32
Views
29
CrossRef citations to date
0
Altmetric
Article

Translational Regulation of Nuclear Gene COX4 Expression by Mitochondrial Content of Phosphatidylglycerol and Cardiolipin in Saccharomyces cerevisiae

&
Pages 743-753 | Received 09 Jun 2005, Accepted 01 Nov 2005, Published online: 27 Mar 2023

REFERENCES

  • Ades, I. Z., and R. A. Butow. 1980. The products of mitochondria-bound cytoplasmic polysomes in yeast. J. Biol. Chem. 255:9918–9924.
  • Ardail, D., F. Lerme, and P. Louisot. 1992. Phospholipid import into mitochondria: possible regulation mediated through lipid polymorphism. Biochem. Biophys. Res. Commun. 186:1384–1390.
  • Barath, Z., and H. Kuntzel. 1972. Cooperation of mitochondrial and nuclear genes specifying the mitochondrial genetic apparatus in Neurospora crassa. Proc. Natl. Acad. Sci. USA 69:1371–1374.
  • Battelli, D., M. Bellei, E. Arrigoni-Martelli, U. Muscatello, and V. Bobyleva. 1992. Interaction of carnitine with mitochondrial cardiolipin. Biochim. Biophys. Acta 1117:33–36.
  • Biswas, G., O. A. Adebanjo, B. D. Freedman, H. K. Anandatheerthavarada, C. Vijayasarathy, M. Zaidi, M. Kotlikoff, and N. G. Avadhani. 1999. Retrograde Ca2+ signaling in C2C12 skeletal myocytes in response to mitochondrial genetic and metabolic stress: a novel mode of inter-organelle crosstalk. EMBO J. 18:522–533.
  • Bonnefoy, N., N. Bsat, and T. D. Fox. 2001. Mitochondrial translation of Saccharomyces cerevisiae COX2 mRNA is controlled by the nucleotide sequence specifying the pre-Cox2p leader peptide. Mol. Cell. Biol. 21:2359–2372.
  • Chang, S. C., P. N. Heacock, C. J. Clancey, and W. Dowhan. 1998. The PEL1 gene (renamed PGS1) encodes the phosphatidylglycero-phosphate synthase of Saccharomyces cerevisiae. J. Biol. Chem. 273:9829–9836.
  • Chang, S. C., P. N. Heacock, E. Mileykovskaya, D. R. Voelker, and W. Dowhan. 1998. Isolation and characterization of the gene (CLS1) encoding cardiolipin synthase in Saccharomyces cerevisiae. J. Biol. Chem. 273:14933–14941.
  • Dagsgaard, C., L. E. Taylor, K. M. O'Brien, and R. O. Poyton. 2001. Effects of anoxia and the mitochondrion on expression of aerobic nuclear COX genes in yeast. Evidence for a signaling pathway from the mitochondrial genome to the nucleus. J. Biol. Chem. 276:7593–7601.
  • de Kroon, A. I., D. Dolis, A. Mayer, R. Lill, and B. de Kruijff. 1997. Phospholipid composition of highly purified mitochondrial outer membranes of rat liver and Neurospora crassa. Is cardiolipin present in the mitochondrial outer membrane? Biochim. Biophys. Acta 1325:108–116.
  • Dowhan, W., C. R. Bibus, and G. Schatz. 1985. The cytoplasmically-made subunit IV is necessary for assembly of cytochrome c oxidase in yeast. EMBO J. 4:179–184.
  • Eble, K. S., W. B. Coleman, R. R. Hantgan, and C. C. Cunningham. 1990. Tightly associated cardiolipin in the bovine heart mitochondrial ATP synthase as analyzed by 31P nuclear magnetic resonance spectroscopy. J. Biol. Chem. 265:19434–19440.
  • Eilers, M., T. Endo, and G. Schatz. 1989. Adriamycin, a drug interacting with acidic phospholipids, blocks import of precursor proteins by isolated yeast mitochondria. J. Biol. Chem. 264:2945–2950.
  • Epstein, C. B., J. A. Waddle, W. ten Hale, V. Dave, J. Thornton, T. L. Macatee, H. R. Garner, and R. A. Butow. 2001. Genome-wide responses to mitochondrial dysfunction. Mol. Biol. Cell 12:297–308.
  • Forsburg, S. L., and L. Guarente. 1989. Communication between mitochondria and the nucleus in regulation of cytochrome genes in the yeast Saccharomyces cerevisiae. Annu. Rev. Cell Biol. 5:153–180.
  • Fry, M., and D. E. Green. 1981. Cardiolipin requirement for electron transfer in complex I and III of the mitochondrial respiratory chain. J. Biol. Chem. 256:1874–1880.
  • Fujiki, M., and K. Verner. 1993. Coupling of cytosolic protein synthesis and mitochondrial protein import in yeast. Evidence for cotranslational import in vivo. J. Biol. Chem. 268:1914–1920.
  • Fujiki, M., and K. Verner. 1991. Coupling of protein synthesis and mitochondrial import in a homologous yeast in vitro system. J. Biol. Chem. 266:6841–6847.
  • Geier, B. M., H. Schagger, C. Ortwein, T. A. Link, W. R. Hagen, U. Brandt, and G. Von Jagow. 1995. Kinetic properties and ligand binding of the eleven-subunit cytochrome-c oxidase from Saccharomyces cerevisiae isolated with a novel large-scale purification method. Eur. J. Biochem. 227:296–302.
  • Glick, B. S., and L. A. Pon. 1995. Isolation of highly purified mitochondria from Saccharomyces cerevisiae. Methods Enzymol. 260:213–223.
  • Gray, N. K., and M. W. Hentze. 1994. Regulation of protein synthesis by mRNA structure. Mol. Biol. Rep. 19:195–200.
  • Gunyuzlu, P. L., G. F. Hollis, and J. H. Toyn. 2001. Plasmid construction by linker-assisted homologous recombination in yeast. BioTechniques 31:1246, 1248, 1250.
  • Harding, H. P., Y. Zhang, A. Bertolotti, H. Zeng, and D. Ron. 2000. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5:897–904.
  • Herskowitz, I., and R. E. Jensen. 1991. Putting the HO gene to work: practical uses for mating-type switching. Methods Enzymol. 194:132–146.
  • Hoch, F. L. 1992. Cardiolipin and biomembrane function. Biochim. Biophys. Acta 1113:71–133.
  • Hoffmann, B., A. Stockl, M. Schlame, K. Beyer, and M. Klingenberg. 1994. The reconstituted ADP/ATP carrier activity has an absolute requirement for cardiolipin as shown in cysteine mutants. J. Biol. Chem. 269:1940–1944.
  • Hovius, R., H. Lambrechts, K. Nicolay, and B. de Kruijff. 1990. Improved methods to isolate and subfractionate rat liver mitochondria. Lipid composition of the inner and outer membrane. Biochim. Biophys. Acta 1021:217–226.
  • Iwawaki, T., A. Hosoda, T. Okuda, Y. Kamigori, C. Nomura-Furuwatari, Y. Kimata, A. Tsuru, and K. Kohno. 2001. Translational control by the ER transmembrane kinase/ribonuclease IRE1 under ER stress. Nat. Cell Biol. 3:158–164.
  • Jauniaux, J. C., L. A. Urrestarazu, and J. M. Wiame. 1978. Arginine metabolism in Saccharomyces cerevisiae: subcellular localization of the enzymes. J. Bacteriol. 133:1096–1107.
  • Jiang, F., H. S. Rizavi, and M. L. Greenberg. 1997. Cardiolipin is not essential for the growth of Saccharomyces cerevisiae on fermentable or non-fermentable carbon sources. Mol. Microbiol. 26:481–491.
  • Jiang, F., M. T. Ryan, M. Schlame, M. Zhao, Z. Gu, M. Klingenberg, N. Pfanner, and M. L. Greenberg. 2000. Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function. J. Biol. Chem. 275:22387–22394.
  • Kadenbach, B., P. Mende, H. V. Kolbe, I. Stipani, and F. Palmieri. 1982. The mitochondrial phosphate carrier has an essential requirement for cardiolipin. FEBS Lett. 139:109–112.
  • Kawasaki, K., O. Kuge, S. C. Chang, P. N. Heacock, M. Rho, K. Suzuki, M. Nishijima, and W. Dowhan. 1999. Isolation of a Chinese hamster ovary (CHO) cDNA encoding phosphatidylglycerophosphate (PGP) synthase, expression of which corrects the mitochondrial abnormalities of a PGP synthase-defective mutant of CHO-K1 cells. J. Biol. Chem. 274:1828–1834.
  • Kirchman, P. A., S. Kim, C. Y. Lai, and S. M. Jazwinski. 1999. Interorganelle signaling is a determinant of longevity in Saccharomyces cerevisiae. Genetics 152:179–190.
  • Koshkin, V., and M. L. Greenberg. 2000. Oxidative phosphorylation in cardiolipin-lacking yeast mitochondria. Biochem. J. 347:687–691.
  • Kozak, M. 1989. Circumstances and mechanisms of inhibition of translation by secondary structure in eucaryotic mRNAs. Mol. Cell. Biol. 9:5134–5142.
  • Kozak, M. 1990. Downstream secondary structure facilitates recognition of initiator codons by eukaryotic ribosomes. Proc. Natl. Acad. Sci. USA 87:8301–8305.
  • Kozak, M. 1986. Influences of mRNA secondary structure on initiation by eukaryotic ribosomes. Proc. Natl. Acad. Sci. USA 83:2850–2854.
  • Law, G. L., A. Raney, C. Heusner, and D. R. Morris. 2001. Polyamine regulation of ribosome pausing at the upstream open reading frame of S-adenosylmethionine decarboxylase. J. Biol. Chem. 276:38036–38043.
  • Lemaire, C., S. Robineau, and P. Netter. 1998. Molecular and biochemical analysis of Saccharomyces cerevisiae cox1 mutants. Curr. Genet. 34:138–145.
  • Lesnefsky, E. J., S. Moghaddas, B. Tandler, J. Kerner, and C. L. Hoppel. 2001. Mitochondrial dysfunction in cardiac disease: ischemia—reperfusion, aging, and heart failure. J. Mol. Cell Cardiol. 33:1065–1089.
  • Lincoln, A. J., Y. Monczak, S. C. Williams, and P. F. Johnson. 1998. Inhibition of CCAAT/enhancer-binding protein alpha and beta translation by upstream open reading frames. J. Biol. Chem. 273:9552–9560.
  • Liu, C. Y., M. Schroder, and R. J. Kaufman. 2000. Ligand-independent dimerization activates the stress response kinases IRE1 and PERK in the lumen of the endoplasmic reticulum. J. Biol. Chem. 275:24881–24885.
  • Mangus, D. A., N. Amrani, and A. Jacobson. 1998. Pbp1p, a factor interacting with Saccharomyces cerevisiae poly(A)-binding protein, regulates polyadenylation. Mol. Cell Biol. 18:7383–7396.
  • Marc, P., A. Margeot, F. Devaux, C. Blugeon, M. Corral-Debrinski, and C. Jacq. 2002. Genome-wide analysis of mRNAs targeted to yeast mitochondria. EMBO Rep. 3:159–164.
  • McMillin, J. B., and W. Dowhan. 2002. Cardiolipin and apoptosis. Biochim. Biophys. Acta 1585:97–107.
  • Mende, P., F. J. Huther, and B. Kadenbach. 1983. Specific and reversible activation and inactivation of the mitochondrial phosphate carrier by cardiolipin and nonionic detergents, respectively. FEBS Lett. 158:331–334.
  • Ostrander, D. B., M. Zhang, E. Mileykovskaya, M. Rho, and W. Dowhan. 2001. 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. 276:25262–25272.
  • Pantopoulos, K. 2004. Iron metabolism and the IRE/IRP regulatory system: an update. Ann. N. Y. Acad. Sci. 1012:1–13.
  • Paradies, G., F. M. Ruggiero, G. Petrosillo, and E. Quagliariello. 1998. Peroxidative damage to cardiac mitochondria: cytochrome oxidase and cardiolipin alterations. FEBS Lett. 424:155–158.
  • Parikh, V. S., M. M. Morgan, R. Scott, L. S. Clements, and R. A. Butow. 1987. The mitochondrial genotype can influence nuclear gene expression in yeast. Science 235:576–580.
  • Pfeiffer, K., V. Gohil, R. A. Stuart, C. Hunte, U. Brandt, M. L. Greenberg, and H. Schagger. 2003. Cardiolipin stabilizes respiratory chain supercomplexes. J. Biol. Chem. 278:52873–52880.
  • Poyton, R. O. 1980. Cooperative interaction between mitochondrial and nuclear genomes: cytochrome c oxidase assembly as a model. Curr. Top. Cell Regul. 17:231–295.
  • Poyton, R. O., and C. J. Dagsgaard. 2000. Mitochondrial-nuclear crosstalk is involved in oxygen-regulated gene expression in yeast. Adv. Exp. Med. Biol. 475:177–184.
  • Robinson, N. C. 1993. Functional binding of cardiolipin to cytochrome c oxidase. J. Bioenerg. Biomembr. 25:153–163.
  • Schneider, J. C., and L. Guarente. 1987. The untranslated leader of nuclear COX4 gene of Saccharomyces cerevisiae contains an intron. Nucleic Acids Res. 15:3515–3529.
  • Sedlak, E., and N. C. Robinson. 1999. Phospholipase A2 digestion of cardiolipin bound to bovine cytochrome c oxidase alters both activity and quaternary structure. Biochemistry 38:14966–14972.
  • Shen, H., and W. Dowhan. 1998. Regulation of phosphatidylglycerophosphate synthase levels in Saccharomyces cerevisiae. J. Biol. Chem. 273:11638–11642.
  • Shen, H., and W. Dowhan. 1997. Regulation of phospholipid biosynthetic enzymes by the level of CDP-diacylglycerol synthase activity. J. Biol. Chem. 272:11215–11220.
  • Shigenaga, M. K., T. M. Hagen, and B. N. Ames. 1994. Oxidative damage and mitochondrial decay in aging. Proc. Natl. Acad. Sci. USA 91:10771–10778.
  • Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19–27.
  • Steele, D. F., C. A. Butler, and T. D. Fox. 1996. Expression of a recoded nuclear gene inserted into yeast mitochondrial DNA is limited by mRNA-specific translational activation. Proc. Natl. Acad. Sci. USA 93:5253–5257.
  • Thomson, A. M., J. T. Rogers, and P. J. Leedman. 1999. Iron-regulatory proteins, iron-responsive elements and ferritin mRNA translation. Int. J. Biochem. Cell Biol. 31:1139–1152.
  • Tuller, G., C. Hrastnik, G. Achleitner, U. Schiefthaler, F. Klein, and G. Daum. 1998. YDL142c encodes cardiolipin synthase (Cls1p) and is non-essential for aerobic growth of Saccharomyces cerevisiae. FEBS Lett. 421:15–18.
  • Vaena de Avalos, S., Y. Okamoto, and Y. A. Hannun. 2004. Activation and localization of inositol phosphosphingolipid phospholipase C, Isc1p, to the mitochondria during growth of Saccharomyces cerevisiae. J. Biol. Chem. 279:11537–11545.
  • Van Loon, A. P., E. Van Eijk, and L. A. Grivell. 1983. Biosynthesis of the ubiquinol-cytochrome c reductase complex in yeast. Discoordinate synthesis of the 11-kd subunit in response to increased gene copy number. EMBO J. 2:1765–1770.
  • Vreken, P., F. Valianpour, L. G. Nijtmans, L. A. Grivell, B. Plecko, R. J. Wanders, and P. G. Barth. 2000. Defective remodeling of cardiolipin and phosphatidylglycerol in Barth syndrome. Biochem. Biophys. Res. Commun. 279:378–382.
  • Westermann, B., and W. Neupert. 2000. Mitochondria-targeted green fluorescent proteins: convenient tools for the study of organelle biogenesis in Saccharomyces cerevisiae. Yeast 16:1421–1427.
  • Wilkie, G. S., K. S. Dickson, and N. K. Gray. 2003. Regulation of mRNA translation by 5′- and 3′-UTR-binding factors. Trends Biochem. Sci. 28:182–188.
  • Yoon, H., S. P. Miller, E. K. Pabich, and T. F. Donahue. 1992. SSL1, a suppressor of a HIS4 5′-UTR stem-loop mutation, is essential for translation initiation and affects UV resistance in yeast. Genes Dev. 6:2463–2477.
  • Zhang, K., and R. J. Kaufman. 2004. Signaling the unfolded protein response from the endoplasmic reticulum. J. Biol. Chem. 279:25935–25938.
  • Zhang, M., E. Mileykovskaya, and W. Dowhan. 2002. Gluing the respiratory chain together. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane. J. Biol. Chem. 277:43553–43556.
  • Zhang, M., X. Su, E. Mileykovskaya, A. A. Amoscato, and W. Dowhan. 2003. Cardiolipin is not required to maintain mitochondrial DNA stability or cell viability for Saccharomyces cerevisiae grown at elevated temperatures. J. Biol. Chem. 278:35204–35210.
  • Zhong, Q., J. Gvozdenovic-Jeremic, P. Webster, J. Zhou, and M. L. Greenberg. 2005. Loss of function of KRE5 suppresses temperature sensitivity of mutants lacking mitochondrial anionic lipids. Mol. Biol. Cell 16:665–675.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.