Genetic Evidence for the Requirement of the Endocytic Pathway in the Uptake of Coenzyme Q6 in Saccharomyces Cerevisiae

Overview

Journal Biochim Biophys Acta

Specialties Biochemistry
Biophysics

Date 2009 Apr 7

PMID 19345667

Citations 14

Authors

Sergio Padilla-Lopez

Maria Jimenez-Hidalgo

Alejandro Martin-Montalvo

Catherine F Clarke

Placido Navas

Carlos Santos-Ocana

Affiliations

Soon will be listed here.

Abstract

Coenzyme Q is an isoprenylated benzoquinone lipid that functions in respiratory electron transport and as a lipid antioxidant. Dietary supplementation with Q is increasingly used as a therapeutic for treatment of mitochondrial and neurodegenerative diseases, yet little is known regarding the mechanism of its uptake. As opposed to other yeast backgrounds, EG103 strains are unable to import exogenous Q(6) to the mitochondria. Furthermore, the distribution of exogenous Q(6) among endomembranes suggests an impairment of the membrane traffic at the level of the endocytic pathway. This fact was confirmed after the detection of defects in the incorporation of FM4-64 marker and CPY delivery to the vacuole. A similar effect was demonstrated in double mutant strains in Q(6) synthesis and several steps of endocytic process; those cells are unable to uptake exogenous Q(6) to the mitochondria and restore the growth on non-fermentable carbon sources. Additional data about the positive effect of peptone presence for exogenous Q(6) uptake support the hypothesis that Q(6) is transported to mitochondria through an endocytic-based system.

Citing Articles

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References

Wiederkehr A, Meier K, Riezman H . Identification and characterization of Saccharomyces cerevisiae mutants defective in fluid-phase endocytosis. Yeast. 2001; 18(8):759-73. DOI: 10.1002/yea.726. View

Raymond C, Vater C, Stevens T . Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol Biol Cell. 1992; 3(12):1389-402. PMC: 275707. DOI: 10.1091/mbc.3.12.1389. View

Munn A, Stevenson B, Pichler H, Riezman H . Specific sterols required for the internalization step of endocytosis in yeast. Mol Biol Cell. 1999; 10(11):3943-57. PMC: 25690. DOI: 10.1091/mbc.10.11.3943. View

Sohal R, Kamzalov S, Sumien N, Ferguson M, Rebrin I, Heinrich K . Effect of coenzyme Q10 intake on endogenous coenzyme Q content, mitochondrial electron transport chain, antioxidative defenses, and life span of mice. Free Radic Biol Med. 2006; 40(3):480-7. PMC: 2834650. DOI: 10.1016/j.freeradbiomed.2005.08.037. View

Jonassen T, Clarke C . Isolation and functional expression of human COQ3, a gene encoding a methyltransferase required for ubiquinone biosynthesis. J Biol Chem. 2000; 275(17):12381-7. DOI: 10.1074/jbc.275.17.12381. View

Daum G, Lees N, Bard M, Dickson R . Biochemistry, cell biology and molecular biology of lipids of Saccharomyces cerevisiae. Yeast. 1999; 14(16):1471-510. DOI: 10.1002/(SICI)1097-0061(199812)14:16<1471::AID-YEA353>3.0.CO;2-Y. View

Santos-Ocana C, Do T, Padilla S, Navas P, Clarke C . Uptake of exogenous coenzyme Q and transport to mitochondria is required for bc1 complex stability in yeast coq mutants. J Biol Chem. 2002; 277(13):10973-81. DOI: 10.1074/jbc.M112222200. View

GLICK B, Pon L . Isolation of highly purified mitochondria from Saccharomyces cerevisiae. Methods Enzymol. 1995; 260:213-23. DOI: 10.1016/0076-6879(95)60139-2. View

Bagnat M, Keranen S, Shevchenko A, Simons K . Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc Natl Acad Sci U S A. 2000; 97(7):3254-9. PMC: 16225. DOI: 10.1073/pnas.97.7.3254. View

10.

Marbois B, Hsu A, Pillai R, Colicelli J, Clarke C . Cloning of a rat cDNA encoding dihydroxypolyprenylbenzoate methyltransferase by functional complementation of a Saccharomyces cerevisiae mutant deficient in ubiquinone biosynthesis. Gene. 1994; 138(1-2):213-7. DOI: 10.1016/0378-1119(94)90810-9. View

11.

Quiles J, Ochoa J, Huertas J, Mataix J . Coenzyme Q supplementation protects from age-related DNA double-strand breaks and increases lifespan in rats fed on a PUFA-rich diet. Exp Gerontol. 2004; 39(2):189-94. DOI: 10.1016/j.exger.2003.10.002. View

12.

Kagan V, Tyurina Y, Witt E . Role of coenzyme Q and superoxide in vitamin E cycling. Subcell Biochem. 1999; 30:491-507. DOI: 10.1007/978-1-4899-1789-8_20. View

13.

Wu W, Routt S, Bankaitis V, Voelker D . A new gene involved in the transport-dependent metabolism of phosphatidylserine, PSTB2/PDR17, shares sequence similarity with the gene encoding the phosphatidylinositol/phosphatidylcholine transfer protein, SEC14. J Biol Chem. 2000; 275(19):14446-56. DOI: 10.1074/jbc.275.19.14446. View

14.

Dallner G, SINDELAR P . Regulation of ubiquinone metabolism. Free Radic Biol Med. 2000; 29(3-4):285-94. DOI: 10.1016/s0891-5849(00)00307-5. View

15.

Takahashi M, Asaumi S, Honda S, Suzuki Y, Nakai D, Kuroyanagi H . Mouse coq7/clk-1 orthologue rescued slowed rhythmic behavior and extended life span of clk-1 longevity mutant in Caenorhabditis elegans. Biochem Biophys Res Commun. 2001; 286(3):534-40. DOI: 10.1006/bbrc.2001.5439. View

16.

Bonangelino C, Chavez E, Bonifacino J . Genomic screen for vacuolar protein sorting genes in Saccharomyces cerevisiae. Mol Biol Cell. 2002; 13(7):2486-501. PMC: 117329. DOI: 10.1091/mbc.02-01-0005. View

17.

Fernandez-Ayala D, Brea-Calvo G, Lopez-Lluch G, Navas P . Coenzyme Q distribution in HL-60 human cells depends on the endomembrane system. Biochim Biophys Acta. 2005; 1713(2):129-37. DOI: 10.1016/j.bbamem.2005.05.010. View

18.

Yamamoto Y, Komuro E, Niki E . Antioxidant activity of ubiquinol in solution and phosphatidylcholine liposome. J Nutr Sci Vitaminol (Tokyo). 1990; 36(5):505-11. DOI: 10.3177/jnsv.36.505. View

19.

Fujiki Y, Hubbard A, Fowler S, Lazarow P . Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J Cell Biol. 1982; 93(1):97-102. PMC: 2112113. DOI: 10.1083/jcb.93.1.97. View

20.

van Meer G . Lipids of the Golgi membrane. Trends Cell Biol. 1998; 8(1):29-33. DOI: 10.1016/s0962-8924(97)01196-3. View