Abstract
Inactivation of the yeast nuclear gene YMe2 causes an increased rate of DNA escape from mitochondria to the nucleus. Mutations in yme2 also show genetic interactions with yme1, a second gene that affects DNA escape from mitochondria to the nucleus. The yme1 cold-sensitive growth phenotype is suppressed by yme2 mutations. In addition, yme1 yme2 double mutants exhibit a synthetic growth defect on ethanol-glycerol medium at 30 degrees C. YME2 was isolated by complementation of the synthetic growth defect of yme1 yme2 strains and was found to be identical with the previously cloned RNA12 gene. The dominant temperature-sensitive mutation RNA12-1 prevents growth of yeast cells at 37 degrees C. YME2 encodes a protein with a predicted molecular weight of 96,681 and is an integral inner mitochondrial membrane protein. The larger carboxyl-terminal domain of the YME2 gene product faces the intermembrane space. Null alleles of yme2 display the same genetic interactions with yme1 and high rate of DNA escape from mitochondria as do the originally isolated yme2 mutant strains. Disruption of yme2 causes a strain-dependent growth defect on nonfermentable carbon sources.
Full Text
The Full Text of this article is available as a PDF (472.6 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Alani E., Cao L., Kleckner N. A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disrupted yeast strains. Genetics. 1987 Aug;116(4):541–545. doi: 10.1534/genetics.112.541.test. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
- Baker K. P., Schatz G. Mitochondrial proteins essential for viability mediate protein import into yeast mitochondria. Nature. 1991 Jan 17;349(6306):205–208. doi: 10.1038/349205a0. [DOI] [PubMed] [Google Scholar]
- Burgess S. M., Delannoy M., Jensen R. E. MMM1 encodes a mitochondrial outer membrane protein essential for establishing and maintaining the structure of yeast mitochondria. J Cell Biol. 1994 Sep;126(6):1375–1391. doi: 10.1083/jcb.126.6.1375. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burns N., Grimwade B., Ross-Macdonald P. B., Choi E. Y., Finberg K., Roeder G. S., Snyder M. Large-scale analysis of gene expression, protein localization, and gene disruption in Saccharomyces cerevisiae. Genes Dev. 1994 May 1;8(9):1087–1105. doi: 10.1101/gad.8.9.1087. [DOI] [PubMed] [Google Scholar]
- Campbell C. L., Tanaka N., White K. H., Thorsness P. E. Mitochondrial morphological and functional defects in yeast caused by yme1 are suppressed by mutation of a 26S protease subunit homologue. Mol Biol Cell. 1994 Aug;5(8):899–905. doi: 10.1091/mbc.5.8.899. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Costanzo M. C., Fox T. D. Product of Saccharomyces cerevisiae nuclear gene PET494 activates translation of a specific mitochondrial mRNA. Mol Cell Biol. 1986 Nov;6(11):3694–3703. doi: 10.1128/mcb.6.11.3694. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Daum G., Böhni P. C., 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] [Google Scholar]
- Fujiki Y., Hubbard A. L., Fowler S., Lazarow P. B. Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J Cell Biol. 1982 Apr;93(1):97–102. doi: 10.1083/jcb.93.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Glick B. S., Brandt A., Cunningham K., Müller S., Hallberg R. L., Schatz G. Cytochromes c1 and b2 are sorted to the intermembrane space of yeast mitochondria by a stop-transfer mechanism. Cell. 1992 May 29;69(5):809–822. doi: 10.1016/0092-8674(92)90292-k. [DOI] [PubMed] [Google Scholar]
- Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
- Lacroute F., Huet J., Exinger F. Dominant and semidominant mutations leading to thermosensitivity of ribonucleic acid biosynthesis in Saccharomyces cerevisiae. J Bacteriol. 1975 Jun;122(3):847–854. doi: 10.1128/jb.122.3.847-854.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lawson J. E., Douglas M. G. Separate genes encode functionally equivalent ADP/ATP carrier proteins in Saccharomyces cerevisiae. Isolation and analysis of AAC2. J Biol Chem. 1988 Oct 15;263(29):14812–14818. [PubMed] [Google Scholar]
- Leighton J., Schatz G. An ABC transporter in the mitochondrial inner membrane is required for normal growth of yeast. EMBO J. 1995 Jan 3;14(1):188–195. doi: 10.1002/j.1460-2075.1995.tb06989.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liang S., Alksne L., Warner J. R., Lacroute F. rna12+, a gene of Saccharomyces cerevisiae involved in pre-rRNA maturation. Characterization of a temperature-sensitive mutant, cloning and sequencing of the gene. Mol Gen Genet. 1992 Mar;232(2):304–312. doi: 10.1007/BF00280010. [DOI] [PubMed] [Google Scholar]
- McConnell S. J., Stewart L. C., Talin A., Yaffe M. P. Temperature-sensitive yeast mutants defective in mitochondrial inheritance. J Cell Biol. 1990 Sep;111(3):967–976. doi: 10.1083/jcb.111.3.967. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Paul M. F., Ackerman S., Yue J., Arselin G., Velours J., Tzagolof A., Ackermann S [corrected to Ackerman S. ]. Cloning of the yeast ATP3 gene coding for the gamma-subunit of F1 and characterization of atp3 mutants. J Biol Chem. 1994 Oct 21;269(42):26158–26164. [PubMed] [Google Scholar]
- Pillus L., Solomon F. Components of microtubular structures in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2468–2472. doi: 10.1073/pnas.83.8.2468. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roise D., Schatz G. Mitochondrial presequences. J Biol Chem. 1988 Apr 5;263(10):4509–4511. [PubMed] [Google Scholar]
- Rose M. D., Novick P., Thomas J. H., Botstein D., Fink G. R. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene. 1987;60(2-3):237–243. doi: 10.1016/0378-1119(87)90232-0. [DOI] [PubMed] [Google Scholar]
- Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sikorski R. S., 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. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Silva J. T., Verícimo M. A., Floriano W. B., Dutra M. B., Panek A. D. On the hsp26 of Saccharomyces cerevisiae. Biochem Mol Biol Int. 1994 May;33(2):211–220. [PubMed] [Google Scholar]
- Singer R. A., Johnston G. C., Bedard D. Methionine analogs and cell division regulation in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1978 Dec;75(12):6083–6087. doi: 10.1073/pnas.75.12.6083. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith D. B., Johnson K. S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 1988 Jul 15;67(1):31–40. doi: 10.1016/0378-1119(88)90005-4. [DOI] [PubMed] [Google Scholar]
- Takeda M., Chen W. J., Saltzgaber J., Douglas M. G. Nuclear genes encoding the yeast mitochondrial ATPase complex. Analysis of ATP1 coding the F1-ATPase alpha-subunit and its assembly. J Biol Chem. 1986 Nov 15;261(32):15126–15133. [PubMed] [Google Scholar]
- Thorsness P. E., Fox T. D. Escape of DNA from mitochondria to the nucleus in Saccharomyces cerevisiae. Nature. 1990 Jul 26;346(6282):376–379. doi: 10.1038/346376a0. [DOI] [PubMed] [Google Scholar]
- Thorsness P. E., Fox T. D. Nuclear mutations in Saccharomyces cerevisiae that affect the escape of DNA from mitochondria to the nucleus. Genetics. 1993 May;134(1):21–28. doi: 10.1093/genetics/134.1.21. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thorsness P. E., White K. H., Fox T. D. Inactivation of YME1, a member of the ftsH-SEC18-PAS1-CDC48 family of putative ATPase-encoding genes, causes increased escape of DNA from mitochondria in Saccharomyces cerevisiae. Mol Cell Biol. 1993 Sep;13(9):5418–5426. doi: 10.1128/mcb.13.9.5418. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Veinot-Drebot L. M., Singer R. A., Johnston G. C. rRNA transcription initiation is decreased by inhibitors of the yeast cell cycle control step "start". J Biol Chem. 1989 Nov 25;264(33):19528–19534. [PubMed] [Google Scholar]
- Weber E. R., Hanekamp T., Thorsness P. E. Biochemical and functional analysis of the YME1 gene product, an ATP and zinc-dependent mitochondrial protease from S. cerevisiae. Mol Biol Cell. 1996 Feb;7(2):307–317. doi: 10.1091/mbc.7.2.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weber E. R., Rooks R. S., Shafer K. S., Chase J. W., Thorsness P. E. Mutations in the mitochondrial ATP synthase gamma subunit suppress a slow-growth phenotype of yme1 yeast lacking mitochondrial DNA. Genetics. 1995 Jun;140(2):435–442. doi: 10.1093/genetics/140.2.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yaffe M. P., Jensen R. E., Guido E. C. 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] [Google Scholar]