Abstract
The maltose transporter of Saccharomyces cerevisiae is rapidly degraded during fermentation in the absence of a nitrogen source. The location and mechanism of degradation of the transporter have been investigated. Using mutants defective in endocytosis, we have shown that degradation of this transporter requires internalization by endocytosis. In addition, studies of mutants defective in proteasome or vacuolar proteolysis revealed that degradation occurs in the vacuole and is independent of proteasome function. The results also revealed that degradation of the maltose transporter requires Sec18p and raised the question of whether in the absence of Sec18p activity the internalized maltose transporter is recycled back to the plasma membrane.
Full Text
The Full Text of this article is available as a PDF (323.1 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Beckers C. J., Block M. R., Glick B. S., Rothman J. E., Balch W. E. Vesicular transport between the endoplasmic reticulum and the Golgi stack requires the NEM-sensitive fusion protein. Nature. 1989 Jun 1;339(6223):397–398. doi: 10.1038/339397a0. [DOI] [PubMed] [Google Scholar]
- Benito B., Lagunas R. The low-affinity component of Saccharomyces cerevisiae maltose transport is an artifact. J Bacteriol. 1992 May;174(9):3065–3069. doi: 10.1128/jb.174.9.3065-3069.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Busturia A., Lagunas R. Catabolite inactivation of the glucose transport system in Saccharomyces cerevisiae. J Gen Microbiol. 1986 Feb;132(2):379–385. doi: 10.1099/00221287-132-2-379. [DOI] [PubMed] [Google Scholar]
- Cheng Q., Michels C. A. MAL11 and MAL61 encode the inducible high-affinity maltose transporter of Saccharomyces cerevisiae. J Bacteriol. 1991 Mar;173(5):1817–1820. doi: 10.1128/jb.173.5.1817-1820.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chiang H. L., Schekman R. Regulated import and degradation of a cytosolic protein in the yeast vacuole. Nature. 1991 Mar 28;350(6316):313–318. doi: 10.1038/350313a0. [DOI] [PubMed] [Google Scholar]
- Ciechanover A. The ubiquitin-proteasome proteolytic pathway. Cell. 1994 Oct 7;79(1):13–21. doi: 10.1016/0092-8674(94)90396-4. [DOI] [PubMed] [Google Scholar]
- Davis N. G., Horecka J. L., Sprague G. F., Jr Cis- and trans-acting functions required for endocytosis of the yeast pheromone receptors. J Cell Biol. 1993 Jul;122(1):53–65. doi: 10.1083/jcb.122.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeJuan C., Lagunas R. Inactivation of the galactose transport system in Saccharomyces cerevisiae. FEBS Lett. 1986 Oct 27;207(2):258–261. doi: 10.1016/0014-5793(86)81500-9. [DOI] [PubMed] [Google Scholar]
- Diaz R., Mayorga L. S., Weidman P. J., Rothman J. E., Stahl P. D. Vesicle fusion following receptor-mediated endocytosis requires a protein active in Golgi transport. Nature. 1989 Jun 1;339(6223):398–400. doi: 10.1038/339398a0. [DOI] [PubMed] [Google Scholar]
- Gruenberg J., Howell K. E. Membrane traffic in endocytosis: insights from cell-free assays. Annu Rev Cell Biol. 1989;5:453–481. doi: 10.1146/annurev.cb.05.110189.002321. [DOI] [PubMed] [Google Scholar]
- Hare J. F. Mechanisms of membrane protein turnover. Biochim Biophys Acta. 1990 Feb 28;1031(1):71–90. doi: 10.1016/0304-4157(90)90003-u. [DOI] [PubMed] [Google Scholar]
- Heinemeyer W., Gruhler A., Möhrle V., Mahé Y., Wolf D. H. PRE2, highly homologous to the human major histocompatibility complex-linked RING10 gene, codes for a yeast proteasome subunit necessary for chrymotryptic activity and degradation of ubiquitinated proteins. J Biol Chem. 1993 Mar 5;268(7):5115–5120. [PubMed] [Google Scholar]
- Heinemeyer W., Kleinschmidt J. A., Saidowsky J., Escher C., Wolf D. H. Proteinase yscE, the yeast proteasome/multicatalytic-multifunctional proteinase: mutants unravel its function in stress induced proteolysis and uncover its necessity for cell survival. EMBO J. 1991 Mar;10(3):555–562. doi: 10.1002/j.1460-2075.1991.tb07982.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hilt W., Heinemeyer W., Wolf D. H. Studies on the yeast proteasome uncover its basic structural features and multiple in vivo functions. Enzyme Protein. 1993;47(4-6):189–201. doi: 10.1159/000468678. [DOI] [PubMed] [Google Scholar]
- Jones E. W. Tackling the protease problem in Saccharomyces cerevisiae. Methods Enzymol. 1991;194:428–453. doi: 10.1016/0076-6879(91)94034-a. [DOI] [PubMed] [Google Scholar]
- Jones E. W. Three proteolytic systems in the yeast saccharomyces cerevisiae. J Biol Chem. 1991 May 5;266(13):7963–7966. [PubMed] [Google Scholar]
- Lagunas R., Dominguez C., Busturia A., Sáez M. J. Mechanisms of appearance of the Pasteur effect in Saccharomyces cerevisiae: inactivation of sugar transport systems. J Bacteriol. 1982 Oct;152(1):19–25. doi: 10.1128/jb.152.1.19-25.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lagunas R. Misconceptions about the energy metabolism of Saccharomyces cerevisiae. Yeast. 1986 Dec;2(4):221–228. doi: 10.1002/yea.320020403. [DOI] [PubMed] [Google Scholar]
- Lagunas R. Sugar transport in Saccharomyces cerevisiae. FEMS Microbiol Rev. 1993 Apr;10(3-4):229–242. doi: 10.1016/0378-1097(93)90598-v. [DOI] [PubMed] [Google Scholar]
- Lai K., Bolognese C. P., Swift S., McGraw P. Regulation of inositol transport in Saccharomyces cerevisiae involves inositol-induced changes in permease stability and endocytic degradation in the vacuole. J Biol Chem. 1995 Feb 10;270(6):2525–2534. doi: 10.1074/jbc.270.6.2525. [DOI] [PubMed] [Google Scholar]
- Lillie S. H., Brown S. S. Artifactual immunofluorescent labelling in yeast, demonstrated by affinity purification of antibody. Yeast. 1987 Jun;3(2):63–70. doi: 10.1002/yea.320030202. [DOI] [PubMed] [Google Scholar]
- Lucero P., Herweijer M., Lagunas R. Catabolite inactivation of the yeast maltose transporter is due to proteolysis. FEBS Lett. 1993 Oct 25;333(1-2):165–168. doi: 10.1016/0014-5793(93)80397-d. [DOI] [PubMed] [Google Scholar]
- Matern H., Holzer H. Catabolite inactivation of the galactose uptake system in yeast. J Biol Chem. 1977 Sep 25;252(18):6399–6402. [PubMed] [Google Scholar]
- Matile P., Wiemken A. The vacuole as the lysosome of the yeast cell. Arch Mikrobiol. 1967 Feb 20;56(2):148–155. doi: 10.1007/BF00408765. [DOI] [PubMed] [Google Scholar]
- Moehle C. M., Dixon C. K., Jones E. W. Processing pathway for protease B of Saccharomyces cerevisiae. J Cell Biol. 1989 Feb;108(2):309–325. doi: 10.1083/jcb.108.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moehle C. M., Tizard R., Lemmon S. K., Smart J., Jones E. W. Protease B of the lysosomelike vacuole of the yeast Saccharomyces cerevisiae is homologous to the subtilisin family of serine proteases. Mol Cell Biol. 1987 Dec;7(12):4390–4399. doi: 10.1128/mcb.7.12.4390. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Novick P., Ferro S., Schekman R. Order of events in the yeast secretory pathway. Cell. 1981 Aug;25(2):461–469. doi: 10.1016/0092-8674(81)90064-7. [DOI] [PubMed] [Google Scholar]
- Raths S., Rohrer J., Crausaz F., Riezman H. end3 and end4: two mutants defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces cerevisiae. J Cell Biol. 1993 Jan;120(1):55–65. doi: 10.1083/jcb.120.1.55. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rendueles P. S., Wolf D. H. Proteinase function in yeast: biochemical and genetic approaches to a central mechanism of post-translational control in the eukaryote cell. FEMS Microbiol Rev. 1988 Feb;4(1):17–45. doi: 10.1111/j.1574-6968.1988.tb02706.x-i1. [DOI] [PubMed] [Google Scholar]
- Riballo E., Lagunas R. Involvement of endocytosis in catabolite inactivation of the K+ and glucose transport systems in Saccharomyces cerevisiae. FEMS Microbiol Lett. 1994 Aug 1;121(1):77–80. doi: 10.1111/j.1574-6968.1994.tb07078.x. [DOI] [PubMed] [Google Scholar]
- Richter-Ruoff B., Wolf D. H., Hochstrasser M. Degradation of the yeast MAT alpha 2 transcriptional regulator is mediated by the proteasome. FEBS Lett. 1994 Oct 31;354(1):50–52. doi: 10.1016/0014-5793(94)01085-4. [DOI] [PubMed] [Google Scholar]
- Richter-Ruoff B., Wolf D. H. Proteasome and cell cycle. Evidence for a regulatory role of the protease on mitotic cyclins in yeast. FEBS Lett. 1993 Dec 20;336(1):34–36. doi: 10.1016/0014-5793(93)81603-w. [DOI] [PubMed] [Google Scholar]
- Riezman H. Yeast endocytosis. Trends Cell Biol. 1993 Aug;3(8):273–277. doi: 10.1016/0962-8924(93)90056-7. [DOI] [PubMed] [Google Scholar]
- Rivett A. J. Proteasomes: multicatalytic proteinase complexes. Biochem J. 1993 Apr 1;291(Pt 1):1–10. doi: 10.1042/bj2910001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rodicio R. Insertion of non-homologous DNA sequences into a regulatory gene cause a constitutive maltase synthesis in yeast. Curr Genet. 1986;11(3):235–241. doi: 10.1007/BF00420612. [DOI] [PubMed] [Google Scholar]
- Schork S. M., Bee G., Thumm M., Wolf D. H. Catabolite inactivation of fructose-1,6-bisphosphatase in yeast is mediated by the proteasome. FEBS Lett. 1994 Aug 1;349(2):270–274. doi: 10.1016/0014-5793(94)00668-7. [DOI] [PubMed] [Google Scholar]
- Schork S. M., Bee G., Thumm M., Wolf D. H. Site of catabolite inactivation. Nature. 1994 May 26;369(6478):283–284. doi: 10.1038/369283a0. [DOI] [PubMed] [Google Scholar]
- Singer B., Riezman H. Detection of an intermediate compartment involved in transport of alpha-factor from the plasma membrane to the vacuole in yeast. J Cell Biol. 1990 Jun;110(6):1911–1922. doi: 10.1083/jcb.110.6.1911. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Teichert U., Mechler B., Müller H., Wolf D. H. Lysosomal (vacuolar) proteinases of yeast are essential catalysts for protein degradation, differentiation, and cell survival. J Biol Chem. 1989 Sep 25;264(27):16037–16045. [PubMed] [Google Scholar]
- Volland C., Urban-Grimal D., Géraud G., Haguenauer-Tsapis R. Endocytosis and degradation of the yeast uracil permease under adverse conditions. J Biol Chem. 1994 Apr 1;269(13):9833–9841. [PubMed] [Google Scholar]
- Woolford C. A., Noble J. A., Garman J. D., Tam M. F., Innis M. A., Jones E. W. Phenotypic analysis of proteinase A mutants. Implications for autoactivation and the maturation pathway of the vacuolar hydrolases of Saccharomyces cerevisiae. J Biol Chem. 1993 Apr 25;268(12):8990–8998. [PubMed] [Google Scholar]
- Yaglom J., Linskens M. H., Sadis S., Rubin D. M., Futcher B., Finley D. p34Cdc28-mediated control of Cln3 cyclin degradation. Mol Cell Biol. 1995 Feb;15(2):731–741. doi: 10.1128/mcb.15.2.731. [DOI] [PMC free article] [PubMed] [Google Scholar]