Cellular processes and pathways that protect Saccharomyces cerevisiae cells against the plasma membrane-perturbing compound chitosan

Eukaryotic Cell

Volumn 6, Issue 4, 2007, Pages 600-608

  Zakrzewska, Anna ^a   Boorsma, Andre ^a   Delneri, Daniela ^b   Brul, Stanley ^a   Oliver, Stephen G ^b   Klis, Frans M ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHITOSAN; GLYCEROL; LIPID; OLIGOSACCHARIDE; SACCHAROMYCES CEREVISIAE PROTEIN; SORBITOL;

ARTICLE; BIOLOGICAL MODEL; CELL MEMBRANE; CYTOLOGY; DRUG EFFECT; FUNGAL GENE; GENE DELETION; GLYCOSYLATION; HOMOZYGOTE; METABOLISM; MICROBIOLOGICAL EXAMINATION; SACCHAROMYCES CEREVISIAE;

CELL MEMBRANE; CHITOSAN; GENE DELETION; GENES, FUNGAL; GLYCEROL; GLYCOSYLATION; HOMOZYGOTE; LIPIDS; MICROBIAL SENSITIVITY TESTS; MODELS, BIOLOGICAL; OLIGOSACCHARIDES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SORBITOL;

SACCHAROMYCES CEREVISIAE;

EID: 34247885929     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00355-06     Document Type: Article

References (64)

1. Alonso-Monge, R., E. Real, I. Wojda, J. P. Bebelman, W. H. Mager, and M. Siderius. 2001. Hyperosmotic stress response and regulation of cell wall integrity in Saccharomyces cerevisiae share common functional aspects. Mol. Microbiol. 41:717-730.
2. Ashburner, M., C. A. Ball, J. A. Blake, D. Botstein, H. Butler, J. M. Cherry, A. P. Davis, K. Dolinski, S. S. Dwight, J. T. Eppig, M. A. Harris, D. P. Hill, L. Issel-Tarver, A. Kasarskis, S. Lewis, J. C. Matese, J. E. Richardson, M. Ringwald, G. M. Rubin, G. Sherlock, et al. 2000. Gene ontology: tool for the unification of biology. Nat. Genet. 25:25-29.
3. Basmaji, F., H. Martin-Yken, F. Durand, A. Dagkessamanskaia, C. Pichereaux, M. Rossignol, and J. Francois. 2006. The 'interactome' of the Knr4/Smi1, a protein implicated in coordinating cell wall synthesis with bud emergence in Saccharomyces cerevisiae. Mol. Genet. Genomics 275:217-230.
4. Birrell, G. W., J. A. Brown, H. I. Wu, G. Giaever, A. M. Chu, R. W. Davis, and J. M. Brown. 2002. Transcriptional response of Saccharomyces cerevisiae to DNA-damaging agents does not identify the genes that protect against these agents. Proc. Natl. Acad. Sci. USA 99:8778-8783.
5. Boorsma, A., B. C. Foat, D. Vis, F. Klis, and H. J. Bussemaker. 2005. T-profiler: scoring the activity of predefined groups of genes using gene expression data. Nucleic Acids Res. 33:W592-W595.
6. Brown, J. A., G. Sherlock, C. L. Myers, N. M. Burrows, C. Deng, H. I. Wu, K. E. McCann, O. G. Troyanskaya, and J. M. Brown. 2006. Global analysis of gene function in yeast by quantitative phenotypic profiling. Mol. Syst. Biol. 2:2006 0001.
7. Burda, P., and M. Aebi. 1999. The dolichol pathway of N-linked glycosylation. Biochim. Biophys. Acta 1426:239-257.
8. Castrillo, J. I., L. A. Zeef, D. C. Hoyle, N. Zhang, A. Hayes, D. C. J. Gardner, M. J. Cornell, J. Petty, L. Hakes, L. Wardleworth, B. Rash, M. Brown, W. B. Dunn, D. Broadhurst, K. O'Donoghue, S. S. Hester, T. P. J. Dunkley, S. R. Hart, S. J. Gaskell, N. W. Paton, K. S. Lilley, D. B. Kell, and S. G. Oliver. Growth control of the eukaryote cell: a systems biology study in yeast. J. Biol., in press.
9. Chang, M., D. French-Cornay, H. Y. Fan, H. Klein, C. L. Denis, and J. A. Jaehning. 1999. A complex containing RNA polymerase II, Paf1p, Cdc73p, Hpr1p, and Ccr4p plays a role in protein kinase C signaling. Mol. Cell. Biol. 19:1056-1067.
10. Chowdhury, S., K. W. Smith, and M. C. Gustin. 1992. Osmotic stress and the yeast cytoskeleton: phenotype-specific suppression of an actin mutation. J. Cell Biol. 118:561-571.
11. Cruz, M. C., A. L. Goldstein, J. R. Blankenship, M. Del Poeta, D. Davis, M. E. Cardenas, J. R. Perfect, J. H. McCusker, and J. Heitman. 2002. Calcineurin is essential for survival during membrane stress in Candida albicans. EMBO J. 21:546-559.
12. Delley, P. A., and M. N. Hall. 1999. Cell wall stress depolarizes cell growth via hyperactivation of RHO1. J. Cell Biol. 147:163-174.
13. DeMarini, D. J., A. E. Adams, H. Fares, C. De Virgilio, G. Valle, J. S. Chuang, and J. R. Pringle. 1997. A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall. J. Cell Biol. 139:75-93.
14. De Nobel, J. G., F. M. Klis, T. Munnik, J. Priem, and H. van den Ende. 1990. An assay of relative cell wall porosity in Saccharomyces cerevisiae, Kluyveromyces lactis and Schizosaccharomyces pombe. Yeast 6:483-490.
15. Dwight, S. S., M. A. Harris, K. Dolinski, C. A. Ball, G. Binkley, K. R. Christie, D. G. Fisk, L. Issel-Tarver, M. Schroeder, G. Sherlock, A. Sethuraman, S. Weng, D. Botstein, and J. M. Cherry. 2002. Saccharomyces Genome Database (SGD) provides secondary gene annotation using the Gene Ontology (GO). Nucleic Acids Res. 30:69-72.
16. Engqvist-Goldstein, A. E., and D. G. Drubin. 2003. Actin assembly and endocytosis: from yeast to mammals. Annu. Rev. Cell Dev. Biol. 19:287-332.
17. Fuchs, S. M., and R. T. Raines. 2006. Internalization of cationic peptides: the road less (or more?) traveled. Cell. Mol. Life Sci. 63:1819-1822.
18. García-Rodriguez, L. J., A. Durán, and C. Roncero. 2000. Calcofluor antifungal action depends on chitin and a functional high-osmolarity glycerol response (HOG) pathway: evidence for a physiological role of the Saccharomyces cerevisiae HOG pathway under noninducing conditions. J. Bacteriol. 182:2428-2437.
19. Gasch, A. P., and M. Werner-Washburne. 2002. The genomics of yeast responses to environmental stress and starvation. Funct. Integr. Genomics 2:181-192.
20. Giaever, G. 2003. A chemical genomics approach to understanding drug action. Trends Pharmacol. Sci. 24:444-446.
21. Giaever, G., A. M. Chu, L. Ni, C. Connelly, L. Riles, S. Veronneau, S. Dow, A. Lucau-Danila, K. Anderson, B. Andre, A. P. Arkin, A. Astromoff, M. El-Bakkoury, R. Bangham, R. Benito, S. Brachat, S. Campanaro, M. Curtiss, K. Davis, A. Deutschbauer, K. D. Entian, P. Flaherty, F. Foury, D. J. Gartinkel, M. Gerstein, D. Gotte, U. Guldener, J. H. Hegemann, S. Hempel, Z. Herman, D. F. Jaramillo, D. E. Kelly, S. L. Kelly, P. Kotter, D. LaBonte, D. C. Lamb, N. Lan, H. Liang, H. Liao, L. Liu, C. Luo, M. Lussier, R. Mao, P. Menard, S. L. Ooi, J. L. Revuelta, C. J. Roberts, M. Rose, P. Ross-Macdonald, B. Scherens, G. Schimmack, B. Shafer, D. D. Shoemaker, S. Sookhai-Mahadeo, R. K. Storms, J. N. Strathern, G. Valle, M. Voet, G. Volckaert, C. Y. Wang, T. R. Ward, J. Wilhelmy, E. A. Winzeler, Y. Yang, G. Yen, E. Youngman, K. Yu, H. Bussey, J. D. Boeke, M. Snyder, P. Philippsen, R. W. Davis, and M. Johnston. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387-391.
22. Giaever, G., P. Flaherty, J. Kumm, M. Proctor, C. Nislow, D. F. Jaramillo, A. M. Chu, M. I. Jordan, A. P. Arkin, and R. W. Davis. 2004. Chemogenomic profiling: identifying the functional interactions of small molecules in yeast. Proc. Natl. Acad. Sci. USA 101:793-798.
23. Giaever, G., D. D. Shoemaker, T. W. Jones, H. Liang, E. A. Winzeler, A. Astromoff, and R. W. Davis. 1999. Genomic profiling of drug sensitivities via induced haploinsufficiency. Nat. Genet. 21:278-283.
24. Guaitieri, T., E. Ragni, L. Mizzi, U. Fascio, and L. Popolo. 2004. The cell wall sensor Wsc1p is involved in reorganization of actin cytoskeleton in response to hypo-osmotic shock in Saccharomyces cerevisiae. Yeast 21:1107-1120.
25. Harbison, C. T., D. B. Gordon, T. I. Lee, N. J. Rinaldi, K. D. Macisaac, T. W. Danford, N. M. Hannett, J. B. Tagne, D. B. Reynolds, J. Yoo, E. G. Jennings, J. Zeitlinger, D. K. Pokholok, M. Kellis, P. A. Rolfe, K. T. Takusagawa, E. S. Lander, D. K. Gifford, E. Fraenkel, and R. A. Young. 2004. Transcriptional regulatory code of a eukaryotic genome. Nature 431:99-104.
26. Hayashi, M., and T. Maeda. 2006. Activation of the HOG pathway upon cold stress in Saccharomyces cerevisiae. J. Biochem. (Tokyo) 139:797-803.
27. Hong, E. L., R. Balakrishnan, K. R. Christie, M. C. Costanzo, S. S. Dwight, S. R. Engel, D. G. Fisk, J. E. Hirschman, M. S. Livstone, R. Nash, R. Oughtred, J. Park, M. Skrzypek, B. Starr, C. L. Theesfeld, R. Andrada, G. Binkley, Q. Dong, C. D. Lane, B. C. Hitz, S. Miyasato, M. Schroeder, S. Weng, E. D. Wong, K. Dolinski, D. Botstein, and J. M. Cherry. 8 November 2006, accession date. Saccharomyces Genome Database. http://www.yeastgenome.org/.
28. Huckaba, T. M., A. C. Gay, L. F. Pantalena, H. C. Yang, and L. A. Pon. 2004. Live cell imaging of the assembly, disassembly, and actin cable-dependent movement of endosomes and actin patches in the budding yeast, Saccharomyces cerevisiae. J. Cell Biol. 167:519-530.
29. Jung, U. S., and D. E. Levin. 1999. Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signalling pathway. Mol. Microbiol. 34:1049-1057.
30. Kamada, Y., U. S. Jung, J. Piotrowski, and D. E. Levin. 1995. The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response. Genes Dev. 9:1559-1571.
31. Kapteyn, J. C., A. F. Ram, E. M. Groos, R. Kollar, R. C. Montijn, H. Van Den Ende, A. Llobell, E. Cabib, and F. M. Klis. 1997. Altered extent of cross-linking of β1,6-glucosylated mannoproteins to chitin in Saccharomyces cerevisiae mutants with reduced cell wall β1,3-glucan content. J. Bacteriol. 179:6279-6284.
32. Kapteyn, J. C., B. ter Riet, E. Vink, S. Blad, H. De Nobel, H. Van Den Ende, and F. M. Klis. 2001. Low external pH induces HOG1-dependent changes in the organization of the Saccharomyces cerevisiae cell wall. Mol. Microbiol. 39:469-479.
33. Lawrence, C. L., C. H. Botting, R. Antrohus, and P. J. Coote. 2004. Evidence of a new role for the high-osmolarity glycerol mitogen-activated protein kinase pathway in yeast: regulating adaptation to citric acid stress. Mol. Cell. Biol. 24:3307-3323.
34. Lee, T. I., N. J. Rinaldi, F. Robert, D. T. Odom, Z. Bar-Joseph, G. K. Gerber, N. M. Hannett, C. T. Harbison, C. M. Thompson, I. Simon, J. Zeitlinger, E. G. Jennings, H. L. Murray, D. B. Gordon, B. Ren, J. J. Wyrick, J. B. Tagne, T. L. Volkert, E. Fraenkel, D. K. Gifford, and R. A. Young. 2002. Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298:799-804.
35. Lever, M., J. C. Powell, M. Killip, and C. W. Small. 1973. A comparison of 4-hydroxybenzoic acid hydrazide (PAHBAH) with other reagents for the determination of glucose. J. Lab. Clin. Med. 82:649-655.
36. Levin, D. E. 2005. Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69:262-291.
37. Liu, H., Y. Du, X. Wang, and L. Sun. 2004. Chitosan kills bacteria through cell membrane damage. Int. J. Food Microbiol. 95:147-155.
38. Lum, P. Y., C. D. Armour, S. B. Stepaniants, G. Cavet, M. K. Wolf, J. S. Butler, J. C. Hinshaw, P. Garnier, G. D. Prestwich, A. Leonardson, P. Garrett-Engele, C. M. Rush, M. Bard, G. Schimmack, J. W. Phillips, C. J. Roberts, and D. D. Shoemaker. 2004. Discovering modes of action for therapeutic compounds using a genome-wide screen of yeast heterozygotes. Cell 116:121-137.
39. Mendizabal, I., G. Rios, J. M. Mulet, R. Serrano, and I. K. de Larrinoa. 1998. Yeast putative transcription factors involved in salt tolerance. FEBS Lett. 425:323-328.
40. Mollapour, M., and P. W. Piper. 2006. Hog1p mitogen-activated protein kinase determines acetic acid resistance in Saccharomyces cerevisiae. FEMS Yeast Res. 6:1274-1280.
41. Ngimhuang, J., F. J. Satoh, T. Furuike, and N. Sakairi. 2004. Synthesis of a novel polymeric surfactant by reductive N-alkylation of chitosan with 3-O-dodecyl-D-glucose. Polymer 45:837-841.
42. Panadero, J., C. Pallotti, S. Rodriguez-Vargas, F. Randez-Gil, and J. A. Prieto. 2006. A downshift in temperature activates the high osmolarity glycerol (HOG) pathway, which determines freeze tolerance in Saccharomyces cerevisiae. J. Biol. Chem. 281:4638-4645.
43. Parsons, A. B., R. L. Brost, H. Ding, Z. Li, C. Zhang, B. Sheikh, G. W. Brown, P. M. Kane, T. R. Hughes, and C. Bonne. 2004. Integration of chemical-genetic and genetic interaction data links bioactive compounds to cellular target pathways. Nat. Biotechnol. 22:62-69.
44. Parsons, A. B., A. Lopez, I. E. Givoni, D. E. Williams, C. A. Gray, J. Porter, G. Chua, R. Sopko, R. L. Brost, C. H. Ho, J. Wang, T. Ketela, C. Brenner, J. A. Brill, G. E. Fernandez, T. C. Lorenz, G. S. Payne, S. Ishihara, Y. Ohya, B. Andrews, T. R. Hughes, B. J. Frey, T. R. Graham, R. J. Andersen, and C. Boone. 2006. Exploring the mode-of-action of bioactive compounds by chemical-genetic profiling in yeast. Cell 126:611-625.
45. Rabea, E. I., M. E. Badawy, C. V. Stevens, G. Smagghe, and W. Steurbaut. 2003. Chitosan as antimicrobial agent: applications and mode of action. Biomacromolecules 4:1457-1465.
46. Rhoades, J., and S. Roller. 2000. Antimicrobial actions of degraded and native chitosan against spoilage organisms in laboratory media and foods. Appl. Environ. Microbiol. 66:80-86.
47. Riederer, M. A., and A. Hinnen. 1991. Removal of N-glycosylation sites of the yeast acid phosphatase severely affects protein folding. J. Bacteriol. 173:3539-3546.
48. Roller, S., and N. Covill. 1999. The antifungal properties of chitosan in laboratory media and apple juice. Int. J. Food Microbiol. 47:67-77.
49. Santos, M., and I. F. de Larrinoa. 2005. Functional characterization of the Candida albicans CRZ1 gene encoding a calcineurin-regulated transcription factor. Curr. Genet. 48:88-100.
50. Storm, D. R., K. S. Rosenthal, and P. E. Swanson. 1977. Polymyxin and related peptide antibiotics. Annu. Rev. Biochem. 46:723-763.
51. Thevissen, K., I. E. Francois, J. Y. Takemoto, K. K. Ferket, E. M. Meert, and B. P. Cammue. 2003. DmAMP1, an antifungal plant defensin from dahlia (Dahlia merckii), interacts with sphingolipids from Saccharomyces cerevisiae. FEMS Microbiol. Lett. 226:169-173.
52. Thevissen, K., F. R. Terras, and W. F. Broekaert. 1999. Permeabilization of fungal membranes by plant defensins inhibits fungal growth. Appl. Environ. Microbiol. 65:5451-5458.
53. Thevissen, K., D. C. Warnecke, I. E. Francois, M. Leipelt, E. Heinz, C. Ott, U. Zahringer, B. P. Thomma, K. K. Ferket, and B. P. Cammue. 2004. Defensins from insects and plants interact with fungal glucosylceramides. J. Biol. Chem. 279:3900-3905.
54. Tong, A. H., M. Evangelista, A. B. Parsons, H. Xu, G. D. Batler, N. Page, M. Robinson, S. Raghibizadeh, C. W. Hogue, H. Bussey, B. Andrews, M. Tyers, and C. Boone. 2001. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294:2364-2368.
55. Tong, A. H., G. Lesage, G. D. Bader, H. Ding, H. Xu, X. Xin, J. Young, G. F. Berriz, R. L. Brost, M. Chang, Y. Chen, X. Cheng, G. Chua, H. Friesen, D. S. Goldberg, J. Haynes, C. Humphries, G. He, S. Hussein, L. Ke, N. Krogan, Z. Li, J. N. Levinson, H. Lu, P. Menard, C. Munyana, A. B. Parsons, O. Ryan, R. Tonikian, T. Roberts, A. M. Sdicu, J. Shapiro, B. Sheikh, B. Suter, S. L. Wong, L. V. Zhang, H. Zhu, C. G. Burd, S. Munro, C. Sander, J. Rine, J. Greenblatt, M. Peter, A. Bretscher, G. Bell, F. P. Roth, G. W. Brown, B. Andrews, H. Bussey, and C. Boone. 2004. Global mapping of the yeast genetic interaction network. Science 303:808-813.
56. van der Lubben, I. M., J. C. Verhoef, G. Borehard, and H. E. Junginger. 2001. Chitosan and its derivatives in mucosal drug and vaccine delivery. Eur. J. Pharm. Sci. 14:201-207.
57. Walther, T. C., J. H. Brickner, P. S. Aguilar, S. Bernales, C. Pantoja, and P. Walter. 2006. Eisosomes mark static sites of endocytosis. Nature 439:998-1003.
58. Warringer, J., E. Ericson, L. Fernandez, O. Nerman, and A. Blomberg. 2003. High-resolution yeast phenomics resolves different physiological features in the saline response. Proc. Natl. Acad. Sci. USA 100:15724-15729.
59. Watanabe, M., C. Y. Chen, and D. E. Levin. 1994. Saccharomyces cerevisiae PKC1 encodes a protein kinase C (PKC) homolog with a substrate specificity similar to that of mammalian PKC. J. Biol. Chem. 269:16829-16836.
60. Wu, H. I., J. A. Brown, M. J. Dorie, L. Lazzeroni, and J. M. Brown. 2004. Genome-wide identification of genes conferring resistance to the anticancer agents cisplatin, oxaliplatin, and mitomycin C. Cancer Res. 64:3940-3948.
61. Yang, F., X. Cui, and X. Yang. 2002. Interaction of low-molecular-weight chitosan with mimic membrane studied by electrochemical methods and surface plasmon resonance. Biophys. Chem. 99:99-106.
62. Yoshida, S., E. Ikeda, I. Uno, and H. Mitsuzawa. 1992. Characterization of a staurosporine- and temperature-sensitive mutant, stt1, of Saccharomyces cerevisiae: STT1 is allelic to PKC1. Mol. Gen. Genet. 231:337-344.
63. Zakrzewska, A., A. Boorsma, S. Brul, K. J. Hellingwerf, and F. M. Klis. 2005. Transcriptional response of Saccharomyces cerevisiae to the plasma membrane-perturbing compound chitosan. Eukaryot. Cell 4:703-715.
64. Zewail, A., M. W. Xie, Y. Xing, L. Lin, P. F. Zhang, W. Zou, J. P. Saxe, and J. Huang. 2003. Novel functions of the phosphatidylinositol metabolic pathway discovered by a chemical genomics screen with wortmannin. Proc. Natl. Acad. Sci. USA 100:3345-3350.