Integrity of the yeast mitochondrial genome, but not its distribution and inheritance, relies on mitochondrial fission and fusion

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 9, 2015, Pages E947-E956

  Osman, Christof ^a,b   Noriega, Thomas R ^a,b   Okreglak, Voytek ^a,b   Fung, Jennifer C ^b   Walter, Peter ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dnm1; Fzo1; Mitochondria; MtDNA; Yeast

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; CELL NUCLEUS DNA; FUNGAL DNA; LATRUNCULIN A; MITOCHONDRIAL DNA; NUCLEOPROTEIN; ACTIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ACTIN FILAMENT; ACUTE TOXICITY; ARTICLE; BIOLISTIC TRANSFORMATION; CELL FUNCTION; CONTROLLED STUDY; DNA RECOMBINATION; FLUORESCENCE MICROSCOPY; FUNGAL GENOME; GENE FUSION; GENETIC ASSOCIATION; INHERITANCE; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL FISSION; MITOCHONDRIAL FUSION; MITOCHONDRIAL GENOME; MITOCHONDRIAL TARGETING SIGNAL; MITOCHONDRION; NEXT GENERATION SEQUENCING; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; YEAST; BIOSYNTHESIS; CELL CYCLE; DNA REPLICATION; GENETIC VARIABILITY; GENETICS; METABOLISM; PHYSIOLOGY;

SACCHAROMYCES CEREVISIAE; VASCONCELLEA CANDICANS;

ACTINS; CELL CYCLE; DNA REPLICATION; DNA, FUNGAL; DNA, MITOCHONDRIAL; GENETIC VARIATION; GENOME, MITOCHONDRIAL; MITOCHONDRIAL DYNAMICS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84924065339     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1501737112     Document Type: Article

References (40)

1. Nunnari J, Suomalainen A (2012) Mitochondria: In sickness and in health. Cell 148(6): 1145-1159.
2. Turk EM, Das V, Seibert RD, Andrulis ED (2013) The mitochondrial RNA landscape of Saccharomyces cerevisiae. PLoS ONE 8(10): e78105.
3. Lipinski KA, Kaniak-Golik A, Golik P (2010) Maintenance and expression of the S. cerevisiae mitochondrial genome: From genetics to evolution and systems biology. Biochim Biophys Acta 1797(6-7): 1086-1098.
4. Chen XJ, Butow RA (2005) The organization and inheritance of the mitochondrial genome. Nat Rev Genet 6(11): 815-825.
5. Nunnari J, et al. (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(7): 1233-1242.
6. Okamoto K, Perlman PS, Butow RA (1998) The sorting of mitochondrial DNA and mitochondrial proteins in zygotes: Preferential transmission of mitochondrial DNA to the medial bud. J Cell Biol 142(3): 613-623.
7. Westermann B (2010) Mitochondrial fusion and fission in cell life and death. Nat Rev Mol Cell Biol 11(12): 872-884.
8. Murley A, et al. (2013) ER-associated mitochondrial division links the distribution of mitochondria and mitochondrial DNA in yeast. eLife 2: e00422.
9. Westermann B (2014) Mitochondrial inheritance in yeast. Biochim Biophys Acta 1837(7): 1039-1046.
10. Bleazard W, et al. (1999) The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat Cell Biol 1(5): 298-304.
11. Hermann GJ, et al. (1998) Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. J Cell Biol 143(2): 359-373.
12. Sesaki H, Jensen RE (1999) Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J Cell Biol 147(4): 699-706.
13. Leibowitz RD (1971) The effect of ethidium bromide on mitochondrial DNA synthesis and mitochondrial DNA structure in HeLa cells. J Cell Biol 51(1): 116-122.
14. Meeusen S, Nunnari J (2003) Evidence for a two membrane-spanning autonomous mitochondrial DNA replisome. J Cell Biol 163(3): 503-510.
15. Robinett CC, et al. (1996) In vivo localization of DNA sequences and visualization of large-scale chromatin organization using lac operator/repressor recognition. J Cell Biol 135(6 Pt 2): 1685-1700.
16. Wang X, Reyes-Lamothe R, Sherratt DJ (2008) Visualizing genetic loci and molecular machines in living bacteria. Biochem Soc Trans 36(Pt 4): 749-753.
17. Betz JL, Sasmor HM, Buck F, Insley MY, Caruthers MH (1986) Base substitution mutants of the lac operator: In vivo and in vitro affinities for lac repressor. Gene 50(1-3): 123-132.
18. Miyakawa I, Sando N, Kawano S, Nakamura S, Kuroiwa T (1987) Isolation of morphologically intact mitochondrial nucleoids from the yeast, Saccharomyces cerevisiae. J Cell Sci 88(Pt 4): 431-439.
19. Jensen RE, Hobbs AE, Cerveny KL, Sesaki H (2000) Yeast mitochondrial dynamics: Fusion, division, segregation, and shape. Microsc Res Tech 51(6): 573-583.
20. Kowald A, Kirkwood TBL (2011) Evolution of the mitochondrial fusion-fission cycle and its role in aging. Proc Natl Acad Sci USA 108(25): 10237-10242.
21. Baranowska H, Szczesniak B, Ejchart A, Kruszewskal A, Claisse M (1983) Re-combinational analysis of oxi2 mutants and preliminary analysis of their translation products in S. cerevisiae. Curr Genet 7(3): 225-233.
22. Gruschke S, et al. (2011) Cbp3-Cbp6 interacts with the yeast mitochondrial ribosomal tunnel exit and promotes cytochrome b synthesis and assembly. J Cell Biol 193(6): 1101-1114.
23. Friedman JR, Nunnari J (2014) Mitochondrial form and function. Nature 505(7483): 335-343.
24. Shadel GS (1999) Yeast as a model for human mtDNA replication. Am J Hum Genet 65(5): 1230-1237.
25. Gerhold JM, et al. (2014) Replication intermediates of the linear mitochondrial DNA of Candida parapsilosis suggest a common recombination based mechanism for yeast mitochondria. J Biol Chem 289(33): 22659-22670.
26. Gerhold JM, Aun A, Sedman T, Jõers P, Sedman J (2010) Strand invasion structures in the inverted repeat of Candida albicans mitochondrial DNA reveal a role for homologous recombination in replication. Mol Cell 39(6): 851-861.
27. Salje J, Gayathri P, Löwe J (2010) The ParMRC system: Molecular mechanisms of plasmid segregation by actin-like filaments. Nat Rev Microbiol 8(10): 683-692.
28. Janke C, et al. (2004) A versatile toolbox for PCR-based tagging of yeast genes: New fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21(11): 947-962.
29. Voth WP, Richards JD, Shaw JM, Stillman DJ (2001) Yeast vectors for integration at the HO locus. Nucleic Acids Res 29(12): E59.
30. Thorsness PE, Fox TD (1993) Nuclear mutations in Saccharomyces cerevisiae that affect the escape of DNA from mitochondria to the nucleus. Genetics 134(1): 21-28.
31. Bonnefoy N, Fox TD (2002) Genetic transformation of Saccharomyces cerevisiae mitochondria. Methods Enzymol 350: 97-111.
32. Meeusen S, et al. (1999) Mgm101p is a novel component of the mitochondrial nucleoid that binds DNA and is required for the repair of oxidatively damaged mitochondrial DNA. J Cell Biol 145(2): 291-304.
33. Hoffman CS, Winston F (1987) A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57(2-3): 267-272.
34. MacAlpine DM, Perlman PS, Butow RA (2000) The numbers of individual mitochondrial DNA molecules and mitochondrial DNA nucleoids in yeast are co-regulated by the general amino acid control pathway. EMBO J 19(4): 767-775.
35. Carlton PM, et al. (2010) Fast live simultaneous multiwavelength four-dimensional optical microscopy. Proc Natl Acad Sci USA 107(37): 16016-16022.
36. Meisinger C, Pfanner N, Truscott KN (2006) Isolation of yeast mitochondria. Methods Mol Biol 313: 33-39.
37. Ameur A, et al. (2011) Ultra-deep sequencing of mouse mitochondrial DNA: Mutational patterns and their origins. PLoS Genet 7(3): e1002028.
38. Zeitouni B, et al. (2010) SVDetect: A tool to identify genomic structural variations from paired-end and mate-pair sequencing data. Bioinformatics 26(15): 1895-1896.
39. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4): 357-359.
40. Krzywinski M, et al. (2009) Circos: An information aesthetic for comparative genomics. Genome Res 19(9): 1639-1645.