Schizosaccharomyces pombe Mti2 and Mti3 act in conjunction during mitochondrial translation initiation.


Journal

The FEBS journal
ISSN: 1742-4658
Titre abrégé: FEBS J
Pays: England
ID NLM: 101229646

Informations de publication

Date de publication:
11 2019
Historique:
received: 27 05 2019
revised: 23 06 2019
accepted: 24 07 2019
pubmed: 28 7 2019
medline: 17 6 2020
entrez: 28 7 2019
Statut: ppublish

Résumé

Mitochondrial DNA encodes key subunits of the oxidative phosphorylation complexes essential for ATP production. Translation initiation in mitochondria requires two general factors, mtIF2 and mtIF3, whose counterparts in bacteria are essential for protein synthesis. In this study, we report the characterization of the fission yeast Schizosaccharomyces pombe mtIF2 (Mti2) and mtIF3 (Mti3). Deletion of mti2 impairs cell growth on the respiratory medium. The growth defect of the mti2 deletion mutant can be suppressed by expressing IFM1, the Saccharomyces cerevisiae homolog of Mti2, demonstrating functional conservation between the two proteins. Deletion of mti2 also impairs mitochondrial protein synthesis. Unlike mti2, deletion of mti3 does not affect cell growth on respiratory media and mitochondrial translation. However, deletion of mti3 exacerbates the growth defect of the Δmti2 mutant, suggesting that the two proteins have distinct, but partially overlapping functions during the process of mitochondrial translation initiation in S. pombe. Both Mti2 and Mti3 are associated with the small subunit of the mitochondrial ribosome (mitoribosome). Disruption of mti2, but not mti3, causes dissociation of the mitoribosome and also abolishes Mti3 binding to the small subunit of the mitoribosome. Our results suggest that Mti2 and Mti3 bind in a sequential manner to the small subunit of the mitoribosome and that Mti3 facilitates the function of Mti2 in mitochondrial translation initiation. Our findings also support the view that the importance of the mitochondrial translation initiation factors varies among the organisms.

Identifiants

pubmed: 31350787
doi: 10.1111/febs.15021
doi:

Substances chimiques

Electron Transport Chain Complex Proteins 0
Eukaryotic Initiation Factors 0
Mitochondrial Proteins 0
Schizosaccharomyces pombe Proteins 0
mti2 protein, S pombe 0
mti3 protein, S pombe 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4542-4553

Subventions

Organisme : the Priority Academic Program Development of Jiangsu Higher Education Institutes
Pays : International
Organisme : National Natural Science Foundation of China
ID : 31770810
Pays : International

Informations de copyright

© 2019 Federation of European Biochemical Societies.

Références

Saraste M (1999) Oxidative phosphorylation at the fin de siecle. Science 283, 1488-1493.
Boczonadi V & Horvath R (2014) Mitochondria: impaired mitochondrial translation in human disease. Int J Biochem Cell Biol 48, 77-84.
Nicholls TJ, Rorbach J & Minczuk M (2013) Mitochondria: mitochondrial RNA metabolism and human disease. Int J Biochem Cell Biol 45, 845-849.
Christian BE & Spremulli LL (2012) Mechanism of protein biosynthesis in mammalian mitochondria. Biochim Biophys Acta 1819, 1035-1054.
Kuzmenko A, Atkinson GC, Levitskii S, Zenkin N, Tenson T, Hauryliuk V & Kamenski P (2014) Mitochondrial translation initiation machinery: conservation and diversification. Biochimie 100, 132-140.
Lightowlers RN, Rozanska A & Chrzanowska-Lightowlers ZM (2014) Mitochondrial protein synthesis: figuring the fundamentals, complexities and complications, of mammalian mitochondrial translation. FEBS Lett 588, 2496-2503.
Christian BE & Spremulli LL (2009) Evidence for an active role of IF3mt in the initiation of translation in mammalian mitochondria. Biochemistry 48, 3269-3278.
Haque ME, Grasso D & Spremulli LL (2008) The interaction of mammalian mitochondrial translational initiation factor 3 with ribosomes: evolution of terminal extensions in IF3mt. Nucleic Acids Res 36, 589-597.
Laursen BS, Sorensen HP, Mortensen KK & Sperling-Petersen HU (2005) Initiation of protein synthesis in bacteria. Microbiol Mol Biol Rev 69, 101-123.
Garofalo C, Trinko R, Kramer G, Appling DR & Hardesty B (2003) Purification and characterization of yeast mitochondrial initiation factor 2. Arch Biochem Biophys 413, 243-252.
Spencer AC & Spremulli LL (2004) Interaction of mitochondrial initiation factor 2 with mitochondrial fMet-tRNA. Nucleic Acids Res 32, 5464-5470.
Atkinson GC (2015) The evolutionary and functional diversity of classical and lesser-known cytoplasmic and organellar translational GTPases across the tree of life. BMC Genom 16, 78.
Yassin AS, Haque ME, Datta PP, Elmore K, Banavali NK, Spremulli LL & Agrawal RK (2011) Insertion domain within mammalian mitochondrial translation initiation factor 2 serves the role of eubacterial initiation factor 1. Proc Natl Acad Sci USA 108, 3918-3923.
Kummer E, Leibundgut M, Rackham O, Lee RG, Boehringer D, Filipovska A & Ban N (2018) Unique features of mammalian mitochondrial translation initiation revealed by cryo-EM. Nature 560, 263-267.
Bhargava K & Spremulli LL (2005) Role of the N- and C-terminal extensions on the activity of mammalian mitochondrial translational initiation factor 3. Nucleic Acids Res 33, 7011-7018.
Koripella RK, Sharma MR, Haque ME, Risteff P, Spremulli LL & Agrawal RK (2019) Structure of human mitochondrial translation initiation factor 3 bound to the small ribosomal subunit. iScience 12, 76-86.
Kuzmenko A, Derbikova K, Salvatori R, Tankov S, Atkinson GC, Tenson T, Ott M, Kamenski P & Hauryliuk V (2016) Aim-less translation: loss of Saccharomyces cerevisiae mitochondrial translation initiation factor mIF3/Aim23 leads to unbalanced protein synthesis. Sci Rep 6, 18749.
Ostojic J, Panozzo C, Bourand-Plantefol A, Herbert CJ, Dujardin G & Bonnefoy N (2016) Ribosome recycling defects modify the balance between the synthesis and assembly of specific subunits of the oxidative phosphorylation complexes in yeast mitochondria. Nucleic Acids Res 44, 5785-5797.
Ma L & Spremulli LL (1995) Cloning and sequence analysis of the human mitochondrial translational initiation factor 2 cDNA. J Biol Chem 270, 1859-1865.
Koc EC & Spremulli LL (2002) Identification of mammalian mitochondrial translational initiation factor 3 and examination of its role in initiation complex formation with natural mRNAs. J Biol Chem 277, 35541-35549.
Gaur R, Grasso D, Datta PP, Krishna PD, Das G, Spencer A, Agrawal RK, Spremulli L & Varshney U (2008) A single mammalian mitochondrial translation initiation factor functionally replaces two bacterial factors. Mol Cell 29, 180-190.
Atkinson GC, Kuzmenko A, Kamenski P, Vysokikh MY, Lakunina V, Tankov S, Smirnova E, Soosaar A, Tenson T & Hauryliuk V (2012) Evolutionary and genetic analyses of mitochondrial translation initiation factors identify the missing mitochondrial IF3 in S. cerevisiae. Nucleic Acids Res 40, 6122-6134.
Kuhl I, Dujeancourt L, Gaisne M, Herbert CJ & Bonnefoy N (2011) A genome wide study in fission yeast reveals nine PPR proteins that regulate mitochondrial gene expression. Nucleic Acids Res 39, 8029-8041.
Wang Y, Yan J, Zhang Q, Ma X, Zhang J, Su M, Wang X & Huang Y (2017) The Schizosaccharomyces pombe PPR protein Ppr10 associates with a novel protein Mpa1 and acts as a mitochondrial translational activator. Nucleic Acids Res 45, 3323-3340.
Su Y, Yang Y & Huang Y (2017) Loss of ppr3, ppr4, ppr6, or ppr10 perturbs iron homeostasis and leads to apoptotic cell death in Schizosaccharomyces pombe. FEBS J 284, 324-337.
Weraarpachai W, Antonicka H, Sasarman F, Seeger J, Schrank B, Kolesar JE, Lochmuller H, Chevrette M, Kaufman BA, Horvath R et al. (2009) Mutation in TACO1, encoding a translational activator of COX I, results in cytochrome c oxidase deficiency and late-onset Leigh syndrome. Nat Genet 41, 833-837.
Richman TR, Spahr H, Ermer JA, Davies SM, Viola HM, Bates KA, Papadimitriou J, Hool LC, Rodger J, Larsson NG et al. (2016) Loss of the RNA-binding protein TACO1 causes late-onset mitochondrial dysfunction in mice. Nat Commun 7, 11884.
Guillon JM, Mechulam Y, Schmitter JM, Blanquet S & Fayat G (1992) Disruption of the gene for Met-tRNA(fMet) formyltransferase severely impairs growth of Escherichia coli. J Bacteriol 174, 4294-4301.
Li Y, Holmes WB, Appling DR & RajBhandary UL (2000) Initiation of protein synthesis in Saccharomyces cerevisiae mitochondria without formylation of the initiator tRNA. J Bacteriol 182, 2886-2892.
Franco LVR, Moda BS, Soares M & Barros MH (2019) Msc6p is required for mitochondrial translation initiation in the absence of formylated Met-tRNA(fMet). FEBS J 286, 1407-1419.
Lee C, Tibbetts AS, Kramer G & Appling DR (2009) Yeast AEP3p is an accessory factor in initiation of mitochondrial translation. J Biol Chem 284, 34116-34125.
Williams EH, Butler CA, Bonnefoy N & Fox TD (2007) Translation initiation in Saccharomyces cerevisiae mitochondria: functional interactions among mitochondrial ribosomal protein Rsm28p, initiation factor 2, methionyl-tRNA-formyltransferase and novel protein Rmd9p. Genetics 175, 1117-1126.
Tucker EJ, Hershman SG, Kohrer C, Belcher-Timme CA, Patel J, Goldberger OA, Christodoulou J, Silberstein JM, McKenzie M, Ryan MT et al. (2011) Mutations in MTFMT underlie a human disorder of formylation causing impaired mitochondrial translation. Cell Metab 14, 428-434.
Zuin A, Gabrielli N, Calvo IA, Garcia-Santamarina S, Hoe KL, Kim DU, Park HO, Hayles J, Ayte J & Hidalgo E (2008) Mitochondrial dysfunction increases oxidative stress and decreases chronological life span in fission yeast. PLoS ONE 3, e2842.
Bin-Umer MA, McLaughlin JE, Butterly MS, McCormick S & Tumer NE (2014) Elimination of damaged mitochondria through mitophagy reduces mitochondrial oxidative stress and increases tolerance to trichothecenes. Proc Natl Acad Sci USA 111, 11798-11803.
Bonawitz ND, Rodeheffer MS & Shadel GS (2006) Defective mitochondrial gene expression results in reactive oxygen species-mediated inhibition of respiration and reduction of yeast life span. Mol Cell Biol 26, 4818-4829.
Matsuyama A, Arai R, Yashiroda Y, Shirai A, Kamata A, Sekido S, Kobayashi Y, Hashimoto A, Hamamoto M, Hiraoka Y et al. (2006) ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe. Nat Biotechnol 24, 841-847.
Myers AM, Pape LK & Tzagoloff A (1985) Mitochondrial protein synthesis is required for maintenance of intact mitochondrial genomes in Saccharomyces cerevisiae. EMBO J 4, 2087-2092.
Chu Z, Li J, Eshaghi M, Karuturi RK, Lin K & Liu J (2007) Adaptive expression responses in the Pol-γ null strain of S. pombe depleted of mitochondrial genome. BMC Genom 8, 323.
Haffter P & Fox TD (1992) Nuclear mutations in the petite-negative yeast Schizosaccharomyces pombe allow growth of cells lacking mitochondrial DNA. Genetics 131, 255-260.
Gouget K, Verde F & Barrientos A (2008) In vivo labeling and analysis of mitochondrial translation products in budding and in fission yeasts. Methods Mol Biol 457, 113-124.
Liu J, Li Y, Chen J, Wang Y, Zou M, Su R & Huang Y (2018) The fission yeast Schizosaccharomyces pombe Mtf2 is required for mitochondrial cox1 gene expression. Microbiology 164, 400-409.
Kuhl I, Fox TD & Bonnefoy N (2012) Schizosaccharomyces pombe homologs of the Saccharomyces cerevisiae mitochondrial proteins Cbp6 and Mss51 function at a post-translational step of respiratory complex biogenesis. Mitochondrion 12, 381-390.
Hussain T, Llacer JL, Wimberly BT, Kieft JS & Ramakrishnan V (2016) Large-Scale Movements of IF3 and tRNA during Bacterial Translation Initiation. Cell 167, 133-144.e13.
Moreno S, Klar A & Nurse P (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194, 795-823.
Wright A, Maundrell K, Heyer WD, Beach D & Nurse P (1986) Vectors for the construction of gene banks and the integration of cloned genes in Schizosaccharomyces pombe and Saccharomyces cerevisiae. Plasmid 15, 156-158.
Gan X, Yang J, Li J, Yu H, Dai H, Liu J & Huang Y (2011) The fission yeast Schizosaccharomyces pombe has two distinct tRNase ZLs encoded by two different genes and differentially targeted to the nucleus and mitochondria. Biochem J 435, 103-111.
Lemaire C & Dujardin G (2008) Preparation of respiratory chain complexes from Saccharomyces cerevisiae wild-type and mutant mitochondria: activity measurement and subunit composition analysis. Methods Mol Biol 432, 65-81.

Auteurs

Ying Luo (Y)

Jiangsu Key Laboratory for Microbes and Functional Genomics, School of Life Sciences, Nanjing Normal University, China.

Ruyue Su (R)

Jiangsu Key Laboratory for Microbes and Functional Genomics, School of Life Sciences, Nanjing Normal University, China.

Yirong Wang (Y)

Jiangsu Key Laboratory for Microbes and Functional Genomics, School of Life Sciences, Nanjing Normal University, China.

Wanqiu Xie (W)

Jiangsu Key Laboratory for Microbes and Functional Genomics, School of Life Sciences, Nanjing Normal University, China.

Zecheng Liu (Z)

Jiangsu Key Laboratory for Microbes and Functional Genomics, School of Life Sciences, Nanjing Normal University, China.

Ying Huang (Y)

Jiangsu Key Laboratory for Microbes and Functional Genomics, School of Life Sciences, Nanjing Normal University, China.

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