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. 1996 Apr;178(8):2245–2254. doi: 10.1128/jb.178.8.2245-2254.1996

Characterization of the glucose-induced inactivation of maltose permease in Saccharomyces cerevisiae.

I Medintz 1, H Jiang 1, E K Han 1, W Cui 1, C A Michels 1
PMCID: PMC177932  PMID: 8636025

Abstract

The addition of glucose to maltose-fermenting Saccharomyces cerevisiae cells causes a rapid and irreversible loss of the ability to transport maltose, resulting both from the repression of transcription of the maltose permease gene and from the inactivation of maltose permease. The latter is referred to as glucose-induced inactivation or catabolite inactivation. We describe an analysis of this process in a maltose-fermenting strain expressing a hemagglutinin (HA)-tagged allele of MAL61, encoding maltose permease. The transfer of maltose-induced cells expressing the Mal61/HA protein to rich medium containing glucose produces a decrease in maltose transport rates which is paralleled by a decrease in Mal61/HA maltose permease protein levels. In nitrogen starvation medium, glucose produces a biphasic inactivation, i.e., an initial, rapid loss in transport activity (inhibition) followed by a slower decrease in transport activity, which correlates with a decrease in the amount of maltose permease protein (proteolysis). The inactivation in both rich and nitrogen-starved media results from a decrease in Vmax with no apparent change in Km. Using strains carrying mutations in END3, REN1(VPS2), PEP4, and PRE1 PRE2, we demonstrate that the proteolysis of Mal61/HAp is dependent on endocytosis and vacuolar proteolysis and is independent of the proteosome. Moreover, we show that the Mal61/HA maltose permease is present in differentially phosphorylated forms.

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Selected References

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  1. Ammerer G., Hunter C. P., Rothman J. H., Saari G. C., Valls L. A., Stevens T. H. PEP4 gene of Saccharomyces cerevisiae encodes proteinase A, a vacuolar enzyme required for processing of vacuolar precursors. Mol Cell Biol. 1986 Jul;6(7):2490–2499. doi: 10.1128/mcb.6.7.2490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Benito B., Moreno E., Lagunas R. Half-life of the plasma membrane ATPase and its activating system in resting yeast cells. Biochim Biophys Acta. 1991 Apr 2;1063(2):265–268. doi: 10.1016/0005-2736(91)90381-h. [DOI] [PubMed] [Google Scholar]
  3. Boeke J. D., LaCroute F., Fink G. R. A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet. 1984;197(2):345–346. doi: 10.1007/BF00330984. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Charron M. J., Dubin R. A., Michels C. A. Structural and functional analysis of the MAL1 locus of Saccharomyces cerevisiae. Mol Cell Biol. 1986 Nov;6(11):3891–3899. doi: 10.1128/mcb.6.11.3891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Cheng Q., Michels C. A. The maltose permease encoded by the MAL61 gene of Saccharomyces cerevisiae exhibits both sequence and structural homology to other sugar transporters. Genetics. 1989 Nov;123(3):477–484. doi: 10.1093/genetics/123.3.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. 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]
  11. Dubin R. A., Charron M. J., Haut S. R., Needleman R. B., Michels C. A. Constitutive expression of the maltose fermentative enzymes in Saccharomyces carlsbergensis is dependent upon the mutational activation of a nonessential homolog of MAL63. Mol Cell Biol. 1988 Mar;8(3):1027–1035. doi: 10.1128/mcb.8.3.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Görts C. P. Effect of glucose on the activity and the kinetics of the maltose-uptake system and of alpha-glucosidase in Saccharomyces cerevisiae. Biochim Biophys Acta. 1969 Jul 30;184(2):299–305. doi: 10.1016/0304-4165(69)90032-4. [DOI] [PubMed] [Google Scholar]
  13. Han E. K., Cotty F., Sottas C., Jiang H., Michels C. A. Characterization of AGT1 encoding a general alpha-glucoside transporter from Saccharomyces. Mol Microbiol. 1995 Sep;17(6):1093–1107. doi: 10.1111/j.1365-2958.1995.mmi_17061093.x. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Hemmings B. A., Zubenko G. S., Hasilik A., Jones E. W. Mutant defective in processing of an enzyme located in the lysosome-like vacuole of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1981 Jan;78(1):435–439. doi: 10.1073/pnas.78.1.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hicke L., Riezman H. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell. 1996 Jan 26;84(2):277–287. doi: 10.1016/s0092-8674(00)80982-4. [DOI] [PubMed] [Google Scholar]
  17. Hu Z., Nehlin J. O., Ronne H., Michels C. A. MIG1-dependent and MIG1-independent glucose regulation of MAL gene expression in Saccharomyces cerevisiae. Curr Genet. 1995 Aug;28(3):258–266. doi: 10.1007/BF00309785. [DOI] [PubMed] [Google Scholar]
  18. James D. E., Hiken J., Lawrence J. C., Jr Isoproterenol stimulates phosphorylation of the insulin-regulatable glucose transporter in rat adipocytes. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8368–8372. doi: 10.1073/pnas.86.21.8368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kolodziej P. A., Young R. A. Epitope tagging and protein surveillance. Methods Enzymol. 1991;194:508–519. doi: 10.1016/0076-6879(91)94038-e. [DOI] [PubMed] [Google Scholar]
  20. Kublaoui B., Lee J., Pilch P. F. Dynamics of signaling during insulin-stimulated endocytosis of its receptor in adipocytes. J Biol Chem. 1995 Jan 6;270(1):59–65. doi: 10.1074/jbc.270.1.59. [DOI] [PubMed] [Google Scholar]
  21. Kölling R., Hollenberg C. P. The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J. 1994 Jul 15;13(14):3261–3271. doi: 10.1002/j.1460-2075.1994.tb06627.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. 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]
  25. Marcus F., Rittenhouse J., Moberly L., Edelstein I., Hiller E., Rogers D. T. Yeast (Saccharomyces cerevisiae) fructose-1,6-bisphosphatase. Properties of phospho and dephospho forms and of two mutants in which serine 11 has been changed by site-directed mutagenesis. J Biol Chem. 1988 May 5;263(13):6058–6062. [PubMed] [Google Scholar]
  26. 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]
  27. Mazón M. J., Gancedo J. M., Gancedo C. Inactivation of yeast fructose-1,6-bisphosphatase. In vivo phosphorylation of the enzyme. J Biol Chem. 1982 Feb 10;257(3):1128–1130. [PubMed] [Google Scholar]
  28. Müller D., Holzer H. Regulation of fructose-1,6-bisphosphatase in yeast by phosphorylation/dephosphorylation. Biochem Biophys Res Commun. 1981 Dec 15;103(3):926–933. doi: 10.1016/0006-291x(81)90899-8. [DOI] [PubMed] [Google Scholar]
  29. Needleman R. Control of maltase synthesis in yeast. Mol Microbiol. 1991 Sep;5(9):2079–2084. doi: 10.1111/j.1365-2958.1991.tb02136.x. [DOI] [PubMed] [Google Scholar]
  30. Neeff J., Hägele E., Nauhaus J., Heer U., Mecke D. Evidence for catabolite degradation in the glucose-dependent inactivation of yeast cytoplasmic malate dehydrogenase. Eur J Biochem. 1978 Jul 3;87(3):489–495. doi: 10.1111/j.1432-1033.1978.tb12399.x. [DOI] [PubMed] [Google Scholar]
  31. Peinado J. M., Loureiro-Dias M. C. Reversible loss of affinity induced by glucose in the maltose-H+ symport of Saccharomyces cerevisiae. Biochim Biophys Acta. 1986 Apr 14;856(2):189–192. doi: 10.1016/0005-2736(86)90027-1. [DOI] [PubMed] [Google Scholar]
  32. Ramos J., Cirillo V. P. Role of cyclic-AMP-dependent protein kinase in catabolite inactivation of the glucose and galactose transporters in Saccharomyces cerevisiae. J Bacteriol. 1989 Jun;171(6):3545–3548. doi: 10.1128/jb.171.6.3545-3548.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ramos J., Szkutnicka K., Cirillo V. P. Relationship between low- and high-affinity glucose transport systems of Saccharomyces cerevisiae. J Bacteriol. 1988 Nov;170(11):5375–5377. doi: 10.1128/jb.170.11.5375-5377.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Riballo E., Herweijer M., Wolf D. H., Lagunas R. Catabolite inactivation of the yeast maltose transporter occurs in the vacuole after internalization by endocytosis. J Bacteriol. 1995 Oct;177(19):5622–5627. doi: 10.1128/jb.177.19.5622-5627.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Rittenhouse J., Harrsch P. B., Kim J. N., Marcus F. Amino acid sequence of the phosphorylation site of yeast (Saccharomyces cerevisiae) fructose-1,6-bisphosphatase. J Biol Chem. 1986 Mar 25;261(9):3939–3943. [PubMed] [Google Scholar]
  37. 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]
  38. Shah H. C., Carlson G. P. Alteration by phenobarbital and 3-methyl-cholanthrene of functional and structural changes in rat liver due to carbon tetrachloride inhalation. J Pharmacol Exp Ther. 1975 Apr;193(1):281–292. [PubMed] [Google Scholar]
  39. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Stanbrough M., Magasanik B. Transcriptional and posttranslational regulation of the general amino acid permease of Saccharomyces cerevisiae. J Bacteriol. 1995 Jan;177(1):94–102. doi: 10.1128/jb.177.1.94-102.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Tortora P., Birtel M., Lenz A. G., Holzer H. Glucose-dependent metabolic interconversion of fructose-1, 6-bisphosphatase in yeast. Biochem Biophys Res Commun. 1981 May 29;100(2):688–695. doi: 10.1016/s0006-291x(81)80230-6. [DOI] [PubMed] [Google Scholar]
  42. Van den Broek P. J., Van Leeuwen C. C., Weusthuis R. A., Postma E., Van Dijken J. P., Karssies R. H., Amons R. Identification of the maltose transport protein of Saccharomyces cerevisiae. Biochem Biophys Res Commun. 1994 Apr 15;200(1):45–51. doi: 10.1006/bbrc.1994.1411. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. Wolf D. H., Fink G. R. Proteinase C (carboxypeptidase Y) mutant of yeast. J Bacteriol. 1975 Sep;123(3):1150–1156. doi: 10.1128/jb.123.3.1150-1156.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Zanolari B., Raths S., Singer-Krüger B., Riezman H. Yeast pheromone receptor endocytosis and hyperphosphorylation are independent of G protein-mediated signal transduction. Cell. 1992 Nov 27;71(5):755–763. doi: 10.1016/0092-8674(92)90552-n. [DOI] [PubMed] [Google Scholar]

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