Catabolite degradation of fructose-1,6-bisphosphatase in the yeast Saccharomyces cerevisiae: A genome-wide screen identifies eight novel GID genes and indicates the existence of two degradation pathways

Molecular Biology of the Cell

Volumn 14, Issue 4, 2003, Pages 1652-1663

  Regelmann, Jochen ^a   Schiile, Thomas ^a   Josupeit, Frank S ^a   Horak, Jaroslav ^b   Rose, Matthias ^c   Entian, Karl Dieter ^c   Thumm, Michael ^a   Wolf, Dieter H ^a  

^a UNIVERSITY OF STUTTGART   (Germany)

^b INSTITUTE OF PHYSIOLOGY   (Czech Republic)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FRUCTOSE BISPHOSPHATASE; GENE PRODUCT; PROTEIN GID; PROTEIN GID1; PROTEIN GID2; PROTEIN GID2P; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; CATABOLISM; COMPLEX FORMATION; FRUCTOSE METABOLISM; FUNGAL GENE; FUNGAL GENETICS; GENE FUNCTION; GENE IDENTIFICATION; GENETIC SCREENING; GENOMICS; GID GENE; GLUCONEOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE; YEAST;

BASE SEQUENCE; CYSTEINE ENDOPEPTIDASES; DNA, FUNGAL; ENDOPEPTIDASES; FRUCTOSE-BISPHOSPHATASE; GENES, FUNGAL; GENOME, FUNGAL; GLUCOSE; MACROMOLECULAR SUBSTANCES; MEMBRANE TRANSPORT PROTEINS; MONOSACCHARIDE TRANSPORT PROTEINS; MULTIENZYME COMPLEXES; PROTEASOME ENDOPEPTIDASE COMPLEX; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN; VACUOLES;

FUNGI; MYXOGASTRIA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0038709277     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-08-0456     Document Type: Article

References (43)

1. Abeijon, C., Orlean, P., Robbins, P.W., and Hirschberg, C.B. (1989). Topography of glycosylation in yeast: characterization of GDPmannose transport and lumenal guanosine diphosphatase activities in Golgi-like vesicles. Proc. Natl. Acad. Sci. USA 86, 6935-6939.
2. Amerik, A., Swaminathan, S., Krantz, B.A., Wilkinson, K.D., and Hochstrasser, M. (1997). In vivo disassembly of free polyubiquitin chains by yeast Ubp14 modulates rates of protein degradation by the proteasome. EMBO J 16, 4826-4838.
3. Ausubel, F.M., Kingston, R.E., Seidman, F.G., Struhl, K., Moore, D.D., Brent, R., and Smith, F.A. (1992). Current Protocols in Molecular Biology, New York: John Wiley & Sons.
4. Bachmair, A., Finley, D., and Varshavsky, A. (1986). In vivo half-life of a protein is a function of its amino-terminal residue. Science 234, 179-86.
5. Barth, H., and Thumm, M. (2001). A genomic screen identifies AUT8 as a novel gene essential for autophagy in the yeast Saccharomyces cerevisiae. Gene 274, 151-156.
6. Baumeister, W., Walz, J., Zuhl, F., and Seemüller, E. (1998). The proteasome: paradigm of a self-compartmentalizing protease. Cell 92, 367-380.
7. Brown, C.R., McCann, J.A., and Chiang, H.L. (2000). The heat shock protein Ssa2p is required for import of fructose-1,6-bisphosphatase into Vid vesicles. J. Cell Biol. 150, 65-76.
8. Brown, C.R., Cui, D.Y., Hung, G.G., and Chiang, H.L. (2001). Cyclophilin A mediates Vid22p function in the import of fructose-1,6-bisphosphatase into Vid vesicles. J. Biol. Chem. 276, 48017-48026.
9. Brown, C.R., McCann, J.A., Hung, G.G., Elco, C.P., and Chiang, H.L. (2002). Vid22p, a novel plasma membrane protein, is required for the fructose-1,6-bisphosphatase degradation pathway. J. Cell Sci. 115, 655-666.
10. Chiang, H.L., and Schekman, R. (1991). Regulated import and degradation of a cytosolic protein in the yeast vacuole. Nature 350, 313-318.
11. Chiang, M.C., and Chiang, H.L. (1998). Vid24p, a novel protein localized to the fructose-1, 6-bisphosphatase-containing vesicles, regulates targeting of fructose-1,6-bisphosphatase from the vesicles to the vacuole for degradation. J. Cell Biol. 140, 1347-1356.
12. Cottarel, G. (1995). The Saccharomyces cerevisiae HIS3 and LYS2 genes complement the Schizosaccharomyces pombe his5-303 and lys1-131 mutations, respectively: new selectable markers and new multipurpose multicopy shuttle vectors, pSP3 and pSP4. Curr. Genet. 28, 380-383.
13. Egner, R., Thumm, M., Straub, M., Simeon, A., Schüller, H.J., and Wolf, D.H. (1993). Tracing intracellular proteolytic pathways. Proteolysis of fatty acid synthase and other cytoplasmic proteins in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 268, 27269-27276.
14. Ellison, M.J., and Hochstrasser, M. (1991). Epitope-tagged ubiquitin. A new probe for analyzing ubiquitin function. J. Biol. Chem. 266, 21150-21157.
15. Funayama, S., Gancedo, J.M., and Gancedo, C. (1980). Turnover of yeast fructose-bisphosphatase in different metabolic conditions. Eur. J. Biochem. 109, 61-66.
16. Gancedo, C. (1971). Inactivation of fructose-1,6-diphosphatase by glucose in yeast. J. Bacteriol. 107, 401-405.
17. Güldener, U., Heck, S., Fielder, T., Beinhauer, J., and Hegemann, J.H. (1996). A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 24, 2519-2524.
18. Guthrie, C., and Fink, G.R. (1991). Guide to Yeast Genetics and Molecular Biology, vol, 194, New York: Academic Press.
19. Hämmerle, M., Bauer, J., Rose, M., Szallies, A., Thumm, M., Dusterhus, S., Mecke, D., Entian, K.D., and Wolf, D.H. (1998). Proteins of newly isolated mutants and the amino-terminal proline are essential for ubiquitin-proteasome-catalyzed catabolite degradation of fructose-1,6-bisphosphatase of Saccharomyces cerevisiae. J. Biol. Chem. 273, 25000-25005.
20. Hilt, W., and Wolf, D.H. (1996). Proteasomes: destruction as a program. Trends Biochem Sci. 21, 96-102.
21. Hilt, W., and Wolf, D.H. (2000). Proteasomes. The World of Regulatory Proteolysis, Georgetown, VA: Landes Bioscience, 1-387.
22. Ho, Y., et al. (2002). Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415, 180-183.
23. Hoffman, M., and Chiang, H.L. (1996). Isolation of degradation-deficient mutants defective in the targeting of fructose-1,6-bisphosphatase into the vacuole for degradation in Saccharomyces cerevisiae. Genetics 143, 1555-1566.
24. Holzer, H. (1976). Catabolite inactivation in yeast. Trends Biochem. Sci. 1, 178-181.
25. Horak, J., Regelmann, J., and Wolf, D.H. (2002). Two distinct proteolytic systems responsible for glucose-induced degradation of fructose-1,6-bisphosphatase and the Gal2p transporter in the yeast Saccharomyces cerevisiae share the same protein components of the glucose signaling pathway. J. Biol. Chem. 277, 8248-8254.
26. Horak, J., and Wolf, D.H. (1997). Catabolite inactivation of the galactose transporter in the yeast Saccharomyces cerevisiae: ubiquitination, endocytosis, and degradation in the vacuole. J. Bacteriol. 179, 1541-1549.
27. Horak, J., and Wolf, D.H. (2001). Glucose-induced monoubiquitination of the Saccharomyces cerevisiae galactose transporter is sufficient to signal its internalization. J. Bacteriol. 183, 3083-3088.
28. Huang, P.H., and Chiang, H.L. (1997). Identification of novel vesicles in the cytosol to vacuole protein degradation pathway. J. Cell Biol. 136, 803-810.
29. Jiang, Y., Davis, C., and Broach, J.R. (1998). Efficient transition to growth on fermentable carbon sources in Saccharomyces cerevisiae requires signaling through the Ras pathway. EMBO J 17, 6942-6951.
30. Kim, J., Scott, S.V., Oda, M.N., and Klionsky, D.J. (1997). Transport of a large oligomeric protein by the cytoplasm to vacuole protein targeting pathway. J. Cell Biol. 137, 609-618.
31. Mechler, B., and Wolf, D.H. (1981). Analysis of proteinase A function in yeast. Eur. J. Biochem. 121, 47-52.
32. Richter-Ruoff, B., Heinemeyer, W., and Wolf, D.H. (1992). The proteasome/multicatalytic-multifunctional proteinase. In vivo function in the ubiquitin-dependent N-end rule pathway of protein degradation in eukaryotes. FEBS Lett. 302, 192-196.
33. Rose, M.D., Novick, P., Thomas, J.H., Botstein, D., and Fink, G.R. (1987). A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene 60, 237-243.
34. Schork, S., Bee, G., Thumm, M., and Wolf, D.H. (1994a). Catabolite inactivation of fructose-1,6-bisphosphatase in yeast is mediated by the proteasome. FEBS Lett. 349, 270-274.
35. Schork, S., Bee, G., Thumm, M., and Wolf, D.H. (1994b). Site of catabolite inactivation. Nature 369, 283-284.
36. Schork, S.M., Thumm, M., and Wolf, D.H. (1995). Catabolite inactivation of fructose-1,6-bisphosphatase of Saccharomyces cerevisiae. Degradation occurs via the ubiquitin pathway. J. Biol. Chem. 270, 26446-26450.
37. Schüle, T., Rose, M., Entian, K.D., Thumm, M., and Wolf, D.H. (2000). Ubc8p functions in catabolite degradation of fructose-1,6-bisphosphatase in yeast. EMBO J. 19, 2161-2167.
38. Seufert, W., and Jentsch, S. (1992). In vivo function of the proteasome in the ubiquitin pathway. EMBO J. 11, 3077-3080.
39. Smith, D.S., Niethammer, M., Ayala, R., Zhou, Y., Gambello, M.J., Wynshaw-Boris, A., and Tsai, L.H. (2000). Regulation of cytoplasmic dynein behavior and microtubule organization by mammalian Lisl. Nat. Cell Biol. 2, 767-75.
40. Smith, T.F., Gaitatzes, C., Saxena, K., and Neer, E.J. (1999). The WD repeat: a common architecture for diverse functions. Trends Biochem. Sci. 24, 181-185.
41. Teichert, U., Mechler, B., Müller, H., and Wolf, D.H. (1989). Lysosomal (vacuolar) proteinases of yeast are essential catalysts for protein degradation, differentiation, and cell survival. J. Biol. Chem. 264, 16037-16045.
42. van der Merwe, G.K., Cooper, T.G., and van Vuuren, H.J. (2001). Ammonia regulates VID30 expression and Vid30p function shifts nitrogen metabolism toward glutamate formation especially when Saccharomyces cerevisiae is grown in low concentrations of ammonia. J. Biol. Chem. 276, 28659-28666.
43. Wolf, D.H., and Ehmann, C. (1979). Studies on a proteinase B mutant of yeast. Eur. J. Biochem. 98, 375-384.