The saccharomyces cerevisiae vacuolar acid trehalase is targeted at the cell surface for its physiological function

FEBS Journal

Volumn 276, Issue 19, 2009, Pages 5432-5446

  He, Susu ^a,b,c   Bystricky, Kerstin ^c,d   Leon, Sebastien ^e   François, Jean M ^a,b,c   Parrou, Jean L ^a,b,c  

^a INSA   (France)

^b UMR792 INGÉNIERIE DES SYSTÈMES BIOLOGIQUES ET DES PROCÉDÉS   (France)

^c CNRS   (France)

^d UNIVERSITÉ DE TOULOUSE   (France)

^e INSTITUT JACQUES MONOD   (France)

Author keywords

Acid trehalase; Cell surface; Fluorescence microscopy; Saccharomyces cerevisiae; Secretion

Indexed keywords

ATH1 ENZYME; BETA FRUCTOFURANOSIDASE; TREHALASE; TREHALOSE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

BASE SEQUENCE; BETA-FRUCTOFURANOSIDASE; CELL MEMBRANE; DNA PRIMERS; DNA, FUNGAL; GENES, FUNGAL; GENETIC COMPLEMENTATION TEST; LUMINESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUCROSE; TREHALASE; TREHALOSE; VACUOLES;

SACCHAROMYCES CEREVISIAE;

EID: 70349229608     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07227.x     Document Type: Article

References (47)

1. Lillie SH Pringle JR (1980) Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J Bacteriol 143, 1384 1394.
2. Hottiger T, Boller T Wiemken A (1987) Rapid changes of heat and desiccation tolerance correlated with changes of trehalose content in Saccharomyces cerevisiae cells subjected to temperature shifts. FEBS Lett 220, 113 115.
3. Jules M, Beltran G, Francois J Parrou JL (2008) New insights into trehalose metabolism by Saccharomyces cerevisiae: NTH2 encodes a functional cytosolic trehalase, and deletion of TPS1 reveals Ath1p-dependent trehalose mobilization. Appl Environ Microbiol 74, 605 614.
4. Singer MA Lindquist S (1998) Thermotolerance in Saccharomyces cerevisiae: the Yin and Yang of trehalose. Trends Biotechnol 16, 460 468.
5. Simola M, Hanninen AL, Stranius SM Makarow M (2000) Trehalose is required for conformational repair of heat-denatured proteins in the yeast endoplasmic reticulum but not for maintenance of membrane traffic functions after severe heat stress [In Process Citation]. Mol Microbiol 37, 42 53.
6. Francois J Parrou JL (2001) Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 25, 125 145.
7. Mittenbuhler K Holzer H (1988) Purification and characterization of acid trehalase from the yeast suc2 mutant. J Biol Chem 263, 8537 8543.
8. Destruelle M, Holzer H Klionsky DJ (1995) Isolation and characterization of a novel yeast gene, ATH1, that is required for vacuolar acid trehalase activity. Yeast 11, 1015 1025.
9. Pedreno Y, Maicas S, Arguelles JC, Sentandreu R Valentin E (2004) The ATC1 gene encodes a cell wall-linked acid trehalase required for growth on trehalose in Candida albicans. J Biol Chem 279, 40852 40860.
10. Swaim CL, Anton BP, Sharma SS, Taron CH Benner JS (2008) Physical and computational analysis of the yeast Kluyveromyces lactis secreted proteome. Proteomics 8, 2714 2723.
11. Keller F, Schellenberg M Wiemken A (1982) Localization of trehalase in vacuoles and of trehalose in the cytosol of yeast (Saccharomyces cerevisiae). Arch Microbiol 131, 298 301.
12. Huang J, Reggiori F Klionsky DJ (2007) The transmembrane domain of acid trehalase mediates ubiquitin-independent multivesicular body pathway sorting. Mol Biol Cell 18, 2511 2524.
13. Nwaka S, Mechler B, Destruelle M Holzer H (1995) Phenotypic features of trehalase mutants in Saccharomyces cerevisiae. FEBS Lett 360, 286 290.
14. Jules M, Guillou V, Francois J Parrou JL (2004) Two distinct pathways for trehalose assimilation in the yeast Saccharomyces cerevisiae. Appl Environ Microbiol 70, 2771 2778.
15. Roberts CJ, Nothwehr SF Stevens TH (1992) Membrane protein sorting in the yeast secretory pathway: evidence that the vacuole may be the default compartment. J Cell Biol 119, 69 83.
16. Leon S, Erpapazoglou Z Haguenauer-Tsapis R (2008) Ear1p and Ssh4p are new adaptors of the ubiquitin ligase Rsp5p for cargo ubiquitylation and sorting at multivesicular bodies. Mol Biol Cell 19, 2379 2388.
17. Silveira MC, Carvajal E Bon EP (1996) Assay for in vivo yeast invertase activity using NaF. Anal Biochem 238, 26 28.
18. San Miguel PF Arguelles JC (1994) Differential changes in the activity of cytosolic and vacuolar trehalases along the growth cycle of Saccharomyces cerevisiae. Biochim Biophys Acta 1200, 155 160.
19. Wieczorke R, Krampe S, Weierstall T, Freidel K, Hollenberg CP Boles E (1999) Concurrent knock-out of at least 20 transporter genes is required to block uptake of hexoses in Saccharomyces cerevisiae. FEBS Lett 464, 123 128.
20. Schultz J, Copley RR, Doerks T, Ponting CP Bork P (2000) SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res 28, 231 234.
21. Letunic I, Doerks T Bork P (2009) SMART 6: recent updates and new developments. Nucleic Acids Res 37, D229 D232.
22. Parrou JL, Jules M, Beltran G Francois J (2005) Acid trehalase in yeasts and filamentous fungi: localization, regulation and physiological function. FEMS Yeast Res 5, 503 511.
23. Haguenauer-Tsapis R (1992) Protein-specific features of the general secretion pathway in yeast: the secretion of acid phosphatase. Mol Microbiol 6, 573 579.
24. Ammerer G, Hunter CP, Rothman JH, Saari GC, Valls LA Stevens TH (1986) PEP4 gene of Saccharomyces cerevisiae encodes proteinase A, a vacuolar enzyme required for processing of vacuolar precursors. Mol Cell Biol 6, 2490 2499.
25. Bryant NJ Stevens TH (1998) Vacuole biogenesis in Saccharomyces cerevisiae: protein transport pathways to the yeast vacuole. Microbiol Mol Biol Rev 62, 230 247.
26. Blondel MO, Morvan J, Dupre S, Urban-Grimal D, Haguenauer-Tsapis R Volland C (2004) Direct sorting of the yeast uracil permease to the endosomal system is controlled by uracil binding and Rsp5p-dependent ubiquitylation. Mol Biol Cell 15, 883 895.
27. Nwaka S Holzer H (1998) Molecular biology of trehalose and the trehalases in the yeast Saccharomyces cerevisiae. Prog Nucleic Acid Res Mol Biol 58, 197 237.
28. Plourde-Owobi L, Durner S, Parrou JL, Wieczorke R, Goma G Francois J (1999) AGT1, encoding an alpha-glucoside transporter involved in uptake and intracellular accumulation of trehalose in Saccharomyces cerevisiae. J Bacteriol 181, 3830 3832.
29. Muller J, Aeschbacher RA, Wingler A, Boller T Wiemken A (2001) Trehalose and trehalase in Arabidopsis. Plant Physiol 125, 1086 1093.
30. Frison M, Parrou JL, Guillaumot D, Masquelier D, Francois J, Chaumont F Batoko H (2007) The Arabidopsis thaliana trehalase is a plasma membrane-bound enzyme with extracellular activity. FEBS Lett 581, 4010 4016.
31. Vater CA, Raymond CK, Ekena K, Howald-Stevenson I Stevens TH (1992) The VPS1 protein, a homolog of dynamin required for vacuolar protein sorting in Saccharomyces cerevisiae, is a GTPase with two functionally separable domains. J Cell Biol 119, 773 786.
32. Gil-Navarro I, Gil ML, Casanova M, O'Connor JE, Martinez JP Gozalbo D (1997) The glycolytic enzyme glyceraldehyde-3-phosphate dehydrogenase of Candida albicans is a surface antigen. J Bacteriol 179, 4992 4999.
33. Alloush HM, Lopez-Ribot JL, Masten BJ Chaffin WL (1997) 3-Phosphoglycerate kinase: a glycolytic enzyme protein present in the cell wall of Candida albicans. Microbiology 143, 321 330.
34. Edwards SR Chaffin WL (1999) Enolase is present in the cell wall of Saccharomyces cerevisiae. FEMS Microbiol Lett 177, 211 216.
35. Lopez-Villar E, Monteoliva L, Larsen MR, Sachon E, Shabaz M, Pardo M, Pla J, Gil C, Roepstorff P Nombela C (2006) Genetic and proteomic evidences support the localization of yeast enolase in the cell surface. Proteomics 6, S107 S118.
36. Nombela C, Gil C Chaffin WL (2006) Non-conventional protein secretion in yeast. Trends Microbiol 14, 15 21.
37. Prudovsky I, Mandinova A, Soldi R, Bagala C, Graziani I, Landriscina M, Tarantini F, Duarte M, Bellum S, Doherty H et al. (2003) The non-classical export routes: FGF1 and IL-1alpha point the way. J Cell Sci 116, 4871 4881.
38. Harris SD Cotter DA (1987) Vacuolar (lysosomal) trehalase of Saccharomyces cerevisiae. Curr Microbiol 15, 245 249.
39. Mittenbuhler K Holzer H (1991) Characterization of different forms of yeast acid trehalase in the secretory pathway. Arch Microbiol 155, 217 220.
40. Biswas N Ghosh AK (1996) Characterisation of an acid trehalase of Saccharomyces cerevisiae present in trehalase-sucrase aggregate. Biochim Biophys Acta 1290, 95 100.
41. Destruelle M, Holzer H Klionsky DJ (1994) Identification and characterization of a novel yeast gene: the YGP1 gene product is a highly glycosylated secreted protein that is synthesized in response to nutrient limitation. Mol Cell Biol 14, 2740 2754.
42. Woods RA Gietz RD (2001) High-efficiency transformation of plasmid DNA into yeast. Methods Mol Biol 177, 85 97.
43. Pont-Kingdon G (1994) Construction of chimeric molecules by a two-step recombinant PCR method. BioTechniques 16, 1010 1011.
44. del Castillo AL, Nieto SA Sentandreu R (1992) Differential expression of the invertase-encoding SUC genes in Saccharomyces cerevisiae. Gene 120, 59 65.
45. Gietz RD Sugino A (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74, 527 534.
46. Castillo L, Martinez AI, Gelis S, Ruiz-Herrera J, Valentin E Sentandreu R (2008) Genomic response programs of Saccharomyces cerevisiae following protoplasting and regeneration. Fungal Genet Biol 45, 253 265.
47. Wach A, Brachat A, Pohlmann R Philippsen P (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793 1808.