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PMID: 11805046 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Sls1p is a membrane-bound regulator of transcription-coupled processes involved in Saccharomyces cerevisiae mitochondrial gene expression.

Genetics ·Vol. 160 ·No. 1 ·2002-01-00 ·Pages 75-82

Bryan AC, Rodeheffer MS, Wearn CM, Shadel GS

Abstract

Mitochondrial translation is largely membrane-associated in S. cerevisiae. Recently, we discovered that the matrix protein Nam1p binds the amino-terminal domain of yeast mtRNA polymerase to couple translation and/or RNA-processing events to transcription. To gain additional insight into these transcription-coupled processes, we performed a genetic screen for genes that suppress the petite phenotype of a point mutation in mtRNA polymerase (rpo41-R129D) when overexpressed. One suppressor identified in this screen was SLS1, which encodes a mitochondrial membrane protein required for assembly of respiratory-chain enzyme complexes III and IV. The mtRNA-processing defects associated with the rpo41-R129D mutation were corrected in the suppressed strain, linking Sls1p to a pathway that includes mtRNA polymerase and Nam1p. This was supported by the observation that SLS1 overexpression rescued the petite phenotype of a NAM1 null mutation. In contrast, overexpression of Nam1p did not rescue the petite phenotype of a SLS1 null mutation, indicating that Nam1p and Sls1p are not functionally redundant but rather exist in an ordered pathway. On the basis of these data, a model in which Nam1p coordinates the delivery of newly synthesized transcripts to the membrane, where Sls1p directs or regulates their subsequent handling by membrane-bound factors involved in translation, is proposed.

MeSH Terms
Apoproteins/metabolism Carrier Proteins/genetics,metabolism,physiology Cytochrome b Group/metabolism Cytochromes b DNA, Mitochondrial/genetics DNA-Directed RNA Polymerases/metabolism Fungal Proteins Gene Expression/physiology Gene Expression Regulation, Fungal/physiology Membrane Proteins/genetics,physiology Mitochondria/genetics Mitochondrial Proteins RNA/metabolism RNA, Fungal/metabolism RNA, Mitochondrial Saccharomyces cerevisiae/genetics Saccharomyces cerevisiae Proteins/genetics,metabolism,physiology Transcription Factors/metabolism Transcription, Genetic
Chemicals
Apoproteins Carrier Proteins Cytochrome b Group DNA, Mitochondrial Fungal Proteins MTF2 protein, S cerevisiae Membrane Proteins Mitochondrial Proteins RNA, Fungal RNA, Mitochondrial SLS1 protein, S cerevisiae Saccharomyces cerevisiae Proteins Transcription Factors RNA Cytochromes b DNA-Directed RNA Polymerases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Bryan Anthony C
Department of Biochemistry, Rollins Research Center, Emory University School of Medicine, Atlanta, Georgia 30322, USA.
Rodeheffer Matthew S
Wearn Christopher M
Shadel Gerald S
References (30)
30 references, click to expand
  1. The PPR motif - a TPR-related motif prevalent in plant organellar proteins.
    Trends Biochem Sci. 2000 Feb;25(2):46-7 PMID: 10664580
  2. Getting started with yeast.
    Methods Enzymol. 1991;194:3-21 PMID: 2005794
  3. Interaction of mammalian mitochondrial ribosomes with the inner membrane.
    J Biol Chem. 2000 Sep 22;275(38):29400-6 PMID: 10887179
  4. Pet111p, an inner membrane-bound translational activator that limits expression of the Saccharomyces cerevisiae mitochondrial gene COX2.
    J Biol Chem. 2001 Mar 2;276(9):6392-7 PMID: 11106667
  5. The genetics and pathology of oxidative phosphorylation.
    Nat Rev Genet. 2001 May;2(5):342-52 PMID: 11331900
  6. Nam1p, a protein involved in RNA processing and translation, is coupled to transcription through an interaction with yeast mitochondrial RNA polymerase.
    J Biol Chem. 2001 Mar 16;276(11):8616-22 PMID: 11118450
  7. Lack of mitochondrial anionic phospholipids causes an inhibition of translation of protein components of the electron transport chain. A yeast genetic model system for the study of anionic phospholipid function in mitochondria.
    J Biol Chem. 2001 Jul 6;276(27):25262-72 PMID: 11335731
  8. Biogenesis of mitochondria. The effects of membrane unsaturated fatty acid content on the activity and assembly of the yeast mitochondrial protein-synthesizing system.
    Arch Biochem Biophys. 1975 Aug;169(2):591-600 PMID: 126665
  9. Biogenesis of mitochondria 51: biochemical characterization of a mitochondrial mutation in Saccharomyces cerevisiae affecting the mitochondrial ribosome by conferring resistance to aminoglycoside antibiotics.
    Mol Gen Genet. 1979 Jun 7;173(2):159-70 PMID: 386034
  10. Yeast RPO41 gene product is required for transcription and maintenance of the mitochondrial genome.
    Proc Natl Acad Sci U S A. 1986 May;83(10):3391-4 PMID: 3517858
  11. Yeast mitochondrial RNA polymerase is homologous to those encoded by bacteriophages T3 and T7.
    Cell. 1987 Oct 9;51(1):89-99 PMID: 3308116
  12. Biogenesis of mitochondria.
    Annu Rev Cell Biol. 1988;4:289-333 PMID: 2461720
  13. Novel class of nuclear genes involved in both mRNA splicing and protein synthesis in Saccharomyces cerevisiae mitochondria.
    Mol Gen Genet. 1989 Feb;215(3):517-28 PMID: 2651895
  14. 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 PMID: 2659436
  15. A novel small-subunit ribosomal protein of yeast mitochondria that interacts functionally with an mRNA-specific translational activator.
    Mol Cell Biol. 1990 Sep;10(9):4590-5 PMID: 2167435
  16. Lambda YES: a multifunctional cDNA expression vector for the isolation of genes by complementation of yeast and Escherichia coli mutations.
    Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1731-5 PMID: 1848010
  17. Control of mitochondrial gene expression in Saccharomyces cerevisiae.
    Annu Rev Genet. 1990;24:91-113 PMID: 2088182
  18. COX3 mRNA-specific translational activator proteins are associated with the inner mitochondrial membrane in Saccharomyces cerevisiae.
    J Biol Chem. 1993 Jun 5;268(16):11737-41 PMID: 8389363
  19. The NAM1/MTF2 nuclear gene product is selectively required for the stability and/or processing of mitochondrial transcripts of the atp6 and of the mosaic, cox1 and cytb genes in Saccharomyces cerevisiae.
    Mol Gen Genet. 1993 Sep;240(3):419-27 PMID: 8413192
  20. The biology of yeast mitochondrial introns.
    Mol Biol Rep. 1993 Jun;18(1):1-13 PMID: 8232290
  21. The NAM1 protein (NAM1p), which is selectively required for cox1, cytb and atp6 transcript processing/stabilisation, is located in the yeast mitochondrial matrix.
    Eur J Biochem. 1994 May 15;222(1):27-32 PMID: 8200349
  22. Regulation of mitochondrial gene expression in Saccharomyces cerevisiae.
    Int Rev Cytol. 1994;152:145-81 PMID: 8206703
  23. SLS1, a new Saccharomyces cerevisiae gene involved in mitochondrial metabolism, isolated as a syntheticlethal in association with an SSM4 deletion.
    Mol Gen Genet. 1996 Oct 28;252(6):700-8 PMID: 8917313
  24. Pet127p, a membrane-associated protein involved in stability and processing of Saccharomyces cerevisiae mitochondrial RNAs.
    Mol Cell Biol. 1997 May;17(5):2816-24 PMID: 9111353
  25. Mitochondrial DNA maintenance in vertebrates.
    Annu Rev Biochem. 1997;66:409-35 PMID: 9242913
  26. The Saccharomyces cerevisiae Pet309 protein is embedded in the mitochondrial inner membrane.
    Eur J Biochem. 1998 Jul 1;255(1):156-61 PMID: 9692914
  27. Accumulation of mitochondrially synthesized Saccharomyces cerevisiae Cox2p and Cox3p depends on targeting information in untranslated portions of their mRNAs.
    EMBO J. 1998 Oct 1;17(19):5796-804 PMID: 9755179
  28. Mitochondrial diseases in man and mouse.
    Science. 1999 Mar 5;283(5407):1482-8 PMID: 10066162
  29. Yeast as a model for human mtDNA replication.
    Am J Hum Genet. 1999 Nov;65(5):1230-7 PMID: 10521287
  30. Pentamidine inhibits mitochondrial intron splicing and translation in Saccharomyces cerevisiae.
    RNA. 2000 Jul;6(7):937-51 PMID: 10917591
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
2002-01-00
Pages
75-82
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1461927
Subset
IM
Grants
NHLBI NIH HHS · HL-59655 · United States
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