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J Cell Biol. 1994 Sep 2; 126(6): 1375–1391.
PMCID: PMC2290956

MMM1 encodes a mitochondrial outer membrane protein essential for establishing and maintaining the structure of yeast mitochondria


In the yeast Saccharomyces cerevisiae, mitochondria are elongated organelles which form a reticulum around the cell periphery. To determine the mechanism by which mitochondrial shape is established and maintained, we screened yeast mutants for those defective in mitochondrial morphology. One of these mutants, mmm1, is temperature- sensitive for the external shape of its mitochondria. At the restrictive temperature, elongated mitochondria appear to quickly collapse into large, spherical organelles. Upon return to the permissive temperature, wild-type mitochondrial structure is restored. The morphology of other cellular organelles is not affected in mmm1 mutants, and mmm1 does not disrupt normal actin or tubulin organization. Cells disrupted in the MMM1 gene are inviable when grown on nonfermentable carbon sources and show abnormal mitochondrial morphology at all temperatures. The lethality of mmm1 mutants appears to result from the inability to segregate the aberrant-shaped mitochondria into daughter cells. Mitochondrial structure is therefore important for normal cell function. Mmm1p is located in the mitochondrial outer membrane, with a large carboxyl-terminal domain facing the cytosol. We propose that Mmm1p maintains mitochondria in an elongated shape by attaching the mitochondrion to an external framework, such as the cytoskeleton.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Ball EH, Singer SJ. Mitochondria are associated with microtubules and not with intermediate filaments in cultured fibroblasts. Proc Natl Acad Sci U S A. 1982 Jan;79(1):123–126. [PMC free article] [PubMed]
  • Bereiter-Hahn J. Dimethylaminostyrylmethylpyridiniumiodine (daspmi) as a fluorescent probe for mitochondria in situ. Biochim Biophys Acta. 1976 Jan 15;423(1):1–14. [PubMed]
  • Bereiter-Hahn J. Behavior of mitochondria in the living cell. Int Rev Cytol. 1990;122:1–63. [PubMed]
  • Bereiter-Hahn J, Vöth M. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc Res Tech. 1994 Feb 15;27(3):198–219. [PubMed]
  • Botstein D, Falco SC, Stewart SE, Brennan M, Scherer S, Stinchcomb DT, Struhl K, Davis RW. Sterile host yeasts (SHY): a eukaryotic system of biological containment for recombinant DNA experiments. Gene. 1979 Dec;8(1):17–24. [PubMed]
  • Chowdhury S, Smith KW, Gustin MC. Osmotic stress and the yeast cytoskeleton: phenotype-specific suppression of an actin mutation. J Cell Biol. 1992 Aug;118(3):561–571. [PMC free article] [PubMed]
  • Collier NC, Sheetz MP, Schlesinger MJ. Concomitant changes in mitochondria and intermediate filaments during heat shock and recovery of chicken embryo fibroblasts. J Cell Biochem. 1993 Jul;52(3):297–307. [PubMed]
  • Criddle RS, Schatz G. Promitochondria of anaerobically grown yeast. I. Isolation and biochemical properties. Biochemistry. 1969 Jan;8(1):322–334. [PubMed]
  • Daum G, Böhni PC, Schatz G. Import of proteins into mitochondria. Cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J Biol Chem. 1982 Nov 10;257(21):13028–13033. [PubMed]
  • Dente L, Cesareni G, Cortese R. pEMBL: a new family of single stranded plasmids. Nucleic Acids Res. 1983 Mar 25;11(6):1645–1655. [PMC free article] [PubMed]
  • Drubin DG, Jones HD, Wertman KF. Actin structure and function: roles in mitochondrial organization and morphogenesis in budding yeast and identification of the phalloidin-binding site. Mol Biol Cell. 1993 Dec;4(12):1277–1294. [PMC free article] [PubMed]
  • Emtage JL, Jensen RE. MAS6 encodes an essential inner membrane component of the yeast mitochondrial protein import pathway. J Cell Biol. 1993 Sep;122(5):1003–1012. [PMC free article] [PubMed]
  • Field J, Nikawa J, Broek D, MacDonald B, Rodgers L, Wilson IA, Lerner RA, Wigler M. Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol Cell Biol. 1988 May;8(5):2159–2165. [PMC free article] [PubMed]
  • Haid A, Suissa M. Immunochemical identification of membrane proteins after sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Methods Enzymol. 1983;96:192–205. [PubMed]
  • Hase T, Riezman H, Suda K, Schatz G. Import of proteins into mitochondria: nucleotide sequence of the gene for a 70-kd protein of the yeast mitochondrial outer membrane. EMBO J. 1983;2(12):2169–2172. [PMC free article] [PubMed]
  • Heggeness MH, Simon M, Singer SJ. Association of mitochondria with microtubules in cultured cells. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3863–3866. [PMC free article] [PubMed]
  • Hoffman CS, Winston F. A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene. 1987;57(2-3):267–272. [PubMed]
  • Hoffmann HP, Avers CJ. Mitochondrion of yeast: ultrastructural evidence for one giant, branched organelle per cell. Science. 1973 Aug 24;181(4101):749–751. [PubMed]
  • Jensen RE, Yaffe MP. Import of proteins into yeast mitochondria: the nuclear MAS2 gene encodes a component of the processing protease that is homologous to the MAS1-encoded subunit. EMBO J. 1988 Dec 1;7(12):3863–3871. [PMC free article] [PubMed]
  • Koehler JK. Fine structure observations in frozen-etched bovine spermatozoa. J Ultrastruct Res. 1966 Oct;16(3):359–375. [PubMed]
  • Koning AJ, Lum PY, Williams JM, Wright R. DiOC6 staining reveals organelle structure and dynamics in living yeast cells. Cell Motil Cytoskeleton. 1993;25(2):111–128. [PubMed]
  • Kovácová V, Irmlerová J, Kovác L. Oxidative phosphorylatiion in yeast. IV. Combination of a nuclear mutation affecting oxidative phosphorylation with cytoplasmic mutation to respiratory deficiency. Biochim Biophys Acta. 1968 Aug 20;162(2):157–163. [PubMed]
  • Kyte J, Doolittle RF. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. [PubMed]
  • Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. [PubMed]
  • Bereiter-Hahn J, Vöth M. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc Res Tech. 1994 Feb 15;27(3):198–219. [PubMed]
  • May R. Microfilaments in yeast mitochondria. Protoplasma. 1974;82(4):395–399. [PubMed]
  • McConnell SJ, Stewart LC, Talin A, Yaffe MP. Temperature-sensitive yeast mutants defective in mitochondrial inheritance. J Cell Biol. 1990 Sep;111(3):967–976. [PMC free article] [PubMed]
  • McDonald K. Osmium ferricyanide fixation improves microfilament preservation and membrane visualization in a variety of animal cell types. J Ultrastruct Res. 1984 Feb;86(2):107–118. [PubMed]
  • Miyakawa I, Aoi H, Sando N, Kuroiwa T. Fluorescence microscopic studies of mitochondrial nucleoids during meiosis and sporulation in the yeast, Saccharomyces cerevisiae. J Cell Sci. 1984 Mar;66:21–38. [PubMed]
  • Mose-Larsen P, Bravo R, Fey SJ, Small JV, Celis JE. Putative association of mitochondria with a subpopulation of intermediate-sized filaments in cultured human skin fibroblasts. Cell. 1982 Dec;31(3 Pt 2):681–692. [PubMed]
  • Nakashima RA, Paggi MG, Pedersen PL. Contributions of glycolysis and oxidative phosphorylation to adenosine 5'-triphosphate production in AS-30D hepatoma cells. Cancer Res. 1984 Dec;44(12 Pt 1):5702–5706. [PubMed]
  • Nasmyth KA, Tatchell K. The structure of transposable yeast mating type loci. Cell. 1980 Mar;19(3):753–764. [PubMed]
  • Niman HL, Houghten RA, Walker LE, Reisfeld RA, Wilson IA, Hogle JM, Lerner RA. 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 U S A. 1983 Aug;80(16):4949–4953. [PMC free article] [PubMed]
  • Pardo JV, Siliciano JD, Craig SW. Vinculin is a component of an extensive network of myofibril-sarcolemma attachment regions in cardiac muscle fibers. J Cell Biol. 1983 Oct;97(4):1081–1088. [PMC free article] [PubMed]
  • Plattner H, Schatz G. Promitochondria of anaerobically grown yeast. 3. Morphology. Biochemistry. 1969 Jan;8(1):339–343. [PubMed]
  • Price MG, Gomer RH. Mitoskelin: a mitochondrial protein found in cytoskeletal preparations. Cell Motil Cytoskeleton. 1989;13(4):274–287. [PubMed]
  • Pringle JR, Preston RA, Adams AE, Stearns T, Drubin DG, Haarer BK, Jones EW. Fluorescence microscopy methods for yeast. Methods Cell Biol. 1989;31:357–435. [PubMed]
  • Putney SD, Benkovic SJ, Schimmel PR. A DNA fragment with an alpha-phosphorothioate nucleotide at one end is asymmetrically blocked from digestion by exonuclease III and can be replicated in vivo. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7350–7354. [PMC free article] [PubMed]
  • Rebhun LI. Polarized intracellular particle transport: saltatory movements and cytoplasmic streaming. Int Rev Cytol. 1972;32:93–137. [PubMed]
  • Riles L, Dutchik JE, Baktha A, McCauley BK, Thayer EC, Leckie MP, Braden VV, Depke JE, Olson MV. Physical maps of the six smallest chromosomes of Saccharomyces cerevisiae at a resolution of 2.6 kilobase pairs. Genetics. 1993 May;134(1):81–150. [PMC free article] [PubMed]
  • Rohde K, Watson NA, Cribb T. Ultrastructure of sperm and spermatogenesis of Lobatostoma manteri (Trematoda, Aspidogastrea). Int J Parasitol. 1991 Jul;21(4):409–419. [PubMed]
  • Rothstein R. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 1991;194:281–301. [PubMed]
  • Ryan KR, Menold MM, Garrett S, Jensen RE. SMS1, a high-copy suppressor of the yeast mas6 mutant, encodes an essential inner membrane protein required for mitochondrial protein import. Mol Biol Cell. 1994 May;5(5):529–538. [PMC free article] [PubMed]
  • Saiki RK, Scharf S, Faloona F, Mullis KB, Horn GT, Erlich HA, Arnheim N. Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science. 1985 Dec 20;230(4732):1350–1354. [PubMed]
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PMC free article] [PubMed]
  • Schiestl RH, Gietz RD. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet. 1989 Dec;16(5-6):339–346. [PubMed]
  • Schnapp BJ, Reese TS. Cytoplasmic structure in rapid-frozen axons. J Cell Biol. 1982 Sep;94(3):667–669. [PMC free article] [PubMed]
  • Sikorski RS, Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. [PMC free article] [PubMed]
  • Smith DS, Järlfors U, Cameron BF. Morphological evidence for the participation of microtubules in axonal transport. Ann N Y Acad Sci. 1975 Jun 30;253:472–506. [PubMed]
  • Tandler B, Erlandson RA, Wynder EL. Riboflavin and mouse hepatic cell structure and function. I. Ultrastructural alterations in simple deficiency. Am J Pathol. 1968 Jan;52(1):69–96. [PMC free article] [PubMed]
  • Thorsness PE. Structural dynamics of the mitochondrial compartment. Mutat Res. 1992 Sep;275(3-6):237–241. [PubMed]
  • Tyers M, Tokiwa G, Nash R, Futcher B. The Cln3-Cdc28 kinase complex of S. cerevisiae is regulated by proteolysis and phosphorylation. EMBO J. 1992 May;11(5):1773–1784. [PMC free article] [PubMed]
  • Wallace PG, Huang M, Linnane AW. The biogenesis of mitochondria. II. The influence of medium composition on the cytology of anaerobically grown Saccharomyces cerevisiae. J Cell Biol. 1968 May;37(2):207–220. [PMC free article] [PubMed]
  • Weinert TA, Hartwell LH. Characterization of RAD9 of Saccharomyces cerevisiae and evidence that its function acts posttranslationally in cell cycle arrest after DNA damage. Mol Cell Biol. 1990 Dec;10(12):6554–6564. [PMC free article] [PubMed]
  • Weisman LS, Emr SD, Wickner WT. Mutants of Saccharomyces cerevisiae that block intervacuole vesicular traffic and vacuole division and segregation. Proc Natl Acad Sci U S A. 1990 Feb;87(3):1076–1080. [PMC free article] [PubMed]
  • Xu H, Boeke JD. Localization of sequences required in cis for yeast Ty1 element transposition near the long terminal repeats: analysis of mini-Ty1 elements. Mol Cell Biol. 1990 Jun;10(6):2695–2702. [PMC free article] [PubMed]
  • Yaffe MP, Schatz G. Two nuclear mutations that block mitochondrial protein import in yeast. Proc Natl Acad Sci U S A. 1984 Aug;81(15):4819–4823. [PMC free article] [PubMed]
  • Yaffe MP, Jensen RE, Guido EC. The major 45-kDa protein of the yeast mitochondrial outer membrane is not essential for cell growth or mitochondrial function. J Biol Chem. 1989 Dec 15;264(35):21091–21096. [PubMed]
  • Yotsuyanagi Y. Fibrous component of yeast mitochondria. J Ultrastruct Mol Struct Res. 1988 Mar;98(3):254–266. [PubMed]
  • Zickler D, Olson LW. The synaptonemal complex and the spindle plaque during meiosis in yeast. Chromosoma. 1975;50(1):1–23. [PubMed]
  • Zorn TM, de Oliveira SF, Abrahamsohn PA. Organization of intermediate filaments and their association with collagen-containing phagosomes in mouse decidual cells. J Struct Biol. 1990 Mar;103(1):23–33. [PubMed]

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