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. 1988 Apr;85(8):2677–2681. doi: 10.1073/pnas.85.8.2677

Specific translational activation by nuclear gene products occurs in the 5' untranslated leader of a yeast mitochondrial mRNA.

M C Costanzo 1, T D Fox 1
PMCID: PMC280061  PMID: 2833749

Abstract

Translation of the yeast mitochondrial mRNA encoding cytochrome c oxidase subunit III (coxIII) is specifically activated by the products of at least three nuclear genes, PET494, PET54, and PET122. To investigate whether the target site for translational activation is within the 5' untranslated leader of the coxIII mRNA, we asked whether translation of another mitochondrial protein, apo-cytochrome b, from a chimeric mRNA bearing the coxIII mRNA leader required PET494, PET54, or PET122. Mutations in any of these three genes abolished translation of cytochrome b from an mRNA bearing the 5' two-thirds of the coxIII mRNA 5' untranslated leader, showing that all three gene products are required for translation of the chimeric mRNA and must act within the 5' two-thirds of the coxIII mRNA leader. Our data suggest that in wild-type cells, the specific activation of coxIII translation by PET494, PET54, and PET122 occurs by the action of these three gene products at a site or sites in a region of the 5' untranslated leader at least 172 nucleotides upstream of the initiation codon.

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Selected References

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  1. Ammerer G. Expression of genes in yeast using the ADCI promoter. Methods Enzymol. 1983;101:192–201. doi: 10.1016/0076-6879(83)01014-9. [DOI] [PubMed] [Google Scholar]
  2. Bonitz S. G., Homison G., Thalenfeld B. E., Tzagoloff A., Nobrega F. G. Assembly of the mitochondrial membrane system. Processing of the apocytochrome b precursor RNAs in Saccharomyces cerevisiae D273-10B. J Biol Chem. 1982 Jun 10;257(11):6268–6274. [PubMed] [Google Scholar]
  3. Bonitz S. G., Homison G., Thalenfeld B. E., Tzagoloff A., Nobrega F. G. Assembly of the mitochondrial membrane system. Processing of the apocytochrome b precursor RNAs in Saccharomyces cerevisiae D273-10B. J Biol Chem. 1982 Jun 10;257(11):6268–6274. [PubMed] [Google Scholar]
  4. Cabral F., Schatz G. Identification of cytochrome c oxidase subunits in nuclear yeast mutants lacking the functional enzyme. J Biol Chem. 1978 Jun 25;253(12):4396–4401. [PubMed] [Google Scholar]
  5. Coruzzi G., Bonitz S. G., Thalenfeld B. E., Tzagoloff A. Assembly of the mitochondrial membrane system. Analysis of the nucleotide sequence and transcripts in the oxi1 region of yeast mitochondrial DNA. J Biol Chem. 1981 Dec 25;256(24):12780–12787. [PubMed] [Google Scholar]
  6. Costanzo M. C., Fox T. D. Product of Saccharomyces cerevisiae nuclear gene PET494 activates translation of a specific mitochondrial mRNA. Mol Cell Biol. 1986 Nov;6(11):3694–3703. doi: 10.1128/mcb.6.11.3694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Costanzo M. C., Seaver E. C., Fox T. D. At least two nuclear gene products are specifically required for translation of a single yeast mitochondrial mRNA. EMBO J. 1986 Dec 20;5(13):3637–3641. doi: 10.1002/j.1460-2075.1986.tb04693.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dieckmann C. L., Tzagoloff A. Assembly of the mitochondrial membrane system. CBP6, a yeast nuclear gene necessary for synthesis of cytochrome b. J Biol Chem. 1985 Feb 10;260(3):1513–1520. [PubMed] [Google Scholar]
  9. Ebner E., Mennucci L., Schatz G. Mitochondrial assembly in respiration-deficient mutants of Saccharomyces cerevisiae. I. Effect of nuclear mutations on mitochondrial protein synthesis. J Biol Chem. 1973 Aug 10;248(15):5360–5368. [PubMed] [Google Scholar]
  10. Hultmark D., Klemenz R., Gehring W. J. Translational and transcriptional control elements in the untranslated leader of the heat-shock gene hsp22. Cell. 1986 Feb 14;44(3):429–438. doi: 10.1016/0092-8674(86)90464-2. [DOI] [PubMed] [Google Scholar]
  11. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Klemenz R., Hultmark D., Gehring W. J. Selective translation of heat shock mRNA in Drosophila melanogaster depends on sequence information in the leader. EMBO J. 1985 Aug;4(8):2053–2060. doi: 10.1002/j.1460-2075.1985.tb03891.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kloeckener-Gruissem B., McEwen J. E., Poyton R. O. Nuclear functions required for cytochrome c oxidase biogenesis in Saccharomyces cerevisiae: multiple trans-acting nuclear genes exert specific effects on expression of each of the cytochrome c oxidase subunits encoded on mitochondrial DNA. Curr Genet. 1987;12(5):311–322. doi: 10.1007/BF00405753. [DOI] [PubMed] [Google Scholar]
  14. Kozak M. Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles. Microbiol Rev. 1983 Mar;47(1):1–45. doi: 10.1128/mr.47.1.1-45.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lopata M. A., Sollner-Webb B., Cleveland D. W. Surprising S1-resistant trimolecular hybrids: potential complication in interpretation of S1 mapping analyses. Mol Cell Biol. 1985 Oct;5(10):2842–2846. doi: 10.1128/mcb.5.10.2842. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. McEwen J. E., Ko C., Kloeckner-Gruissem B., Poyton R. O. Nuclear functions required for cytochrome c oxidase biogenesis in Saccharomyces cerevisiae. Characterization of mutants in 34 complementation groups. J Biol Chem. 1986 Sep 5;261(25):11872–11879. [PubMed] [Google Scholar]
  17. McGarry T. J., Lindquist S. The preferential translation of Drosophila hsp70 mRNA requires sequences in the untranslated leader. Cell. 1985 Oct;42(3):903–911. doi: 10.1016/0092-8674(85)90286-7. [DOI] [PubMed] [Google Scholar]
  18. Mueller P. P., Harashima S., Hinnebusch A. G. A segment of GCN4 mRNA containing the upstream AUG codons confers translational control upon a heterologous yeast transcript. Proc Natl Acad Sci U S A. 1987 May;84(9):2863–2867. doi: 10.1073/pnas.84.9.2863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mueller P. P., Hinnebusch A. G. Multiple upstream AUG codons mediate translational control of GCN4. Cell. 1986 Apr 25;45(2):201–207. doi: 10.1016/0092-8674(86)90384-3. [DOI] [PubMed] [Google Scholar]
  20. Müller P. P., Reif M. K., Zonghou S., Sengstag C., Mason T. L., Fox T. D. A nuclear mutation that post-transcriptionally blocks accumulation of a yeast mitochondrial gene product can be suppressed by a mitochondrial gene rearrangement. J Mol Biol. 1984 Jun 5;175(4):431–452. doi: 10.1016/0022-2836(84)90178-5. [DOI] [PubMed] [Google Scholar]
  21. Poutre C. G., Fox T. D. PET111, a Saccharomyces cerevisiae nuclear gene required for translation of the mitochondrial mRNA encoding cytochrome c oxidase subunit II. Genetics. 1987 Apr;115(4):637–647. doi: 10.1093/genetics/115.4.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rogers D., Bussey H. Fidelity of conjugation in Saccharomyces cerevisiae. Mol Gen Genet. 1978 Jun 14;162(2):173–182. doi: 10.1007/BF00267874. [DOI] [PubMed] [Google Scholar]
  23. Rödel G., Fox T. D. The yeast nuclear gene CBS1 is required for translation of mitochondrial mRNAs bearing the cob 5' untranslated leader. Mol Gen Genet. 1987 Jan;206(1):45–50. doi: 10.1007/BF00326534. [DOI] [PubMed] [Google Scholar]
  24. Rödel G., Körte A., Kaudewitz F. Mitochondrial suppression of a yeast nuclear mutation which affects the translation of the mitochondrial apocytochrome b transcript. Curr Genet. 1985;9(8):641–648. doi: 10.1007/BF00449816. [DOI] [PubMed] [Google Scholar]
  25. Rödel G. Two yeast nuclear genes, CBS1 and CBS2, are required for translation of mitochondrial transcripts bearing the 5'-untranslated COB leader. Curr Genet. 1986;11(1):41–45. doi: 10.1007/BF00389424. [DOI] [PubMed] [Google Scholar]
  26. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Scherer S., Davis R. W. Replacement of chromosome segments with altered DNA sequences constructed in vitro. Proc Natl Acad Sci U S A. 1979 Oct;76(10):4951–4955. doi: 10.1073/pnas.76.10.4951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sharp P. A., Berk A. J., Berget S. M. Transcription maps of adenovirus. Methods Enzymol. 1980;65(1):750–768. doi: 10.1016/s0076-6879(80)65071-x. [DOI] [PubMed] [Google Scholar]
  29. Sprague G. F., Jr, Jensen R., Herskowitz I. Control of yeast cell type by the mating type locus: positive regulation of the alpha-specific STE3 gene by the MAT alpha 1 product. Cell. 1983 Feb;32(2):409–415. doi: 10.1016/0092-8674(83)90460-9. [DOI] [PubMed] [Google Scholar]
  30. Strausberg R. L., Butow R. A. Expression of petite mitochondrial DNA in vivo: zygotic gene rescue. Proc Natl Acad Sci U S A. 1977 Jul;74(7):2715–2719. doi: 10.1073/pnas.74.7.2715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Strick C. A., Fox T. D. Saccharomyces cerevisiae positive regulatory gene PET111 encodes a mitochondrial protein that is translated from an mRNA with a long 5' leader. Mol Cell Biol. 1987 Aug;7(8):2728–2734. doi: 10.1128/mcb.7.8.2728. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Thalenfeld B. E., Hill J., Tzagoloff A. Assembly of the mitochondrial membrane system. Characterization of the oxi2 transcript and localization of its promoter in Saccharomyces cerevisiae D273-10B. J Biol Chem. 1983 Jan 10;258(1):610–615. [PubMed] [Google Scholar]
  33. Thalenfeld B. E., Tzagoloff A. Assembly of the mitochondrial membrane system. Sequence of the oxi 2 gene of yeast mitochondrial DNA. J Biol Chem. 1980 Jul 10;255(13):6173–6180. [PubMed] [Google Scholar]

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