Proline transport and stress tolerance of ammonia-insensitive mutants of the PUT4-encoded proline-specific permease in yeast

Journal of General and Applied Microbiology

Volumn 55, Issue 6, 2009, Pages 427-439

  Poole, Kate ^a,c   Walker, Michelle E ^a   Warren, Tristan ^a   Gardner, Jennie ^a   McBryde, Colin ^a   Lopes, Miguel De Barros ^b,d   Jiranek, Vladimir ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b AUSTRALIAN WINE RESEARCH INSTITUTE   (Australia)

^c JPK Instruments AG   (Germany)

^d UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

Proline uptake; Proline specific permease; PUT4; Saccharomyces cerevisiae; Site directed mutagenesis; Stress tolerance

Indexed keywords

AMMONIA; ENZYME VARIANT; FUNGAL ENZYME; FUNGAL PROTEIN; HEAT SHOCK PROTEIN; NITROGEN; PERMEASE; PROLINE; PROTEIN PUT4; PROTEIN PUT4P; SERINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO ACID TRANSPORT; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL VIABILITY; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DOWN REGULATION; ENZYME REPRESSION; ENZYME SPECIFICITY; GENE MUTATION; HEAT STRESS; NONHUMAN; OSMOTIC STRESS; PROMOTER REGION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SITE DIRECTED MUTAGENESIS; YEAST; YEAST CELL;

AMINO ACID TRANSPORT SYSTEMS, NEUTRAL; AMMONIA; GENE EXPRESSION REGULATION, FUNGAL; HEAT-SHOCK RESPONSE; INDUSTRIAL MICROBIOLOGY; MUTAGENESIS, SITE-DIRECTED; MUTATION; NITROGEN; OSMOTIC PRESSURE; PROLINE; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

EID: 76149094527     PISSN: 00221260     EISSN: 13498037     Source Type: Journal    
DOI: 10.2323/jgam.55.427     Document Type: Article

References (57)

1. Adams, A., Gottschling, D. E., Kaiser, C. A., and Stearns, T. (1997) Methods in Yeast Genetics, Cold Spring Harbor Press, Cold Spring Harbor, New York.
2. Andréasson, C., Neve, E. P. A., and Ljungdah, P. O. (2004) Four permeases import proline and the toxic proline analogue azetidine-2-carboxylate into yeast. Yeast, 21, 193-199.
3. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K. (1994) Current Protocols in Molecular Biology, John Wiley and Sons, Inc., New York.
4. Bely, M., Sablayrolles, J. M., and Barre, P. (1990) Automatic detection of assimilable nitrogen deficiencies during alcoholic fermentation in oenological conditions. J. Ferm. Bioeng., 70, 246-252.
5. Blom, N., Gammeltoft, S., and Brunak, S. (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol., 294, 1351-1362.
6. Bonneaud, N., Ozier-Kalogeropoulos, O., Li, G., Labouesse, M., Minvielle-Sebastia, L., and Lacroute, F. (1991) A family of low and high copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors. Yeast, 7, 609-615.
7. Chen, C. and Dickman, M. B. (2005) Proline suppresses apoptosis in the fungal pathogen of Colletotrichum trifolii. Proc. Natl. Acad. Sci. USA, 102, 3459-3464.
8. Courchesne, W. E. and Magasanik, B. (1988) Regulation of nitrogen assimilation in Saccharomyces cerevisiae: Roles of the URE2 and GLN3 genes. J. Bacteriol., 170, 708-711.
9. Csonka, L. N. (1981) Proline over-production results in enhanced osmotolerance in Salmonella typhimurium. Mol. Gen. Genet., 182, 82-86.
10. De Craene, J. O., Soetens, O., and André, B. (2001) The Npr1 kinase controls biosynthetic and endocytic sorting of the yeast Gap1 permease. J. Biol. Chem., 276, 43939-43948.
11. Delauney, A. J. and Verma, D. P. S. (1993) Proline biosynthesis and osmoregulation in plants. Plant J., 4, 215-223.
12. Galan, J. M., Moreau, V., André, B., Volland, C., and Haguenauer-Tsapis, R. (1996) Ubiquitination mediated by the Npi1p/ Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J. Biol. Chem., 271, 10946-10952.
13. Giesler, C., Dietrich, J., Nielsen, B., Kastrup, J., Lauritsen, J. P., Odum, N., and Christensen, M. D. (1998) Leucine-based receptor sorting motifs are dependent on the spacing relative to the plasma membrane. J. Biol. Chem., 273, 21316-21323.
14. Gietz, R. S., St. Jean, A., Woods, R. A., and Schiestl, R. H. (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res., 20, 1425.
15. Grenson, M. (1983) Inactivation-reactivation process and repression of permease formation regulate several ammonia-sensitive permeases in the yeast Saccharomyces cerevisiae. Eur. J. Biochem., 133, 135-139.
16. Guthrie, C. and Fink, G. R. (1991) Guide to yeast genetics and molecular biology. Methods Enzymol., 194, 182-187.
17. +-induced inactivation and degradation of the general amino acid permease, Gap1p, of Saccharomyces cerevisiae. Mol. Microbiol., 24, 607-616.
18. Henschke, P. A. and Jiranek, V. (1993) Yeast-metabolism of nitrogen compounds. In Wine Microbiology and Biotechnology, ed. by Fleet, G. H., Harwood Academic Publishers, Newark, NJ, pp. 77-164.
19. Hicke, L. and Riezman, H. (1996) Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell, 84, 277-287.
20. Horak, J. and Rihova, L. (1982) L-Proline transport in Saccharomyces cerevisiae. Biochim. Biophys. Acta, 691, 144-150.
21. Ingledew, W. M., Magnus, C. A., and Sosulski, R. W. (1987) In-fluence of oxygen on proline utilization during the wine fermentation. Am. J. Enol. Vitic., 38, 246-248.
22. Iraqui, I., Vissers, S., Bernard, F., de Craene, J.-O., Boles, E., Urrestarazu, A., and André, B. (1999) Amino acid signaling in Saccharomyces cerevisiae: A permease-like sensor of external amino acids and F-box protein Grr1p are required for transcriptional induction of the AGP1 gene, which encodes a broad-specificity amino acid permease. Mol. Cell. Biol., 19, 989-1001.
23. Jauniaux, J. C., Vandenbol, M., Vissers, S., Broman, K., and Grenson, M. (1987) Nitrogen catabolite regulation of proline permease in Saccharomyces cerevisiae. Cloning of the PUT4 gene and study of PUT4 RNA levels in wild-type and mutant strains. Eur. J. Biochem., 164, 601-606.
24. Krzywicki, K. A. and Brandriss, M. C. (1984) Primary structure of the nuclear PUT2 gene involved in the mitochondrial pathway for proline utilization in Saccharomyces cerevisiae. Mol. Cell. Biol., 4, 2837-2842.
25. Lasko, P. F. and Brandriss, M. C. (1981) Proline transport in Saccharomyces cerevisiae. J. Bacteriol., 148, 241-247.
26. Le Rudulier, D., Strom, A. R., Dandekar, A. M., Smith, L. T., and Valentine, R. C. (1984) Molecular biology of osmoregulation. Science, 224, 1064-1068.
27. Ma, H., Kunes, S., Schatz, P. J., and Botstein, D. (1987) Plasmid construction by homologous recombination in yeast. Gene, 58, 201-216.
28. Magana-Schwencke, N. and Schwencke, J. (1969) A proline transport system in Saccharomyces chevalieri. Biochim. Biophys. Acta, 173, 313-323.
29. Maniatis, T., Fritsch, E. F. and Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Press, Cold Spring Harbor, New York.
30. Martin, O., Brandriss, M. C., Schneider, G., and Bakalinsky, A. T. (2003) Improved anaerobic use of arginine by Saccharomyces cerevisiae. Appl. Environ. Microbiol., 69, 1623-1628.
31. Morita, Y., Nakamori, S., and Takagi, H. (2002) Effect of proline and arginine metabolism on freezing stress of Saccharomyces cerevisiae. J. Biosci. Bioeng., 94, 390-394.
32. Mumberg, D., Mueller, R., and Funk, M. (1995) Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene, 156, 119-122.
33. Omura, F., Fujita, A., Miyajima, K., and Fukui, N. (2005) Engineering of yeast Put4 permease and its application to lager yeast for efficient proline assimilation. Biosci. Biotech. Biochem., 69, 1162-1171.
34. Omura, F., Kodama, Y., and Ashikari, T. (2001) The N-terminal domain of the yeast permease Bap2p plays a role in its degradation. Biochem. Biophys. Res. Commun., 287, 1045-1050.
35. Ough, C. S. and Amerine, M. A. (1988) Methods for Analysis of Musts and Wines, Wiley Interscience, New York. Ough, C. S. and Stashak, R. M. (1974) Further studies on proline concentration in grapes and wines. Am. J. Enol. Vitic., 25, 8-12.
36. Piruat, J. I., Chavez, S., and Aguilera, A. (1997) The yeast HRS1 gene is involved in positive and negative regulation of transcription and shows genetic characteristics similar to SIN4 and GAL1. Genetics 147, 1585-1594.
37. Poole, K. (2002) Enhancing Yeast Performance under Oenological Conditions by Enabling Proline Utilisation, Department of Horticulture, Viticulture and Oenology, University of Adelaide, Adelaide.
38. Regenberg, B., During-Olsen, L., Kielland-Brandt, M. C., and Holmberg, S. (1999) Substrate specificity and gene expression of the amino-acid permeases in Saccharomyces cerevisiae. Curr. Genet., 36, 317-328.
39. Roberg, K. J., Rowley, N., and Kaiser, C. A. (1997) Physiological regulation of membrane protein sorting late in the secretory pathway of Saccharomyces cerevisiae. J. Cell Biol., 137, 1469-1482.
40. Rousselet, G., Simon, M., Ripoche, P., and Buhler, J. M. (1995) A second nitrogen permease regulator in Saccharomyces cerevisiae. FEBS Lett., 359, 215-219.
41. Schmitt, M. E., Brown, T. A., and Trumpower, B. L. (1990) A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res., 18, 3091-3092.
42. Schreve, J. L., Sin, J. K., and Garrett, J. M. (1998) The Saccharomyces cerevisiae YCC5 (YCL025c) gene encodes an amino acid permease, Agp1, which transports asparagine and glutamine. J. Bacteriol., 180, 2556-2559.
43. Sherman, F. (1991) Getting Started with Yeast, Academic Press, Inc., San Diego, Ca.
44. Soetens, O., De Craene, J. O., and André, B. (2001) Ubiquitin is required for sorting to the vacuole of the yeast general amino acid permease, Gap1. J. Biol. Chem., 276, 43949-43957.
45. Springael, J. Y. and André, B. (1998) Nitrogen-regulated ubiquitination of the Gap1 permease of Saccharomyces cerevisiae. Mol. Cell. Biol., 9, 1253-1263.
46. Springael, J. Y., De Craene, J. O., and André, B. (1999a) The yeast Npi1/Rsp5 ubiquitin ligase lacking its N-terminal C2 domain is competent for ubiquitination but not for subsequent endocytosis of the Gap1 permease. Biochem. Biophys. Res. Commun., 257, 561-566.
47. +-induced down-regulation of the Saccharomyces cerevisiae Gap1p permease involves its ubiquitination with lysine-63-linked chains. J. Cell Sci., 112, 1375-1383.
48. Stanbrough, M. and Magasanik, B. (1995) Transcriptional and posttranslational regulation of the general amino acid permease of Saccharomyces cerevisiae. J. Bacteriol., 177, 94-102.
49. Stark, M. J. R. (1998) Studying Posttranslational Modifications in Yeast: Intracellular Proteins, Academic Press, Ltd., San Diego.
50. Takagi, H., Sakai, K., Morida, K., and Nakamori, S. (2000) Proline accumulation by mutation or disruption of the proline oxidase gene improves resistance to freezing and desiccation stresses in Saccharomyces cerevisiae. FEBS Lett., 184, 103-108.
51. Terao, Y., Nakamori, S., and Takagi, H. (2003) Gene dosage effect of L-proline biosynthetic enzymes on L-proline accumulation and freeze tolerance in Saccharomyces cerevisiae. Appl. Environ. Microbiol., 69, 6527-6532.
52. Van Miltenburg, R., Ruger, B., Grunewald-Janho, S., Leons, M., and Schroder, C. (1995) The DIG System User's Guide for Filter Hybridisation, 1995 ed., Biochemica, Boehringer Mannheim GmbH.
53. Wach, A., Brachat, A., Pohlmann, R., and Philippsen, P. (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast, 10, 1793-1808.
54. Walker, M. E., Gardner, J. M., Vystavelova, A., McBryde, C., de Barros Lopes, M., and Jiranek, V. (2003) Application of the reuseable, kanMX selectable marker to industrial yeast: Construction and evaluation of heterothallic wine strains of Saccharomyces cerevisiae, possessing minimal foreign DNA sequences. FEMS Yeast Res., 4, 339-347.
55. Wang, S.-S. and Brandriss, M. C. (1987) Proline utilization in Saccharomyces cerevisiae: Sequence, regulation, and mitochondrial localization of the PUT1 gene product. Mol. Cell. Biol., 7, 4431-4440.
56. Wiederkehr, A., Avaro, S., Presianotto-Baschong, C., Haguenauer-Tsapis, R., and Riezman, H. (2000) The F-box protein Rcy1p is involved in endocytic membrane traffic and recycling out of an early endosome in Saccharomyces cerevisiae. J. Cell Biol., 149, 397-410.
57. Xu, S., Falvey, D. A., and Brandriss, M. C. (1995) Roles of URE2 and GLN3 in the proline utilization pathway in Saccharomyces cerevisiae. J. Bacteriol., 130, 714-723.