Identification of yeast genes that confer resistance to chitosan oligosaccharide (COS) using chemogenomics

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Jaime, Maria D L A ^a   Lopez Llorca, Luis V ^b   Conesa, Ana ^c   Lee, Anna Y ^d   Proctor, Michael ^e   Heisler, Lawrence E ^a,d   Gebbia, Marinella ^a,d   Giaever, Guri ^a,d   Westwood, J T ^a   Nislow, Corey ^a,d  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF ALICANTE   (Spain)

^c Prince Felipe Research Centre   (Spain)

^d UNIVERSITY OF TORONTO   (Canada)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antifungal resistance; ARL1; Chemogenomics; Chitosan oligosaccharide; Haploinsufficiency profiling (HIP); Homozygous profiling (HOP); Multi copy suppression profiling (MSP); Saccharomyces cerevisiae; Stress response; Transcriptional analysis

Indexed keywords

AMPHOTERICIN B; CHITOSAN; CHITOSAN DERIVATIVE; CHITOSAN OLIGOSACCHARIDE; DODECYL SULFATE SODIUM; FLUCONAZOLE; HYDROGEN PEROXIDE; HYGROMYCIN B; LITHIUM CHLORIDE; PROTEASOME; RAS PROTEIN; SODIUM CHLORIDE; SORBITOL; TERBINAFINE; UNCLASSIFIED DRUG;

ANTIFUNGAL ACTIVITY; ANTIFUNGAL RESISTANCE; ARL1 GENE; ARTICLE; BCK2 GENE; BIOASSAY; CELL CYCLE; CELL DIVISION; CELL MEMBRANE; CELLULAR STRESS RESPONSE; CHEMOGENOMICS; CONTROLLED STUDY; DOWN REGULATION; DRUG EXPOSURE; DRUG SENSITIVITY; DRUG TARGETING; ENVIRONMENTAL STRESS; ERG24 GENE; FUNGAL GENE; FUNGAL STRAIN; GENE DELETION; GENE FUNCTION; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENE REPRESSION; GENETIC PROCEDURES; GENETIC TRANSCRIPTION; GENOMICS; HAPLOINSUFFICIENCY; HOMOZYGOSITY; MEMBRANE STRUCTURE; MEMBRANE TRANSPORT; MSG5 GENE; MULTICOPY SUPPRESSION PROFILING; NONHUMAN; OSMOTIC STRESS; OXIDATIVE STRESS; PROTEIN FOLDING; RBA50 GENE; REGULATORY MECHANISM; RESPIRATORY CHAIN; RNA TRANSCRIPTION; RNA TRANSLATION; SALT STRESS; SIGNAL TRANSDUCTION; TEMPERATURE STRESS; TRANSCRIPTOMICS; UPREGULATION; WILD TYPE;

AMPHOTERICIN B; ANTIFUNGAL AGENTS; CELL MEMBRANE PERMEABILITY; CHITOSAN; DRUG RESISTANCE, FUNGAL; FLUCONAZOLE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; HAPLOINSUFFICIENCY; MONOMERIC GTP-BINDING PROTEINS; NAPHTHALENES; OXIDATIVE STRESS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; VESICULAR TRANSPORT PROTEINS;

FUNGI; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 84862525742     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-267     Document Type: Article

References (76)

1. Kumar M. A review of chitin and chitosan applications. React Funct Polym 2000, 46:1-27.
2. Hayes M, Carney B, Slater J, Bruck W. Mining marine shellfish wastes for bioactive molecules: chitin and chitosan-Part A: extraction methods. Biotechnol J 2008, 3:871-877.
3. Bartnicki-Garcia S. Cell wall chemistry, morphogenesis, and taxonomy of fungi. Annu Rev Microbiol 1968, 22:87-108.
4. Ruiz-Herrera J, Gonzalez-Prieto JM, Ruiz-Medrano R. Evolution and phylogenetic relationships of chitin synthases from yeasts and fungi. FEMS Yeast Res 2002, 1:247-256.
5. Kurita K. Chitin and chitosan: functional biopolymers from marine crustaceans. Mar Biotechnol (NY) 2006, 8:203-226.
6. Kim SK, Rajapakse N. Enzymatic production and biological activities of chitosan oligosaccharides (COS): A review. Carbohyd Polym 2005, 62:357-368.
7. Allan CR, Hadwiger LA. The fungicidal effect of chitosan on fungi of varying cell wall composition. Exp Mycol 1979, 3:285-287.
8. Palma-Guerrero J, Larriba E, Güerri-Agulló B, Jansson H-B, Salinas J, Lopez-Llorca LV. Chitosan increases conidiation in fungal pathogens of invertebrates. Appl Microbiol Biot 2010, 87:2237-2245.
9. Hirano S, Nagao N. Effects of chitosan, pectic acid, lysozyme, and chitinase on the growth of several phytopathogens. Agric Biol Chem 1989, 53:2.
10. El Ghaouth A, Arul J, Asselin A, Benhamou N. Antifungal activity of chitosan on post-harvest pathogens: induction of morphological and cytological alterations in. Mycol Res 1992, 769.
11. Benhamou N, Lafontaine PJ, Nicole M. Induction of systemic resistance to Fusarium crown and root rot in tomato plants by seed treatment with chitosan. Phytopathology 1994, 84:1432-1444.
12. Laflamme P, Benhamou N, Bussieres G, Dessureault M. Differential effect of chitosan on root rot fungal pathogens in forest nurseries. Can J Bot 1999, 77:1460-1468.
13. Hadwiger LA, Beckman JM. Chitosan as a component of pea-Fusarium solani interactions. Plant Physiol 1980, 66:205-211.
14. Plascencia-Jatomea M, Viniegra G, Olayo R, Castillo-Ortega MM, Shirai K. Effect of chitosan and temperature on spore germination of Aspergillus niger. Macromol Biosci 2003, 3:582-586.
15. Reddy MVB, Arul J, Ait-Barka E, Angers P, Richard C, Castaigne F. Effect of chitosan on growth and toxin production by Alternaria alternata f. sp. lycopersici. Biocontrol Sci Techn 1998, 8:33-43.
16. Mellegard H, Strand SP, Christensen BE, Granum PE, Hardy SP. Antibacterial activity of chemically defined chitosans: Influence of molecular weight, degree of acetylation and test organism. Int J Food Microbiol 2011, 148:48-54.
17. Stössel P, Leuba JL. Effect of chitosan, chitin and some aminosugars on growth of various soilborne phytopathogenic fungi. J Phytopathol 1984, 111:82-90.
18. Liu H, Du Y, Wang X, Sun L. Chitosan kills bacteria through cell membrane damage. Int J Food Microbiol 2004, 95:147-155.
19. Liu XF, Guan YL, Yang DZ, Li Z, De Yao K. Antibacterial action of chitosan and carboxymethylated chitosan. J Appl Polym Sci 2001, 79:1324-1335.
20. Tikhonov V, Stepnova E, Babak V, Yamskov I, Palma-Guerrero J, Jansson H, Lopez-Llorca L, Salinas J, Gerasimenko D, Avdienko I, Varlamov V. Bactericidal and antifungal activities of a low molecular weight chitosan and its N-/2(3)-(dodec-2-enyl)succinoyl/-derivatives. Carbohyd Polym 2006, 64:66-72.
21. Helander IM, Nurmiaho-Lassila EL, Ahvenainen R, Rhoades J, Roller S. Chitosan disrupts the barrier properties of the outer membrane of gram-negative bacteria. Int J Food Microbiol 2001, 71:235-244.
22. Zakrzewska A, Boorsma A, Brul S, Hellingwerf KJ, Klis FM. Transcriptional response of Saccharomyces cerevisiae to the plasma membrane-perturbing compound chitosan. Eukaryot Cell 2005, 4:703-715.
23. Zakrzewska A, Boorsma A, Delneri D, Brul S, Oliver SG, Klis FM. Cellular processes and pathways that protect Saccharomyces cerevisiae cells against the plasma membrane-perturbing compound chitosan. Eukaryot Cell 2007, 6:600-608.
24. Ericson E, Hoon S, St Onge RP, Giaever G, Nislow C. Exploring gene function and drug action using chemogenomic dosage assays. Methods Enzymol 2010, 470:233-255.
25. Hoon S, Smith AM, Wallace IM, Suresh S, Miranda M, Fung E, Proctor M, Shokat KM, Zhang C, Davis RW, et al. An integrated platform of genomic assays reveals small-molecule bioactivities. Nat Chem Biol 2008, 4:498-506.
26. Giaever G, Flaherty P, Kumm J, Proctor M, Nislow C, Jaramillo DF, Chu AM, Jordan MI, Arkin AP, Davis RW. Chemogenomic profiling: identifying the functional interactions of small molecules in yeast. Proc Natl Acad Sci U S A 2004, 101:793-798.
27. Amor JC, Horton JR, Zhu X, Wang Y, Sullards C, Ringe D, Cheng X, Kahn RA. Structures of yeast ARF2 and ARL1: distinct roles for the N terminus in the structure and function of ARF family GTPases. J Biol Chem 2001, 276:42477-42484.
28. Lee FJ, Huang CF, Yu WL, Buu LM, Lin CY, Huang MC, Moss J, Vaughan M. Characterization of an ADP-ribosylation factor-like 1 protein in Saccharomyces cerevisiae. J Biol Chem 1997, 272:30998-31005.
29. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 2005, 102:15545-15550.
30. Magtanong L, Ho CH, Barker SL, Jiao W, Baryshnikova A, Bahr S, Smith AM, Heisler LE, Choy JS, Kuzmin E, et al. Dosage suppression genetic interaction networks enhance functional wiring diagrams of the cell. Nat Biotechnol 2011, 29:505-511.
31. Martin-Yken H, Dagkessamanskaia A, De Groot P, Ram A, Klis F, Francois J. Saccharomyces cerevisiae YCRO17c/CWH43 encodes a putative sensor/transporter protein upstream of the BCK2 branch of the PKC1-dependent cell wall integrity pathway. Yeast 2001, 18:827-840.
32. Lee KS, Irie K, Gotoh Y, Watanabe Y, Araki H, Nishida E, Matsumoto K, Levin DE. A yeast mitogen-activated protein kinase homolog (Mpk1p) mediates signalling by protein kinase C. Mol Cell Biol 1993, 13:3067-3075.
33. Flandez M, Cosano IC, Nombela C, Martin H, Molina M. Reciprocal regulation between Slt2 MAPK and isoforms of Msg5 dual-specificity protein phosphatase modulates the yeast cell integrity pathway. J Biol Chem 2004, 279:11027-11034.
34. Nordle AK, Rios P, Gaulton A, Pulido R, Attwood TK, Tabernero L. Functional assignment of MAPK phosphatase domains. Proteins 2007, 69:19-31.
35. Medina I, Carbonell J, Pulido L, Madeira SC, Goetz S, Conesa A, Tárraga J, Pascual-Montano A, Nogales-Cadenas R, Santoyo J, et al. Babelomics: an integrative platform for the analysis of transcriptomics, proteomics and genomic data with advanced functional profiling. Nucleic Acids Res 2010, 38:W210-W213.
36. Al-Shahrour F, Carbonell J, Minguez P, Goetz S, Conesa A, Tárraga J, Medina I, Alloza E, Montaner D, Dopazo J. Babelomics: advanced functional profiling of transcriptomics, proteomics and genomics experiments. Nucleic Acids Res 2008, 36:W341-W346.
37. Thevissen K, Terras FR, Broekaert WF. Permeabilization of fungal membranes by plant defensins inhibits fungal growth. Appl Environ Microbiol 1999, 65:5451-5458.
38. Berry DB, Gasch AP. Stress-activated genomic expression changes serve a preparative role for impending stress in yeast. Mol Biol Cell 2008, 19:4580-4587.
39. Roberts CJ, Nelson B, Marton MJ, Stoughton R, Meyer MR, Bennett HA, He YD, Dai H, Walker WL, Hughes TR, et al. Signaling and circuitry of multiple MAPK pathways revealed by a matrix of global gene expression profiles. Science 2000, 287:873-880.
40. Ostrosky-Zeichner L, Casadevall A, Galgiani JN, Odds FC, Rex JH. An insight into the antifungal pipeline: selected new molecules and beyond. Nat Rev Drug Discov 2010, 9:719-727.
41. Kong M, Chen XG, Xing K, Park HJ. Antimicrobial properties of chitosan and mode of action: A state of the art review. Int J Food Microbiol 2010, 144:51-63.
42. Xia W, Liu P, Zhang J, Chen J. Biological activities of chitosan and chitooligosaccharides. Food Hydrocolloids 2011, 25:170-179.
43. Pierce SE, Davis RW, Nislow C, Giaever G. Genome-wide analysis of barcoded Saccharomyces cerevisiae gene-deletion mutants in pooled cultures. Nat Protoc 2007, 2:2958-2974.
44. Munson AM, Haydon DH, Love SL, Fell GL, Palanivel VR, Rosenwald AG. Yeast ARL1 encodes a regulator of K + influx. J Cell Sci 2004, 117:2309-2320.
45. Munro S. The Arf-like GTPase Arl1 and its role in membrane traffic. Biochem Soc Trans 2005, 33:601-605.
46. Marešová L, Sychrová H. Genetic interactions among the Arl1 GTPase and intracellular Na(+)/H(+) antiporters in pH homeostasis and cation detoxification. FEMS Yeast Res 2010, 10:802-811.
47. Rosenwald AG, Rhodes MA, Van Valkenburgh H, Palanivel V, Chapman G, Boman A, Zhang CJ, Kahn RA. ARL1 and membrane traffic in Saccharomyces cerevisiae. Yeast 2002, 19:1039-1056.
48. Bonangelino CJ, Chavez EM, Bonifacino JS. Genomic screen for vacuolar protein sorting genes in Saccharomyces cerevisiae. Mol Biol Cell 2002, 13:2486-2501.
49. Lomize AL, Pogozheva ID, Lomize MA, Mosberg HI. Positioning of proteins in membranes: a computational approach. Protein Sci 2006, 15:1318-1333.
50. Lomize MA, Lomize AL, Pogozheva ID, Mosberg HI. OPM: orientations of proteins in membranes database. Bioinformatics 2006, 22:623-625.
51. Palma-Guerrero J, Lopez-Jimenez JA, Pérez-Berná AJ, Huang I-C, Jansson H-B, Salinas J, Villalaín J, Read ND, Lopez-Llorca LV. Membrane fluidity determines sensitivity of filamentous fungi to chitosan. Mol Microbiol 2010, 75:1021-1032.
52. Opekarova M, Malinsky J, Tanner W. Plants and fungi in the era of heterogeneous plasma membranes. Plant Biol (Stuttg) 2010, 12(Suppl 1):94-98.
53. Hardie DG, Carling D. The AMP-activated protein kinase-fuel gauge of the mammalian cell?. Eur J Biochem 1997, 246:259-273.
54. Palma-Guerrero J, Huang I-C, Jansson H-B, Salinas J, Lopez-Llorca LV, Read ND. Chitosan permeabilizes the plasma membrane and kills cells of Neurospora crassa in an energy dependent manner. Fungal Genet Biol 2009, 46:585-594.
55. Palma-Guerrero J, Jansson H-B, Salinas J, Lopez-Llorca LV. Effect of chitosan on hyphal growth and spore germination of plant pathogenic and biocontrol fungi. J Appl Microbiol 2008, 104:541-553.
56. Gomez-Rivas L, Escudero-Abarca BI, Aguilar-Uscanga MG, Hayward-Jones PM, Mendoza P, Ramirez M. Selective antimicrobial action of chitosan against spoilage yeasts in mixed culture fermentations. J Ind Microbiol Biotechnol 2004, 31:16-22.
57. Hillenmeyer ME, Fung E, Wildenhain J, Pierce SE, Hoon S, Lee W, Proctor M, St Onge RP, Tyers M, Koller D, et al. The chemical genomic portrait of yeast: uncovering a phenotype for all genes. Science 2008, 320:362-365.
58. Sheehan DJ, Hitchcock CA, Sibley CM. Current and emerging azole antifungal agents. Clin Microbiol Rev 1999, 12:40-79.
59. Odds FC, Brown AJ, Gow NA. Antifungal agents: mechanisms of action. Trends Microbiol 2003, 11:272-279.
60. Gruszecki WI, Gagos M, Herec M, Kernen P. Organization of antibiotic amphotericin B in model lipid membranes. A mini review. Cell Mol Biol Lett 2003, 8:161-170.
61. Brajtburg J, Powderly WG, Kobayashi GS, Medoff G. Amphotericin B: current understanding of mechanisms of action. Antimicrob Agents Chemother 1990, 34:183-188.
62. Bottema CK, Parks LW. Delta14-sterol reductase in Saccharomyces cerevisiae. Biochim Biophys Acta 1978, 531:301-307.
63. Burke D. Methods in yeast genetics: a Cold Spring Harbor Laboratory course manual 2000, Cold Spring Harbor Laboratory Press, Plainview, N.Y..
64. Gietz RD, Schiestl RH. Large-scale high-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2007, 2:38-41.
65. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987, 162:156-159.
66. Carvalho BS, Irizarry RA. A framework for oligonucleotide microarray preprocessing. Bioinformatics 2010, 26:2363-2367.
67. Smyth G, Thorne N, Wettenhall J. Limma: linear models for microarray data user's guide. Software manual available from http://www bioconductor org 2003.
68. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30:207-210.
69. Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 1998, 95:14863-14868.
70. de Hoon MJ, Imoto S, Nolan J, Miyano S. Open source clustering software. Bioinformatics 2004, 20:1453-1454.
71. Saldanha AJ. Java Treeview-extensible visualization of microarray data. Bioinformatics 2004, 20:3246-3248.
72. Benschop JJ, Brabers N, van Leenen D, Bakker LV, van Deutekom HW, van Berkum NL, Apweiler E, Lijnzaad P, Holstege FC, Kemmeren P. A consensus of core protein complex compositions for Saccharomyces cerevisiae. Mol Cell 2010, 38:916-928.
73. Merico D, Isserlin R, Stueker O, Emili A, Bader GD. Enrichment map: a network-based method for gene-set enrichment visualization and interpretation. PLoS One 2010, 5:e13984.
74. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2011, 27:431-432.
75. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO. Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 2000, 11:4241-4257.
76. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 2000, 132:365-386.