Crossref journal-article
Rockefeller University Press
Journal of Cell Biology (291)
Abstract

Mitochondria contain their own genetic system to express a small number of hydrophobic polypeptides, including cytochrome b, an essential subunit of the bc1 complex of the respiratory chain. In this paper, we show in yeast that Cbp3, a bc1 complex assembly factor, and Cbp6, a regulator of cytochrome b translation, form a complex that associates with the polypeptide tunnel exit of mitochondrial ribosomes and that exhibits two important functions in the biogenesis of cytochrome b. On the one hand, the interaction of Cbp3 and Cbp6 with mitochondrial ribosomes is necessary for efficient translation of cytochrome b transcript. On the other hand, the Cbp3–Cbp6 complex interacts directly with newly synthesized cytochrome b in an assembly intermediate that is not ribosome bound and that contains the assembly factor Cbp4. Our results suggest that synthesis of cytochrome b occurs preferentially on those ribosomes that have the Cbp3–Cbp6 complex bound to their tunnel exit, an arrangement that may ensure tight coordination of cytochrome b synthesis and assembly.

Authors 8
  1. Steffi Gruschke (first)
  2. Kirsten Kehrein (additional)
  3. Katharina Römpler (additional)
  4. Kerstin Gröne (additional)
  5. Lars Israel (additional)
  6. Axel Imhof (additional)
  7. Johannes M. Herrmann (additional)
  8. Martin Ott (additional)
References 48 Referenced 98
  1. 10.1038/sj.emboj.7600358 / EMBO J. / Mss51p and Cox14p jointly regulate mitochondrial Cox1p expression in Saccharomyces cerevisiae by Barrientos (2004)
  2. 10.1038/nature06683 / Nature. / A peptide deformylase-ribosome complex reveals mechanism of nascent chain processing by Bingel-Erlenmeyer (2008)
  3. 10.1007/PL00008646 / Mol. Gen. Genet. / In vivo analysis of mutated initiation codons in the mitochondrial COX2 gene of Saccharomyces cerevisiae fused to the reporter gene ARG8m reveals lack of downstream reinitiation by Bonnefoy (2000)
  4. 10.1007/978-1-59745-365-3_11 / Methods Mol. Biol. / Directed alteration of Saccharomyces cerevisiae mitochondrial DNA by biolistic transformation and homologous recombination by Bonnefoy (2007)
  5. 10.1016/0092-8674(78)90257-X / Cell. / The mitochondrial genome of yeast by Borst (1978)
  6. 10.1016/j.cell.2009.08.005 / Cell. / Importing mitochondrial proteins: machineries and mechanisms by Chacinska (2009)
  7. 10.1073/pnas.85.8.2677 / Proc. Natl. Acad. Sci. USA. / Specific translational activation by nuclear gene products occurs in the 5′ untranslated leader of a yeast mitochondrial mRNA by Costanzo (1988)
  8. 10.1016/S0021-9258(17)31961-0 / J. Biol. Chem. / Characterization of CBP4, a new gene essential for the expression of ubiquinol-cytochrome c reductase in Saccharomyces cerevisiae by Crivellone (1994)
  9. 10.1016/0092-8674(82)90051-4 / Cell. / Critical sequences within mitochondrial introns: pleiotropic mRNA maturase and cis-dominant signals of the box intron controlling reductase and oxidase by De La Salle (1982)
  10. 10.1073/pnas.78.3.1778 / Proc. Natl. Acad. Sci. USA. / Regulatory interactions between mitochondrial genes: interactions between two mosaic genes by Dhawale (1981)
  11. 10.1016/S0021-9258(18)89622-3 / J. Biol. Chem. / Assembly of the mitochondrial membrane system. CBP6, a yeast nuclear gene necessary for synthesis of cytochrome b by Dieckmann (1985)
  12. 10.1073/pnas.79.6.1805 / Proc. Natl. Acad. Sci. USA. / Identification and cloning of a yeast nuclear gene (CBP1) involved in expression of mitochondrial cytochrome b by Dieckmann (1982)
  13. 10.1016/S0021-9258(17)42907-3 / J. Biol. Chem. / Assembly of the mitochondrial membrane system. CBP1, a yeast nuclear gene involved in 5′ end processing of cytochrome b pre-mRNA by Dieckmann (1984)
  14. 10.1073/pnas.2135169100 / Proc. Natl. Acad. Sci. USA. / The two rotor components of yeast mitochondrial ATP synthase are mechanically coupled by subunit delta by Duvezin-Caubet (2003)
  15. 10.1128/MCB.18.4.1826 / Mol. Cell. Biol. / Functional interactions between yeast mitochondrial ribosomes and mRNA 5′ untranslated leaders by Green-Willms (1998)
  16. 10.1074/jbc.M110.113837 / J. Biol. Chem. / Proteins at the polypeptide tunnel exit of the yeast mitochondrial ribosome by Gruschke (2010)
  17. 10.1261/rna.2196403 / RNA. / The signal recognition particle binds to protein L23 at the peptide exit of the Escherichia coli ribosome by Gu (2003)
  18. 10.1093/genetics/127.2.319 / Genetics. / Functional interactions among two yeast mitochondrial ribosomal proteins and an mRNA-specific translational activator by Haffter (1991)
  19. 10.1074/jbc.M206132200 / J. Biol. Chem. / Cbp1 is required for translation of the mitochondrial cytochrome b mRNA of Saccharomyces cerevisiae by Islas-Osuna (2002)
  20. 10.1038/nature01047 / Nature. / L23 protein functions as a chaperone docking site on the ribosome by Kramer (2002)
  21. 10.1038/nsmb.1614 / Nat. Struct. Mol. Biol. / The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins by Kramer (2009)
  22. 10.1007/s00294-004-0503-y / Curr. Genet. / Saccharomyces cerevisiae translational activator Cbs2p is associated with mitochondrial ribosomes by Krause-Buchholz (2004)
  23. 10.1515/BC.2005.049 / Biol. Chem. / Saccharomyces cerevisiae translational activator Cbs1p is associated with translationally active mitochondrial ribosomes by Krause-Buchholz (2005)
  24. 10.1007/s00294-005-0561-9 / Curr. Genet. / Organization of assembly factors Cbp3p and Cbp4p and their effect on bc(1) complex assembly in Saccharomyces cerevisiae by Kronekova (2005)
  25. 10.1093/nar/24.17.3469 / Nucleic Acids Res. / One-step PCR mediated strategy for the construction of conditionally expressed and epitope tagged yeast proteins by Lafontaine (1996)
  26. 10.1016/j.mito.2010.12.002 / Mitochondrion. / A transcriptome screen in yeast identifies a novel assembly factor for the mitochondrial complex III by Mathieu (2011)
  27. {'key': '2023072302414287400_bib27', 'first-page': '4590', 'article-title': 'A novel small-subunit ribosomal protein of yeast mitochondria that interacts functionally with an mRNA-specific translational activator', 'volume': '10', 'author': 'McMullin', 'year': '1990', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / A novel small-subunit ribosomal protein of yeast mitochondria that interacts functionally with an mRNA-specific translational activator by McMullin (1990)
  28. 10.1016/S1097-2765(00)00118-0 / Mol. Cell. / The structure of ribosome-channel complexes engaged in protein translocation by Ménétret (2000)
  29. 10.1038/nrm3029 / Nat. Rev. Mol. Cell Biol. / Inventory control: cytochrome c oxidase assembly regulates mitochondrial translation by Mick (2011)
  30. 10.1146/annurev.biochem.76.052705.163409 / Annu. Rev. Biochem. / Translocation of proteins into mitochondria by Neupert (2007)
  31. 10.1002/j.1460-2075.1992.tb05474.x / EMBO J. / BCS1, a novel gene required for the expression of functional Rieske iron-sulfur protein in Saccharomyces cerevisiae by Nobrega (1992)
  32. 10.1534/genetics.106.063883 / Genetics. / Rmd9p controls the processing/stability of mitochondrial mRNAs and its overexpression compensates for a partial deficiency of oxa1p in Saccharomyces cerevisiae by Nouet (2007)
  33. 10.1093/emboj/cdg566 / EMBO J. / Mss51p promotes mitochondrial Cox1p synthesis and interacts with newly synthesized Cox1p by Perez-Martinez (2003)
  34. 10.1091/mbc.E08-12-1162 / Mol. Biol. Cell. / Mrpl36 is important for generation of assembly competent proteins during mitochondrial translation by Prestele (2009)
  35. 10.1073/pnas.0910351106 / Proc. Natl. Acad. Sci. USA. / F1-dependent translation of mitochondrially encoded Atp6p and Atp8p subunits of yeast ATP synthase by Rak (2009)
  36. 10.1074/jbc.M608692200 / J. Biol. Chem. / Yeast cells lacking the mitochondrial gene encoding the ATP synthase subunit 6 exhibit a selective loss of complex IV and unusual mitochondrial morphology by Rak (2007)
  37. 10.1007/BF00389424 / Curr. Genet. / Two yeast nuclear genes, CBS1 and CBS2, are required for translation of mitochondrial transcripts bearing the 5′-untranslated COB leader by Rödel (1986)
  38. 10.1007/s002940050219 / Curr. Genet. / Translational activator proteins required for cytochrome b synthesis in Saccharomyces cerevisiae by Rödel (1997)
  39. 10.1007/BF00326534 / Mol. Gen. Genet. / The yeast nuclear gene CBS1 is required for translation of mitochondrial mRNAs bearing the cob 5′ untranslated leader by Rödel (1987)
  40. 10.1016/S0092-8674(03)00762-1 / Cell. / Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins by Sharma (2003)
  41. 10.1073/pnas.0901631106 / Proc. Natl. Acad. Sci. USA. / Structure of a mitochondrial ribosome with minimal RNA by Sharma (2009)
  42. 10.1093/genetics/122.1.19 / Genetics. / A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae by Sikorski (1989)
  43. 10.1073/pnas.93.11.5253 / Proc. Natl. Acad. Sci. USA. / Expression of a recoded nuclear gene inserted into yeast mitochondrial DNA is limited by mRNA-specific translational activation by Steele (1996)
  44. 10.1016/S0021-9258(19)40840-5 / J. Biol. Chem. / Assembly of the mitochondrial membrane system. Characterization of nuclear mutants of Saccharomyces cerevisiae with defects in mitochondrial ATPase and respiratory enzymes by Tzagoloff (1975)
  45. 10.1128/EC.4.2.337-345.2005 / Eukaryot. Cell. / Alteration of a novel dispensable mitochondrial ribosomal small-subunit protein, Rsm28p, allows translation of defective COX2 mRNAs by Williams (2005)
  46. 10.1534/genetics.106.064576 / Genetics. / Translation initiation in Saccharomyces cerevisiae mitochondria: functional interactions among mitochondrial ribosomal protein Rsm28p, initiation factor 2, methionyl-tRNA-formyltransferase and novel protein Rmd9p by Williams (2007)
  47. 10.1016/S0021-9258(18)60438-7 / J. Biol. Chem. / Identification and characterization of a new gene (CBP3) required for the expression of yeast coenzyme QH2-cytochrome c reductase by Wu (1989)
  48. 10.1016/j.bbamcr.2008.04.011 / Biochim. Biophys. Acta. / Biogenesis of the yeast cytochrome bc1 complex by Zara (2009)
Dates
Type When
Created 14 years, 2 months ago (June 13, 2011, 4:58 p.m.)
Deposited 2 years, 1 month ago (July 22, 2023, 10:42 p.m.)
Indexed 1 month ago (July 25, 2025, 6:46 a.m.)
Issued 14 years, 2 months ago (June 13, 2011)
Published 14 years, 2 months ago (June 13, 2011)
Published Online 14 years, 2 months ago (June 13, 2011)
Published Print 14 years, 2 months ago (June 13, 2011)
Funders 0

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@article{Gruschke_2011, title={Cbp3–Cbp6 interacts with the yeast mitochondrial ribosomal tunnel exit and promotes cytochrome b synthesis and assembly}, volume={193}, ISSN={0021-9525}, url={http://dx.doi.org/10.1083/jcb.201103132}, DOI={10.1083/jcb.201103132}, number={6}, journal={Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Gruschke, Steffi and Kehrein, Kirsten and Römpler, Katharina and Gröne, Kerstin and Israel, Lars and Imhof, Axel and Herrmann, Johannes M. and Ott, Martin}, year={2011}, month=jun, pages={1101–1114} }