The subcellular localization of yeast glycogen synthase is dependent upon glycogen content

Canadian Journal of Microbiology

Volumn 56, Issue 5, 2010, Pages 408-420

  Wilson, Wayne A ^a   Boyer, Michael P ^a   Davis, Keri D ^a   Burke, Michael ^a   Roach, Peter J ^b  

^a Des Moines University College of Osteopathic Medicine   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Glycogen synthase; Localization; Nucleus; Saccharomyces cerevisiae

Indexed keywords

GLYCOGEN SYNTHASE; GREEN FLUORESCENT PROTEIN; LOCALIZATION PATTERNS; NUTRIENT LIMITATIONS; SACCHAROMYCES CEREVISIAE; SUBCELLULAR DISTRIBUTION; SUBCELLULAR LOCALIZATIONS;

CELLS; CYTOLOGY;

YEAST;

GLYCOGEN; GLYCOGEN SYNTHASE; GREEN FLUORESCENT PROTEIN; GLYCOGEN PHOSPHORYLASE;

BIOACCUMULATION; CATALYSIS; CYTOPLASM; ENZYME ACTIVITY; GENE EXPRESSION; NUTRIENT LIMITATION; POLYSACCHARIDE; PROTEIN; TRANSLOCATION; YEAST;

ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CYTOPLASM; ENZYME LOCALIZATION; GENE; GLYCOGEN ANALYSIS; GSY2P GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; YEAST; ENZYMOLOGY; IMMUNOBLOTTING; METABOLISM; MICROSCOPY;

CELL NUCLEUS; CYTOPLASM; GLYCOGEN; GLYCOGEN PHOSPHORYLASE; GLYCOGEN SYNTHASE; IMMUNOBLOTTING; MICROSCOPY; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 77953389369     PISSN: 00084166     EISSN: None     Source Type: Journal    
DOI: 10.1139/W10-027     Document Type: Article

References (56)

1. Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72(1-2): 248-254. doi:10.1016/0003-2697(76)90527-3. PMID:942051.
2. Cahill, G., Walsh, P.K., and Donnelly, D. 2000. Determination of yeast glycogen content by individual cell spectroscopy using image analysis. Biotechnol. Bioeng. 69(3): 312-322. doi:10.1002/1097-0290(20000805)69: 3〈312::AID-BIT9〉3.0.CO;2-Y. PMID: 10861411.
3. Cheng, C., Mu, J., Farkas, I., Huang, D., Goebl, M.G., and Roach, P.J. 1995. Requirement of the self-glucosylating initiator proteins Glg1p and Glg2p for glycogen accumulation in Saccharomyces cerevisiae. Mol. Cell. Biol. 15(12): 6632-6640. PMID: 8524228.
4. Chester, V.E. 1968. Heritable glycogen-storage deficiency in yeast and its induction by ultra-violet light. J. Gen. Microbiol. 51(1): 49-56. PMID:5653230.
5. Cid, E., Cifuentes, D., Baqué, S., Ferrer, J.C., and Guinovart, J.J. 2005. Determinants of the nucleocytoplasmic shuttling of muscle glycogen synthase. FEBS J. 272(12): 3197-3213. doi:10.1111/j.1742-4658.2005.04738.x. PMID:15955076.
6. Farkas, I., Hardy, T.A., Goebl, M.G., and Roach, P.J. 1991. Two glycogen synthase isoforms in Saccharomyces cerevisiae are coded by distinct genes that are differentially controlled. J. Biol. Chem. 266(24): 15602-15607. PMID:1908457.
7. Feng, Z.H., Wilson, S.E., Peng, Z.Y., Schlender, K.K., Reimann, E.M., and Trumbly, R.J. 1991. The yeast GLC7 gene required for glycogen accumulation encodes a type 1 protein phosphatase. J. Biol. Chem. 266(35): 23796-23801. PMID:1660885.
8. Fernández-Novell, J.M., Ariño, J., Vilaró, S., and Guinovart, J.J. 1992a. Glucose induces the translocation and the aggregation of glycogen synthase in rat hepatocytes. Biochem. J. 281(2): 443-448. PMID:1736893.
9. Fernández-Novell, J.M., Ariño, J., Vilaró, S., Bellido, D., and Guinovart, J.J. 1992b. Role of glucose 6-phosphate in the translocation of glycogen synthase in rat hepatocytes. Biochem. J. 288(2): 497-501. PMID:1334407.
10. Fernández-Novell, J.M., Roca, A., Bellido, D., Vilaró, S., and Guinovart, J.J. 1996. Translocation and aggregation of hepatic glycogen synthase during the fasted-to-refed transition in rats. Eur. J. Biochem. 238(2): 570-575. doi:10.1111/j.1432-1033.1996.0570z.x. PMID:8681973.
11. Fernández-Novell, J.M., Bellido, D., Vilaró, S., and Guinovart, J.J. 1997. Glucose induces the translocation of glycogen synthase to the cell cortex in rat hepatocytes. Biochem. J. 321(1): 227-231. PMID:9003423. (Pubitemid 27032591)
12. Ferrer, J.C., Baqué, S., and Guinovart, J.J. 1997. Muscle glycogen synthase translocates from the cell nucleus to the cystosol in response to glucose. FEBS Lett. 415(3): 249-252. doi:10.1016/S0014-5793(97)01136-8. PMID:9357976.
13. François, J., and Hers, H.G. 1988. The control of glycogen metabolism in yeast. 2. A kinetic study of the two forms of glycogen synthase and of glycogen phosphorylase and an investigation of their interconversion in a cell-free extract. Eur. J. Biochem. 174(3): 561-567. doi:10.1111/j.1432-1033. 1988.tb14135.x. PMID: 2839335.
14. François, J., and Parrou, J.L. 2001. Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol. Rev. 25(1): 125-145. doi:10.1016/S0168-6445(00)00059-0. PMID:11152943.
15. François, J., Villanueva, M.E., and Hers, H.G. 1988. The control of glycogen metabolism in yeast. 1. Interconversion in vivo of glycogen synthase and glycogen phosphorylase induced by glucose, a nitrogen source or uncouplers. Eur. J. Biochem. 174(3): 551-559. doi:10.1111/j.1432-1033.1988.tb14134.x. PMID:2839334.
16. François, J.M., Thompson-Jaeger, S., Skroch, J., Zellenka, U., Spevak, W., and Tatchell, K. 1992. GAC1 may encode a regulatory subunit for protein phosphatase type 1 in Saccharomyces cerevisiae. EMBO J. 11(1): 87-96. PMID:1310938.
17. Fries, T., Betz, C., Sohn, K., Caesar, S., Schlenstedt, G., and Bailer, S.M. 2007. A novel conserved nuclear localization signal is recognized by a group of yeast importins. J. Biol. Chem. 282(27): 19292-19301. doi:10.1074/jbc.M700217200. PMID:17485461.
18. Gilboe, D.P., Larson, K.L., and Nuttall, F.Q. 1972. Radioactive method for the assay of glycogen phosphorylases. Anal. Biochem. 47(1): 20-27. doi:10.1016/0003-2697(72)90274-6. PMID: 5031114.
19. Guthrie, C., and Fink, G.R. 1991. Guide to yeast genetics and molecular biology. Methods Enzymol. 194.
20. Hanashiro, I., and Roach, P.J. 2002. Mutations of muscle glycogen synthase that disable activation by glucose 6-phosphate. Arch. Biochem. Biophys. 397(2): 286-292. doi:10.1006/abbi.2001.2623. PMID:11795884.
21. Hardy, T.A., and Roach, P.J. 1993. Control of yeast glycogen synthase-2 by COOH-terminal phosphorylation. J. Biol. Chem. 268(32): 23799-23805. PMID:8226915.
22. Hardy, T.A., Huang, D., and Roach, P.J. 1994. Interactions between cAMP-dependent and SNF1 protein kinases in the control of glycogen accumulation in Saccharomyces cerevisiae. J. Biol. Chem. 269(45): 27907-27913. PMID:7961723.
23. Ho, Y., Gruhler, A., Heilbut, A., Bader, G.D., Moore, L., Adams, S.L., et al. 2002. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature (Lond.), 415(6868): 180-183. doi:10.1038/415180a. PMID:11805837.
24. Huang, D., Farkas, I., and Roach, P.J. 1996a. Pho85p, a cyclin-dependent protein kinase, and the Snf1p protein kinase act antagonistically to control glycogen accumulation in Saccharomyces cerevisiae. Mol. Cell. Biol. 16(8): 4357-4365. PMID: 8754836.
25. Huang, D., Chun, K.T., Goebl, M.G., and Roach, P.J. 1996b. Genetic interactions between REG1/HEX2 and GLC7, the gene encoding the protein phosphatase type 1 catalytic subunit in Saccharomyces cerevisiae. Genetics, 143(1): 119-127. PMID: 8722767.
26. Huang, D., Wilson, W.A., and Roach, P.J. 1997. Glucose-6-P control of glycogen synthase phosphorylation in yeast. J. Biol. Chem. 272(36): 22495-22501. doi:10.1074/jbc.272.36.22495. PMID:9278401.
27. Huang, D., Moffat, J., Wilson, W.A., Moore, L., Cheng, C., Roach, P.J., and Andrews, B. 1998. Cyclin partners determine Pho85 protein kinase substrate specificity in vitro and in vivo: control of glycogen biosynthesis by Pcl8 and Pcl10. Mol. Cell. Biol. 18(6): 3289-3299. PMID:9584169.
28. Huh, W.K., Falvo, J.V., Gerke, L.C., Carroll, A.S., Howson, R.W., Weissman, J.S., and O'Shea, E.K. 2003. Global analysis of protein localization in budding yeast. Nature (Lond.), 425(6959): 686-691. doi:10.1038/nature02026. PMID:14562095.
29. Hwang, P.K., and Fletterick, R.J. 1986. Convergent and divergent evolution of regulatory sites in eukaryotic phosphorylases. Nature (Lond.), 324(6092): 80-84. doi:10.1038/324080a0. PMID: 3537803.
30. Ito, T., Chiba, T., Ozawa, R., Yoshida, M., Hattori, M., and Sakaki, Y. 2001. A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. U.S.A. 98(8): 4569-4574. doi:10.1073/pnas.061034498. PMID:11283351.
31. Krogan, N.J., Cagney, G., Yu, H., Zhong, G., Guo, X., Ignatchenko, A., et al. 2006. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature (Lond.), 440(7084): 637-643. doi:10.1038/nature04670. PMID:16554755.
32. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.), 227(5259): 680-685. doi:10.1038/227680a0. PMID:5432063.
33. Meyer, F., Heilmeyer, L.M., Jr., Haschke, R.H., and Fischer, E.H. 1970. Control of phosphorylase activity in a muscle glycogen particle. I. Isolation and characterization of the protein-glycogen complex. J. Biol. Chem. 245(24): 6642-6648. PMID:4320610.
34. Ni, H.T., and LaPorte, D.C. 1995. Response of a yeast glycogen synthase gene to stress. Mol. Microbiol. 16(6): 1197-1205. doi:10.1111/j.1365-2958.1995. tb02342.x. PMID:8577253.
35. Ou, H., Yan, L., Osmanovic, S., Greenberg, C.C., and Brady, M.J. 2005. Spatial reorganization of glycogen synthase upon activation in 3T3-L1 adipocytes. Endocrinology, 146(1): 494-502. doi:10.1210/en.2004-1022. PMID:15486231.
36. Pederson, B.A., Cheng, C., Wilson, W.A., and Roach, P.J. 2000. Regulation of glycogen synthase. Identification of residues involved in regulation by the allosteric ligand glucose-6-P and by phosphorylation. J. Biol. Chem. 275(36): 27753-27761. PMID: 10874034.
37. Pederson, B.A., Wilson, W.A., and Roach, P.J. 2004. Glycogen synthase sensitivity to glucose-6-P is important for controlling glycogen accumulation in Saccharomyces cerevisiae. J. Biol. Chem. 279(14): 13764-13768. doi:10.1074/jbc.M312335200. PMID:14742447.
38. Prats, C., Cadefau, J.A., Cussó, R., Qvortrup, K., Nielsen, J.N., Wojtaszewski, J.F., et al. 2005. Phosphorylation-dependent translocation of glycogen synthase to a novel structure during glycogen resynthesis. J. Biol. Chem. 280(24): 23165-23172. doi:10.1074/jbc.M502713200. PMID:15840572.
39. Roach, P.J., Skurat, A.V., and Harris, R.A. 2001. Regulation of glycogen metabolism. In Handbook of physiology. Vol. II. Edited by L.S. Jefferson and A.D. Cherrington. Lippincott Company, Philadelphia, Penn. pp. 609-647.
40. Rothman-Denes, L.B., and Cabib, E. 1970. Two forms of yeast glycogen synthetase and their role in glycogen accumulation. Proc. Natl. Acad. Sci. U.S.A. 66(3): 967-974. doi:10.1073/pnas.66.3.967. PMID:4987630.
41. Rothman-Denes, L.B., and Cabib, E. 1971. Glucose 6-phosphate dependent and independent forms of yeast glycogen synthetase. Their properties and interconversions. Biochemistry, 10(7): 1236-1242. doi:10.1021/bi00783a021. PMID:5553327.
42. Rowen, D.W., Meinke, M., and LaPorte, D.C. 1992. GLC3 and GHA1 of Saccharomyces cerevisiae are allelic and encode the glycogen branching enzyme. Mol. Cell. Biol. 12(1): 22-29. PMID:1729600.
43. Sambrook, J., Fritsch, E.F., and Maniatis, T. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
44. Sheff, M.A., and Thorn, K.S. 2004. Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast, 21(8): 661-670. doi:10.1002/yea.1130. PMID:15197731.
45. Sikorski, R.S., and Hieter, P. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics, 122(1): 19-27. PMID: 2659436.
46. Sirover, M.A. 2005. New nuclear functions of the glycolytic protein, glyceraldehyde-3-phosphate dehydrogenase, in mammalian cells. J. Cell. Biochem. 95(1): 45-52. doi:10.1002/jcb.20399. PMID:15770658.
47. Smith, A., Ward, M.P., and Garrett, S. 1998. Yeast PKA represses Msn2p/Msn4p-dependent gene expression to regulate growth, stress response and glycogen accumulation. EMBO J. 17(13): 3556-3564. doi:10.1093/emboj/17.13.3556. PMID:9649426.
48. Stuart, J.S., Frederick, D.L., Varner, C.M., and Tatchell, K. 1994. The mutant type 1 protein phosphatase encoded by glc7-1 from Saccharomyces cerevisiae fails to interact productively with the GAC1-encoded regulatory subunit. Mol. Cell. Biol. 14(2): 896-905. PMID:8289829.
49. Teste, M.A., Enjalbert, B., Parrou, J.L., and François, J.M. 2000. The Saccharomyces cerevisiae YPR184w gene encodes the glycogen debranching enzyme. FEMS Microbiol. Lett. 193(1): 105-110. doi:10.1111/j.1574-6968.2000. tb09410.x. PMID:11094287.
50. Thomas, J.A., Schlender, K.K., and Larner, J. 1968. A rapid filter paper assay for UDPglucose-glycogen glucosyltransferase, including an improved biosynthesis of UDP-14C-glucose. Anal. Biochem. 25(1): 486-499. doi:10.1016/0003-2697(68)90127-9. PMID:5704765.
51. Timblin, B.K., Tatchell, K., and Bergman, L.W. 1996. Deletion of the gene encoding the cyclin-dependent protein kinase Pho85 alters glycogen metabolism in Saccharomyces cerevisiae. Genetics, 143(1): 57-66. PMID:8722762.
52. Torija, M.J., Novo, M., Lemassu, A., Wilson, W., Roach, P.J., François, J., and Parrou, J.L. 2005. Glycogen synthesis in the absence of glycogenin in the yeast Saccharomyces cerevisiae. FEBS Lett. 579(18): 3999-4004. doi:10.1016/j.febslet.2005.06.007. PMID:16004992.
53. Tu, J.L., and Carlson, M. 1995. REG1 binds to protein phosphatase type 1 and regulates glucose repression in Saccharomyces cerevisiae. EMBO J. 14(23): 5939-5946. PMID:8846786.
54. Wang, Z., Wilson, W.A., Fujino, M.A., and Roach, P.J. 2001. Antagonistic controls of autophagy and glycogen accumulation by Snf1p, the yeast homolog of AMP-activated protein kinase, and the cyclin-dependent kinase Pho85p. Mol. Cell. Biol. 21(17): 5742-5752. doi:10.1128/MCB.21.17.5742-5752.2001. PMID:11486014.
55. Wilson, W.A., Mahrenholz, A.M., and Roach, P.J. 1999. Substrate targeting of the yeast cyclin-dependent kinase Pho85p by the cyclin Pcl10p. Mol. Cell. Biol. 19(10): 7020-7030. PMID: 10490639.
56. Yamashita, I., and Fukui, S. 1985. Transcriptional control of the sporulation-specific glucoamylase gene in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 5(11): 3069-3073. PMID: 3939312.