tyers, M., Tokiwa, G., Nash, R., and Futcher, B. (1992). The Cln3-Cdc28 kinase complex of S. cerevisiae is regulated by proteolysis and phosphorylation. EMBO J. 11, 1773-1784.
58. Tyler, D. (1992). The Mitochondrion. New York: VCH Publishers.
59. Weber, T., Parlati, F., McNew, J.A., Johnston, R.J., Westermann, B., Sollner, T.H., and Rothman, J.E. (2000). SNAREpins are functionally resistant to disruption by NSF and alphaSNAP. J. Cell Biol. 149, 1063-1072.
60. Winston, F., Dollard, C., and Ricupero-Hovasse, S.L. (1995). Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11, 53-55.
61. 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.
62. Yaffe, M.P. (1999). Dynamic mitochondria. Nat. Cell Biol. 1, E149-E150.
63. Yaffe, M.P., Jensen, R.E., and Guido, E.C. (1989). The major 45-kDa protein of the yeast mitochondrial outer membrane is not essential for cell growth or mitochondrial function. J. Biol. Chem. 264, 21091-21096.