Schizosaccharomyces pombe Sls1 is primarily required for cox1 mRNA translation.
Adenosine Triphosphate
/ metabolism
Carbon
/ metabolism
DNA, Mitochondrial
/ genetics
Electron Transport Complex IV
/ genetics
Glycerol
/ metabolism
Mitochondrial Proteins
/ genetics
Protein Biosynthesis
RNA, Messenger
/ genetics
Saccharomyces cerevisiae
/ genetics
Saccharomyces cerevisiae Proteins
/ genetics
Schizosaccharomyces
/ genetics
Sucrose
/ metabolism
Cox1
Schizosaccharomyces pombe
mitochondria
translation
Journal
Yeast (Chichester, England)
ISSN: 1097-0061
Titre abrégé: Yeast
Pays: England
ID NLM: 8607637
Informations de publication
Date de publication:
10 2022
10 2022
Historique:
revised:
26
07
2022
received:
07
04
2022
accepted:
08
09
2022
pubmed:
13
9
2022
medline:
12
10
2022
entrez:
12
9
2022
Statut:
ppublish
Résumé
Mitochondrial DNA (mtDNA) encodes essential subunits of the oxidative phosphorylation (OXPHOS) complexes; thus, the expression of mtDNA-encoded genes is essential for the synthesis of adenosine triphosphate. However, factors involved in mitochondrial translation have not been fully characterized. In this study, we characterized Schizosaccharomyces pombe Sls1, which has sequence similarity to Saccharomyces cerevisiae Sls1 that is required for the translation of all mtDNA-encoded messenger RNAs (mRNAs). Deletion of S. pombe sls1 severely impaired the growth of the cells on a rich medium containing the nonfermentable carbon source glycerol, which requires mitochondrial respiration. We found that the translation of mtDNA-encoded Cox1, the largest subunit of the cytochrome c oxidase complex, was severely impaired in Δsls1 cells. Deletion of S. pombe sls1 also resulted in a barely detectable steady-state level of mature cox1 mRNA. RNA immunoprecipitation showed that S. pombe Sls1 interacts with cox1 mRNA. Sucrose gradient sedimentation analysis revealed that S. pombe Sls1 is associated with the small subunit of mitochondrial ribosomes. Our results suggest that unlike S. cerevisiae Sls1, S. pombe Sls1 is primarily required for the accumulation and translation of cox1 mRNA.
Substances chimiques
DNA, Mitochondrial
0
Mitochondrial Proteins
0
RNA, Messenger
0
Saccharomyces cerevisiae Proteins
0
Sucrose
57-50-1
Carbon
7440-44-0
Adenosine Triphosphate
8L70Q75FXE
Cox1 protein, S cerevisiae
EC 1.9.3.1
Electron Transport Complex IV
EC 1.9.3.1
Glycerol
PDC6A3C0OX
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
521-534Informations de copyright
© 2022 John Wiley & Sons Ltd.
Références
Anziano, P. Q., Perlman, P. S., Lang, B. F., & Wolf, K. (1983). The mitochondrial genome of the fission yeast Schizosaccharomyces pombe: I. Isolation and physical mapping of mitochondrial DNA. Current Genetics, 7(4), 273-284. https://doi.org/10.1007/BF00376072
Bahler, J., Wu, J. Q., Longtine, M. S., Shah, N. G., McKenzie, A., 3rd, Steever, A. B., Wach, A., Philippsen, P., & Pringle, J. R. (1998). Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast, 14(10), 943-951. https://doi.org/10.1002/(sici)1097-0061(199807)14:10%3C943::aid-yea292%3E3.0.co;2-y
Barrientos, A., Zambrano, A., & Tzagoloff, A. (2004). Mss51p and Cox14p jointly regulate mitochondrial Cox1p expression in Saccharomyces cerevisiae. The EMBO Journal, 23(17), 3472-3482. https://doi.org/10.1038/sj.emboj.7600358
Bock, F. J., & Tait, S. W. G. (2020). Mitochondria as multifaceted regulators of cell death. Nature Reviews Molecular Cell Biology, 21(2), 85-100. https://doi.org/10.1038/s41580-019-0173-8
Bryan, A. C., Rodeheffer, M. S., Wearn, C. M., & Shadel, G. S. (2002). Sls1p is a membrane-bound regulator of transcription-coupled processes involved in Saccharomyces cerevisiae mitochondrial gene expression. Genetics, 160(1), 75-82. https://doi.org/10.1093/genetics/160.1.75
Chujo, T., Ohira, T., Sakaguchi, Y., Goshima, N., Nomura, N., Nagao, A., & Suzuki, T. (2012). LRPPRC/SLIRP suppresses PNPase-mediated mRNA decay and promotes polyadenylation in human mitochondria. Nucleic Acids Research, 40(16), 8033-8047. https://doi.org/10.1093/nar/gks506
De Silva, D., Fontanesi, F., & Barrientos, A. (2013). The DEAD box protein Mrh4 functions in the assembly of the mitochondrial large ribosomal subunit. Cell Metabolism, 18(5), 712-725. https://doi.org/10.1016/j.cmet.2013.10.007
De Silva, D., Tu, Y. T., Amunts, A., Fontanesi, F., & Barrientos, A. (2015). Mitochondrial ribosome assembly in health and disease. Cell Cycle, 14(14), 2226-2250. https://doi.org/10.1080/15384101.2015.1053672
De Silva, D., Poliquin, S., Zeng, R., Zamudio-Ochoa, A., Marrero, N., Perez-Martinez, X., Fontanesi, F., & Barrientos, A. (2017). The DEAD-box helicase Mss116 plays distinct roles in mitochondrial ribogenesis and mRNA-specific translation. Nucleic Acids Research, 45(11), 6628-6643. https://doi.org/10.1093/nar/gkx426
Dujeancourt, L., Richter, R., Chrzanowska-Lightowlers, Z. M., Bonnefoy, N., & Herbert, C. J. (2013). Interactions between peptidyl tRNA hydrolase homologs and the ribosomal release factor Mrf1 in S. pombe mitochondria. Mitochondrion, 13(6), 871-880. https://doi.org/10.1016/j.mito.2013.07.115
Forsburg, S. L. (1999). The best yeast? Trends in Genetics, 15(9), 340-344. https://doi.org/10.1016/s0168-9525(99)01798-9
Foury, F., Roganti, T., Lecrenier, N., & Purnelle, B. (1998). The complete sequence of the mitochondrial genome of Saccharomyces cerevisiae. FEBS Letters, 440(3), 325-331. https://doi.org/10.1016/s0014-5793(98)01467-7
Gouget, K., Verde, F., & Barrientos, A. (2008). In vivo labeling and analysis of mitochondrial translation products in budding and in fission yeasts. Methods in Molecular Biology, 457, 113-124. https://doi.org/10.1007/978-1-59745-261-8_8
Henze, K., & Martin, W. (2003). Evolutionary biology: Essence of mitochondria. Nature, 426(6963), 127-128. https://doi.org/10.1038/426127a
Herbert, C. J., Golik, P., & Bonnefoy, N. (2013). Yeast PPR proteins, watchdogs of mitochondrial gene expression. RNA Biology, 10(9), 1477-1494. https://doi.org/10.4161/rna.25392
Herbert, C. J., Labarre-Mariotte, S., Cornu, D., Sophie, C., Panozzo, C., Michel, T., Dujardin, G., & Bonnefoy, N. (2021). Translational activators and mitoribosomal isoforms cooperate to mediate mRNA-specific translation in Schizosaccharomyces pombe mitochondria. Nucleic Acids Research, 49(19), 11145-11166. https://doi.org/10.1093/nar/gkab789
Herrmann, J. M., Woellhaf, M. W., & Bonnefoy, N. (2013). Control of protein synthesis in yeast mitochondria: The concept of translational activators. Biochimica et Biophysic Acta, 1833(2), 286-294. https://doi.org/10.1016/j.bbamcr.2012.03.007
Jones, J. L., Hofmann, K. B., Cowan, A. T., Temiakov, D., Cramer, P., & Anikin, M. (2019). Yeast mitochondrial protein Pet111p binds directly to two distinct targets in COX2 mRNA, suggesting a mechanism of translational activation. Journal of Biological Chemistry, 294(18), 7528-7536. https://doi.org/10.1074/jbc.RA118.005355
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Zidek, A., Potapenko, A., Bridgland, A., Meyer, C., Kohl, S. A. A., Ballard, A. J., Cowie, A., Romera-Paredes, B., Nikolov, S., Jain, R., Adler, J., … Hassabis, D. (2021). Highly accurate protein structure prediction with AlphaFold. Nature, 596(7873), 583-589. https://doi.org/10.1038/s41586-021-03819-2
Kauppila, T. E. S., Kauppila, J. H. K., & Larsson, N. G. (2017). Mammalian mitochondria and aging: An update. Cell Metabolism, 25(1), 57-71. https://doi.org/10.1016/j.cmet.2016.09.017
Kim, D. U., Hayles, J., Kim, D., Wood, V., Park, H. O., Won, M., Yoo, H. S., Duhig, T., Nam, M., Palmer, G., Han, S., Jeffery, L., Baek, S. T., Lee, H., Shim, Y. S., Lee, M., Kim, L., Heo, K. S., Noh, E. J., … Hoe, K. L. (2010). Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe. Nature Biotechnology, 28(6), 617-623. https://doi.org/10.1038/nbt.1628
Kuhl, I., Fox, T. D., & 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(3), 381-390. https://doi.org/10.1016/j.mito.2012.02.002
Kuhl, I., Dujeancourt, L., Gaisne, M., Herbert, C. J., & Bonnefoy, N. (2011). A genome wide study in fission yeast reveals nine PPR proteins that regulate mitochondrial gene expression. Nucleic Acids Research, 39(18), 8029-8041. https://doi.org/10.1093/nar/gkr511
Kuzmenko, A., Atkinson, G. C., Levitskii, S., Zenkin, N., Tenson, T., Hauryliuk, V., & Kamenski, P. (2014). Mitochondrial translation initiation machinery: Conservation and diversification. Biochimie, 100, 132-140. https://doi.org/10.1016/j.biochi.2013.07.024
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-Sgm, 164(3), 400-409. https://doi.org/10.1099/mic.0.000602
Liu, Z., Li, Y., Xie, W., & Huang, Y. (2020). Schizosaccharomyces pombe Ppr10 is required for mitochondrial translation. FEMS Microbiology Letters, 367(19), fnaa170. https://doi.org/10.1093/femsle/fnaa170
Liu, Z., Ebrahim, A., Wu, X., Li, M., & Huang, Y. (2022). Loss of PPR protein Ppr2 induces ferroptosis-like cell death in Schizosaccharomyces pombe. Archives of Microbiology, 204(7) 360. https://doi.org/10.1007/s00203-022-02970-2
Luo, Y., Wang, Y., & Huang, Y. (2021). Schizosaccharomyces pombe Ppr10 and Mpa1 together mediate mitochondrial translational initiation. Journal of Biological Chemistry, 297(1), 100869. https://doi.org/10.1016/j.jbc.2021.100869
Luo, Y., Su, R., Wang, Y., Xie, W., Liu, Z., & Huang, Y. (2019). Schizosaccharomyces pombe Mti2 and Mti3 act in conjunction during mitochondrial translation initiation. The FEBS Journal, 286(22), 4542-4553. https://doi.org/10.1111/febs.15021
Meisinger, C., Pfanner, N., & Truscott, K. N. (2006). Isolation of yeast mitochondria. Methods in Molecular Biology, 313, 33-39. https://doi.org/10.1385/1-59259-958-3:033
Moreno, S., Klar, A., & Nurse, P. (1991). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods in Enzymology, 194, 795-823. https://doi.org/10.1016/0076-6879(91)94059-l
Nakagawa, S., Niimura, Y., Miura, K., & Gojobori, T. (2010). Dynamic evolution of translation initiation mechanisms in prokaryotes. Proceedings of the National Academy of Sciences of the United States of America, 107(14), 6382-6387. https://doi.org/10.1073/pnas.1002036107
Ott, M., Amunts, A., & Brown, A. (2016). Organization and regulation of mitochondrial protein synthesis. Annual Review of Biochemistry, 85, 77-101. https://doi.org/10.1146/annurev-biochem-060815-014334
Patch, A. M., & Aves, S. J. (2007). Fingerprinting fission yeast: Polymorphic markers for molecular genetic analysis of Schizosaccharomyces pombe strains. Microbiology, 153(Pt 3), 887-897. https://doi.org/10.1099/mic.0.2006/001669-0
Pearce, S. F., Rebelo-Guiomar, P., D'Souza, A. R., Powell, C. A., Van Haute, L., & Minczuk, M. (2017). Regulation of mammalian mitochondrial gene expression: Recent advances. Trends in Biochemical Sciences, 42(8), 625-639. https://doi.org/10.1016/j.tibs.2017.02.003
Perez-Martinez, X., Broadley, S. A., & Fox, T. D. (2003). Mss51p promotes mitochondrial Cox1p synthesis and interacts with newly synthesized Cox1p. The EMBO Journal, 22(21), 5951-5961. https://doi.org/10.1093/emboj/cdg566
Richman, T. R., Spahr, H., Ermer, J. A., Davies, S. M. K., Viola, H. M., Bates, K. A., Papadimitriou, J., Hool, L. C., Rodger, J., Larsson, N. G., Rackham, O., & Filipovska, A. (2016). Loss of the RNA-binding protein TACO1 causes late-onset mitochondrial dysfunction in mice. Nature Communications, 7, 11884. https://doi.org/10.1038/ncomms11884
Rodeheffer, M. S., & Shadel, G. S. (2003a). Multiple interactions involving the amino-terminal domain of yeast mtRNA polymerase determine the efficiency of mitochondrial protein synthesis. Journal of Biological Chemistry, 278(20), 18695-18701. https://doi.org/10.1074/jbc.M301399200
Rodeheffer, M. S., & Shadel, G. S. (2003b). Multiple interactions involving the amino-terminal domain of yeast mtRNA polymerase determine the efficiency of mitochondrial protein synthesis. Journal of Biological Chemistry, 278(20), 18695-18701. https://doi.org/10.1074/jbc.M301399200
Rodeheffer, M. S., Boone, B. E., Bryan, A. C., & Shadel, G. S. (2001). Nam1p, a protein involved in RNA processing and translation, is coupled to transcription through an interaction with yeast mitochondrial RNA polymerase. Journal of Biological Chemistry, 276(11), 8616-8622. https://doi.org/10.1074/jbc.m009901200
Roloff, G. A., & Henry, M. F. (2015). Mam33 promotes cytochrome c oxidase subunit I translation in Saccharomyces cerevisiae mitochondria. Molecular Biology of the Cell, 26(16), 2885-2894. https://doi.org/10.1091/mbc.E15-04-0222
Rutter, J., & Hughes, A. L. (2015). Power(2): The power of yeast genetics applied to the powerhouse of the cell. Trends in Endocrinology and Metabolism, 26(2), 59-68. https://doi.org/10.1016/j.tem.2014.12.002
Ruzzenente, B., Metodiev, M. D., Wredenberg, A., Bratic, A., Park, C. B., Camara, Y., Milenkovic, D., Zickermann, V., Wibom, R., Hultenby, K., Erdjument-Bromage, H., Tempst, P., Brandt, U., Stewart, J. B., Gustafsson, C. M., & Larsson, N. G. (2012). LRPPRC is necessary for polyadenylation and coordination of translation of mitochondrial mRNAs. The EMBO Journal, 31(2), 443-456. https://doi.org/10.1038/emboj.2011.392
Sasarman, F., Brunel-Guitton, C., Antonicka, H., Wai, T., Shoubridge, E. A., & Consortium, L. (2010). LRPPRC and SLIRP interact in a ribonucleoprotein complex that regulates posttranscriptional gene expression in mitochondria. Molecular Biology of the Cell, 21(8), 1315-1323. https://doi.org/10.1091/mbc.E10-01-0047
Schafer, B. (2005). RNA maturation in mitochondria of S. cerevisiae and S. pombe. Gene, 354, 80-85. https://doi.org/10.1016/j.gene.2005.03.032
Schafer, B., Gan, L., & Perlman, P. S. (2003). Reverse transcriptase and reverse splicing activities encoded by the mobile group II intron COBI1 of fission yeast mitochondrial DNA. Journal of Molecular Biology, 329(2), 191-206. https://doi.org/10.1016/S0022-2836(03)00441-8
Schafer, B., Hansen, M., & Lang, B. F. (2005). Transcription and RNA-processing in fission yeast mitochondria. RNA, 11(5), 785-795. https://doi.org/10.1261/rna.7252205
Schafer, B., Merlos-Lange, A. M., Anderl, C., Welser, F., Zimmer, M., & Wolf, K. (1991). The mitochondrial genome of fission yeast: Inability of all introns to splice autocatalytically, and construction and characterization of an intronless genome. Molecular and General Genetics, 225(1), 158-167. https://doi.org/10.1007/BF00282654
Smits, P., Smeitink, J., & van den Heuvel, L. (2010). Mitochondrial translation and beyond: Processes implicated in combined oxidative phosphorylation deficiencies. Journal of Biomedicine and Biotechnology, 2010, 737385. https://doi.org/10.1155/2010/737385
Su, Y., Yang, Y. M., & Huang, Y. (2017). Loss of ppr3, ppr4, ppr6, or ppr10 perturbs iron homeostasis and leads to apoptotic cell death in Schizosaccharomyces pombe. The FEBS Journal, 284(2), 324-337. https://doi.org/10.1111/febs.13978
Tavares-Carreon, F., Camacho-Villasana, Y., Zamudio-Ochoa, A., Shingu-Vazquez, M., Torres-Larios, A., & Perez-Martinez, X. (2008). The pentatricopeptide repeats present in pet309 are necessary for translation but not for stability of the mitochondrial COX1 mRNA in yeast. Journal of Biological Chemistry, 283(3), 1472-1479. https://doi.org/10.1074/jbc.M708437200
Varadi, M., Anyango, S., Deshpande, M., Nair, S., Natassia, C., Yordanova, G., Yuan, D., Stroe, O., Wood, G., Laydon, A., Zidek, A., Green, T., Tunyasuvunakool, K., Petersen, S., Jumper, J., Clancy, E., Green, R., Vora, A., Lutfi, M., … Velankar, S. (2022). AlphaFold Protein Structure Database: Massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Research, 50(D1), D439-D444. https://doi.org/10.1093/nar/gkab1061
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 Research, 45(6), 3323-3340. https://doi.org/10.1093/nar/gkx127
Weraarpachai, W., Antonicka, H., Sasarman, F., Seeger, J., Schrank, B., Kolesar, J. E., Lochmuller, H., Chevrette, M., Kaufman, B. A., Horvath, R., & Shoubridge, E. A. (2009). Mutation in TACO1, encoding a translational activator of COX I, results in cytochrome c oxidase deficiency and late-onset Leigh syndrome. Nature Genetics, 41(7), 833-896. https://doi.org/10.1038/ng.390
Zhang, Y., & Skolnick, J. (2005). TM-align: A protein structure alignment algorithm based on the TM-score. Nucleic Acids Research, 33(7), 2302-2309. https://doi.org/10.1093/nar/gki524