Abstract
Nuclear respiratory-deficient mutants of Saccharomyces cerevisiae (pet mutants) have been screened for defects in the mitochondrial ATPase. Mutants in two complementation groups were found to have 10% or less of wild-type ATPase activity. The two wild-type nuclear genes defined by the mutants have been designated ATP11 and ATP12. The proteins encoded by the two genes are not subunits of the ATPase but rather appear to exercise an important function at a late stage in the synthesis of F1 after transport of the subunits into the internal compartment of mitochondria. Mitochondria of atp11 and atp12 mutants have only marginally reduced levels of the alpha and beta subunits of F1. Both proteins are processed to their mature size but are not part of a native F1 structure or associated with the mitochondrial membrane. The most reasonable explanation for the mutant phenotype is a block in the assembly of the F1 oligomer.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Burns D. J., Lewin A. S. The rate of import and assembly of F1-ATPase in Saccharomyces cerevisiae. J Biol Chem. 1986 Sep 15;261(26):12066–12073. [PubMed] [Google Scholar]
- Cheng M. Y., Hartl F. U., Martin J., Pollock R. A., Kalousek F., Neupert W., Hallberg E. M., Hallberg R. L., Horwich A. L. Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature. 1989 Feb 16;337(6208):620–625. doi: 10.1038/337620a0. [DOI] [PubMed] [Google Scholar]
- Crivellone M. D., Wu M. A., Tzagoloff A. Assembly of the mitochondrial membrane system. Analysis of structural mutants of the yeast coenzyme QH2-cytochrome c reductase complex. J Biol Chem. 1988 Oct 5;263(28):14323–14333. [PubMed] [Google Scholar]
- Ebner E., Schatz G. Mitochondrial assembly in respiration-deficient mutants of Saccharomyces cerevisiae. 3. A nuclear mutant lacking mitochondrial adenosine triphosphatase. J Biol Chem. 1973 Aug 10;248(15):5379–5384. [PubMed] [Google Scholar]
- Faye G., Kujawa C., Fukuhara H. Physical and genetic organization of petite and grande yeast mitochondrial DNA. IV. In vivo transcription products of mitochondrial DNA and localization of 23 S ribosomal RNA in petite mutants of saccharomyces cerevisiae. J Mol Biol. 1974 Sep 5;88(1):185–203. doi: 10.1016/0022-2836(74)90304-0. [DOI] [PubMed] [Google Scholar]
- Futai M., Kanazawa H. Structure and function of proton-translocating adenosine triphosphatase (F0F1): biochemical and molecular biological approaches. Microbiol Rev. 1983 Sep;47(3):285–312. doi: 10.1128/mr.47.3.285-312.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hemmingsen S. M., Woolford C., van der Vies S. M., Tilly K., Dennis D. T., Georgopoulos C. P., Hendrix R. W., Ellis R. J. Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature. 1988 May 26;333(6171):330–334. doi: 10.1038/333330a0. [DOI] [PubMed] [Google Scholar]
- Hensgens L. A., Grivell L. A., Borst P., Bos J. L. Nucleotide sequence of the mitochondrial structural gene for subunit 9 of yeast ATPase complex. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1663–1667. doi: 10.1073/pnas.76.4.1663. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Lewin A. S., Gregor I., Mason T. L., Nelson N., Schatz G. Cytoplasmically made subunits of yeast mitochondrial F1-ATPase and cytochrome c oxidase are synthesized as individual precursors, not as polyproteins. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3998–4002. doi: 10.1073/pnas.77.7.3998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maccecchini M. L., Rudin Y., Blobel G., Schatz G. Import of proteins into mitochondria: precursor forms of the extramitochondrially made F1-ATPase subunits in yeast. Proc Natl Acad Sci U S A. 1979 Jan;76(1):343–347. doi: 10.1073/pnas.76.1.343. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Macino G., Tzagoloff A. Assembly of the mitochondrial membrane system: sequence analysis of a yeast mitochondrial ATPase gene containing the oli-2 and oli-4 loci. Cell. 1980 Jun;20(2):507–517. doi: 10.1016/0092-8674(80)90637-6. [DOI] [PubMed] [Google Scholar]
- Macreadie I. G., Novitski C. E., Maxwell R. J., John U., Ooi B. G., McMullen G. L., Lukins H. B., Linnane A. W., Nagley P. Biogenesis of mitochondria: the mitochondrial gene (aap1) coding for mitochondrial ATPase subunit 8 in Saccharomyces cerevisiae. Nucleic Acids Res. 1983 Jul 11;11(13):4435–4451. doi: 10.1093/nar/11.13.4435. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Myers A. M., Tzagoloff A. MSW, a yeast gene coding for mitochondrial tryptophanyl-tRNA synthetase. J Biol Chem. 1985 Dec 5;260(28):15371–15377. [PubMed] [Google Scholar]
- Ng R., Abelson J. Isolation and sequence of the gene for actin in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3912–3916. doi: 10.1073/pnas.77.7.3912. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ostermann J., Horwich A. L., Neupert W., Hartl F. U. Protein folding in mitochondria requires complex formation with hsp60 and ATP hydrolysis. Nature. 1989 Sep 14;341(6238):125–130. doi: 10.1038/341125a0. [DOI] [PubMed] [Google Scholar]
- Penefsky H. S., Warner R. C. Partial resolution of the enzymes catalyzing oxidative phosphorylation. VI. Studies on the mechanism of cold inactivation of mitochondrial adenosine triphosphatase. J Biol Chem. 1965 Dec;240(12):4694–4702. [PubMed] [Google Scholar]
- Reading D. S., Hallberg R. L., Myers A. M. Characterization of the yeast HSP60 gene coding for a mitochondrial assembly factor. Nature. 1989 Feb 16;337(6208):655–659. doi: 10.1038/337655a0. [DOI] [PubMed] [Google Scholar]
- Rothstein R. J. One-step gene disruption in yeast. Methods Enzymol. 1983;101:202–211. doi: 10.1016/0076-6879(83)01015-0. [DOI] [PubMed] [Google Scholar]
- Ryrie I. J. The yeast mitochondrial adenosine triphosphatase complex. Purification, subunit composition, and some effects of protease inhibitors. Arch Biochem Biophys. 1977 Dec;184(2):464–475. doi: 10.1016/0003-9861(77)90456-8. [DOI] [PubMed] [Google Scholar]
- Schatz G. Impaired binding of mitochondrial adenosine triphosphatase in the cytoplasmic "petite" mutant of Saccharomyces cerevisiae. J Biol Chem. 1968 May 10;243(9):2192–2199. [PubMed] [Google Scholar]
- Schmidt R. J., Myers A. M., Gillham N. W., Boynton J. E. Immunological similarities between specific chloroplast ribosomal proteins from Chlamydomonas reinhardtii and ribosomal proteins from Escherichia coli. Mol Biol Evol. 1984 Jul;1(4):317–334. doi: 10.1093/oxfordjournals.molbev.a040320. [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]
- Takeda M., Vassarotti A., Douglas M. G. Nuclear genes coding the yeast mitochondrial adenosine triphosphatase complex. Primary sequence analysis of ATP2 encoding the F1-ATPase beta-subunit precursor. J Biol Chem. 1985 Dec 15;260(29):15458–15465. [PubMed] [Google Scholar]
- Todd R. D., McAda P. C., Douglas M. G. A nuclear mutation altering the assembly of the energy-transducing membrane of yeast. J Biol Chem. 1979 Nov 10;254(21):11134–11141. [PubMed] [Google Scholar]
- Tzagoloff A., Akai A., Foury F. Assembly of the mitochondrial membrane system XVI. Modified form of the ATPase proteolipid in oligomycin-resistant mutants of Saccharomyces cerevisiae. FEBS Lett. 1976 Jun 15;65(3):391–395. doi: 10.1016/0014-5793(76)80154-8. [DOI] [PubMed] [Google Scholar]
- Tzagoloff A., Akai A., Needleman R. B. Assembly of the mitochondrial membrane system. Characterization of nuclear mutants of Saccharomyces cerevisiae with defects in mitochondrial ATPase and respiratory enzymes. J Biol Chem. 1975 Oct 25;250(20):8228–8235. [PubMed] [Google Scholar]
- Tzagoloff A. Assembly of the mitochondrial membrane system. II. Synthesis of the mitochondrial adenosine triphosphatase. F1. J Biol Chem. 1969 Sep 25;244(18):5027–5033. [PubMed] [Google Scholar]
- Tzagoloff A. Assembly of the mitochondrial membrane system. IV. Role of mitochondrial and cytoplasmic protein synthesis in the biosynthesis of the rutamycin-sensitive adenosine triphosphatase. J Biol Chem. 1971 May 10;246(9):3050–3056. [PubMed] [Google Scholar]
- Tzagoloff A. Oligomycin-sensitive ATPase of Saccharomyces cerevisiae. Methods Enzymol. 1979;55:351–358. doi: 10.1016/0076-6879(79)55044-7. [DOI] [PubMed] [Google Scholar]
- Walker J. E., Fearnley I. M., Gay N. J., Gibson B. W., Northrop F. D., Powell S. J., Runswick M. J., Saraste M., Tybulewicz V. L. Primary structure and subunit stoichiometry of F1-ATPase from bovine mitochondria. J Mol Biol. 1985 Aug 20;184(4):677–701. doi: 10.1016/0022-2836(85)90313-4. [DOI] [PubMed] [Google Scholar]