Chitin and Glucan, the Yin and Yang of the Fungal Cell Wall, Implications for Antifungal Drug Discovery and Therapy

Advances in Applied Microbiology

Volumn 83, Issue , 2013, Pages 145-172

  Munro, Carol A ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Candida; Chitin; Echinocandins; Glucan; Saccharomyces

Indexed keywords

ANTIFUNGAL AGENT; BETA(1-3)GLUCAN; CARBOHYDRATE; CASPOFUNGIN; CHITIN; CHITIN SYNTHASE; ECHINOCANDIN; GLUCAN; GLUCOSIDASE; MANNOPROTEIN; NIKKOMYCIN X; NIKKOMYCIN Z; POLYOXIN B; POLYSACCHARIDE; UNCLASSIFIED DRUG; FUNGAL PROTEIN;

ARTICLE; CALCIUM SIGNALING; CANDIDA ALBICANS; CANDIDIASIS; CELL MEMBRANE; CELL WALL; ENDOPLASMIC RETICULUM; FUNGAL CELL; HOST CELL; NEUROSPORA CRASSA; NONHUMAN; POINT MUTATION; PROTEIN CROSS LINKING; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; ANTIFUNGAL RESISTANCE; CANDIDA; DRUG DEVELOPMENT; GENETICS; HUMAN;

ANTIFUNGAL AGENTS; CANDIDA; CELL WALL; CHITIN; DRUG DISCOVERY; DRUG RESISTANCE, FUNGAL; ECHINOCANDINS; FUNGAL PROTEINS; GLUCANS; HUMANS;

EID: 84877122870     PISSN: 00652164     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-407678-5.00004-0     Document Type: Chapter

References (190)

1. Aebi M., Bernasconi R., Clerc S., Molinari M. N-glycan structures: recognition and processing in the ER. Trends in Biochemical Sciences 2010, 35:74-82.
2. Alvarez F.J., Konopka J.B. Identification of an N-acetylglucosamine transporter that mediates hyphal induction in Candida albicans. Molecular Biology of the Cell 2006, 18:965-975.
3. Arroyo J., Sarfati J., Baixench M.T., Ragni E., Guillen M., Rodriguez-Pena J.M., et al. The GPI-anchored gas and Crh families are fungal antigens. Yeast 2007, 24:289-296.
4. Au-Young J., Robbins P.W. Isolation of a chitin synthase gene (CHS1) from Candida albicans by expression in Saccharomyces cerevisiae. Molecular Microbiology 1990, 4:197-207.
5. Badrane H., Nguyen M.H., Blankenship J.R., Cheng S., Hao B., Mitchell A.P., et al. Rapid redistribution of phosphatidylinositol-(4,5)-bisphosphate and septins during the Candida albicans response to caspofungin. Antimicrobial Agents and Chemotherapy 2012, 56:4614-4624.
6. Beauvais A., Maubon D., Park S., Morelle W., Tanguy M., Huerre M., et al. Two alpha(1-3) glucan synthases with different functions in Aspergillus fumigatus. Applied and Environmental Microbiology 2005, 71:1531-1538.
7. Becker J.M., Marcus S., Tullock J., Miller D., Krainer E., Khare E., et al. Use of the chitin-synthesis inhibitor nikkomycin to treat disseminated candidiasis in mice. The Journal of Infectious Diseases 1988, 157:212-213.
8. Ben Ami R., Garcia-Effron G., Lewis R.E., Gamarra S., Leventakos K., Perlin D.S., et al. Fitness and virulence costs of Candida albicans FKS1 hot spot mutations associated with echinocandin resistance. The Journal of Infectious Diseases 2011, 204:626-635.
9. Blankenship J.R., Mitchell A.P. How to build a biofilm: a fungal perspective. Current Opinion in Microbiology 2006, 9:588-594.
10. Bowen A.R., Chen-Wu J.L., Momany M., Young R., Szaniszlo P.J., Robbins P.W. Classification of fungal chitin synthases. Proceedings of the National Academy of Sciences of the United States of America 1992, 89:519-523.
11. Bruno V.M., Kalachikov S., Subaran R., Nobile C.J., Kyratsous C., Mitchell A.P. Control of the C. albicans cell wall damage response by transcriptional regulator Cas5. PLoS Pathogens 2006, 2:e21.
12. Bulawa C.E. CSD2, CSD3, and CSD4, genes required for chitin synthesis in Saccharomyces cerevisiae: the CSD2 gene product is related to chitin synthases and to developmentally regulated proteins in Rhizobium species and Xenopus laevis. Molecular and Cellular Biology 1992, 12:1764-1776.
13. Bulawa C.E. Genetics and molecular biology of chitin synthesis in fungi. Annual Review of Microbiology 1993, 47:505-534.
14. Bulawa C.E., Miller D.W., Henry L.K., Becker J.M. Attenuated virulence of chitin-deficient mutants of Candida albicans. Proceedings of the National Academy of Sciences of the United States of America 1995, 92:10570-10574.
15. Bulik D.A., Olczak M., Lucero H.A., Osmond B.C., Robbins P.W., Specht C.A. Chitin synthesis in Saccharomyces cerevisiae in response to supplementation of growth medium with glucosamine and cell wall stress. Eukaryotic Cell 2003, 2:886-900.
16. Butler G., Rasmussen M.D., Lin M.F., Santos M.A., Sakthikumar S., Munro C.A., et al. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 2009, 459:657-662.
17. Cabib E. Differential inhibition of chitin synthetases 1 and 2 from Saccharomyces cerevisiae by polyoxin D and nikkomycins. Antimicrobial Agents and Chemotherapy 1991, 35:170-173.
18. Cabib E. Two novel techniques for determination of polysaccharide cross-links show that Crh1p and Crh2p attach chitin to both beta(1-6)- and beta(1-3)glucan in the Saccharomyces cerevisiae cell wall. Eukaryotic Cell 2009, 8:1626-1636.
19. Cabib E., Blanco N., Grau C., Rodriguez-Pena J.M., Arroyo J. Crh1p and Crh2p are required for the cross-linking of chitin to beta(1-6)glucan in the Saccharomyces cerevisiae cell wall. Molecular Microbiology 2007, 63:921-935.
20. Cabib E., Farkas V., Kosik O., Blanco N., Arroyo J., McPhie P. Assembly of the yeast cell wall. Crh1p and Crh2p act as transglycosylases in vivo and in vitro. The Journal of Biological Chemistry 2008, 283:29859-29872.
21. Cantarel B.L., Coutinho P.M., Rancurel C., Bernard T., Lombard V., Henrissat B. The carbohydrate-active enZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Research 2009, 37:D233-D238.
22. Castillo L., Martinez A.I., Garcera A., Garcia-Martinez J., Ruiz-Herrera J., Valentin E., et al. Genomic response programs of Candida albicans following protoplasting and regeneration. Fungal Genetics and Biology 2006, 43:124-134.
23. Chaffin W.L. Candida albicans cell wall proteins. Microbiology and Molecular Biology Reviews 2008, 72:495-544.
24. Chamilos G., Lewis R.E., Albert N., Kontoyiannis D.P. Paradoxical effect of echinocandins across Candida species in vitro: evidence for echinocandin-specific and Candida species-related differences. Antimicrobial Agents and Chemotherapy 2007, 51:2257-2259.
25. Chapman T., Kinsman O., Houston J. Chitin biosynthesis in Candida albicans grown in vitro and in vivo and its inhibition by nikkomycin Z. Antimicrobial Agents and Chemotherapy 1992, 36:1909-1914.
26. Chin C.F., Bennett A.M., Ma W.K., Hall M.C., Yeong F.M. Dependence of Chs2 ER export on dephosphorylation by cytoplasmic Cdc14 ensures that septum formation follows mitosis. Molecular and Cellular Biology 2012, 23:45-58.
27. Coronado J.E., Mneimneh S., Epstein S.L., Qiu W.G., Lipke P.N. Conserved processes and lineage-specific proteins in fungal cell wall evolution. Eukaryotic Cell 2007, 6:2269-2277.
28. Cota J.M., Grabinski J.L., Talbert R.L., Burgess D.S., Rogers P.D., Edlind T.D., et al. Increases in SLT2 expression and chitin content are associated with incomplete killing of Candida glabrata by caspofungin. Antimicrobial Agents and Chemotherapy 2008, 52:1144-1146.
29. Cote P., Hogues H., Whiteway M. Transcriptional analysis of the Candida albicans cell cycle. Molecular and Cellular Biology 2009, 20:3363-3373.
30. Cutler J.E. N-glycosylation of yeast, with emphasis on Candida albicans. Medical Mycology 2001, 39(Suppl. 1):75-86.
31. De Bernardis F., Muhlschlegel F.A., Cassone A., Fonzi W.A. The pH of the host niche controls gene expression in and virulence of Candida albicans. Infection and Immunity 1998, 66:3317-3325.
32. De Groot P.W., de Boer A.D., Cunningham J., Dekker H.L., de Jong L., Hellingwerf K.J., et al. Proteomic analysis of Candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukaryotic Cell 2004, 3:955-965.
33. De Groot P.W., Hellingwerf K.J., Klis F.M. Genome-wide identification of fungal GPI proteins. Yeast 2003, 20:781-796.
34. Decker H., Zahner H., Heitsch H., Konig W.A., Fiedler H.-P. Structure-activity relationships of the nikkomycins. Journal of General Microbiology 1991, 137:1805-1813.
35. Denning D.W. Echinocandin antifungal drugs. Lancet 2003, 362:1142-1151.
36. Douglas C.M. Fungal beta(1,3)-d-glucan synthesis. Medical Mycology 2001, 39(Suppl. 1):55-66.
37. Douglas C.M., D'Ippolito J.A., Shei G.J., Meinz M., Onishi J., Marrinan J.A., et al. Identification of the FKS1 gene of Candida albicans as the essential target of 1,3-beta-D-glucan synthase inhibitors. Antimicrobial Agents and Chemotherapy 1997, 41:2471-2479.
38. Douglas C.M., Foor F., Marrinan J.A., Morin N., Nielsen J.B., Dahl A.M., et al. The Saccharomyces cerevisiae FKS1 (ETG1) gene encodes an integral membrane protein which is a subunit of 1,3-beta-D-glucan synthase. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:12907-12911.
39. Drgonova J., Drgon T., Tanaka K., Kollar R., Chen G.C., Ford R.A., et al. Rho1p, a yeast protein at the interface between cell polarization and morphogenesis. Science 1996, 272:277-279.
40. Dunkler A., Walther A., Specht C.A., Wendland J. Candida albicans CHT3 encodes the functional homolog of the Cts1 chitinase of Saccharomyces cerevisiae. Fungal Genetics and Biology 2005, 42:935-947.
41. Edwards J.E. Fungal cell wall vaccines: an update. Journal of Medical Microbiology 2012, 61:895-903.
42. Eisman B., Alonso-Monge R., Roman E., Arana D., Nombela C., Pla J. The Cek1 and Hog1 mitogen-activated protein kinases play complementary roles in cell wall biogenesis and chlamydospore formation in the fungal pathogen Candida albicans. Eukaryotic Cell 2006, 5:347-358.
43. Ene I.V., Adya A.K., Wehmeier S., Brand A.C., MacCallum D.M., Gow N.A., et al. Host carbon sources modulate cell wall architecture, drug resistance and virulence in a fungal pathogen. Cellular Microbiology 2012, 14:1319-1335.
44. Ene I.V., Heilmann C.J., Sorgo A.G., Walker L.A., De Koster C.G., Munro C.A., et al. Carbon source-induced reprogramming of the cell wall proteome and secretome modulates the adherence and drug resistance of the fungal pathogen Candida albicans. Proteomics 2012, 12:3164-3179.
45. Ernst J.F., Pla J. Signaling the glycoshield: maintenance of the Candida albicans cell wall. International Journal of Medical Microbiology 2011, 301:378-383.
46. Ernst J.F., Prill S.K. O-glycosylation. Medical Mycology 2001, 39(Suppl. 1):67-74.
47. Esteban P.F., Rios I., Garcia R., Duenas E., Pla J., Sanchez M., et al. Characterization of the CaENG1 gene encoding an endo-1,3-beta-glucanase involved in cell separation in Candida albicans. Current Microbiology 2005, 51:385-392.
48. Fortwendel J.R., Juvvadi P.R., Perfect B.Z., Rogg L.E., Perfect J.R., Steinbach W.J. Transcriptional regulation of chitin synthases by calcineurin controls paradoxical growth of Aspergillus fumigatus in response to caspofungin. Antimicrobial Agents and Chemotherapy 2010, 54:1555-1563.
49. Fortwendel J.R., Juvvadi P.R., Pinchai N., Perfect B.Z., Alspaugh J.A., Perfect J.R., et al. Differential effects of inhibiting chitin and 1,3-{beta}-d-glucan synthesis in ras and calcineurin mutants of Aspergillus fumigatus. Antimicrobial Agents and Chemotherapy 2009, 53:476-482.
50. Garcera-Teruel A., Xoconostle-Cazares B., Rosas-Quijano R., Ortiz L., Leon-Ramirez C., Specht C.A., et al. Loss of virulence in Ustilago maydis by Umchs6 gene disruption. Research in Microbiology 2004, 155:87-97.
51. Garcia R., Bermejo C., Grau C., Perez R., Rodriguez-Pena J.M., Francois J., et al. The global transcriptional response to transient cell wall damage in Saccharomyces cerevisiae and its regulation by the cell integrity signaling pathway. Journal of Biological Chemistry 2004, 279:15183-15195.
52. Garcia R., Rodriguez-Pena J.M., Bermejo C., Nombela C., Arroyo J. The high osmotic response and cell wall integrity pathways cooperate to regulate transcriptional responses to zymolyase-induced cell wall stress in Saccharomyces cerevisiae. Journal of Biological Chemistry 2009, 284:10901-10911.
53. 2+/calmodulin-dependent protein phosphatase, is essential in yeast mutants with cell integrity defects and in mutants that lack a functional vacuolar H(+)-ATPase. Molecular and Cellular Biology 1995, 15:4103-4114.
54. Gaughran J.P., Lai M.H., Kirsch D.R., Silverman S.J. Nikkomycin Z is a specific inhibitor of Saccharomyces cerevisiae chitin synthase isozyme Chs3 in vitro and in vivo. Journal of Bacteriology 1994, 176:5857-5860.
55. Goldman R.C., Sullivan P.A., Zakula D., Capobianco J.O. Kinetics of beta-1,3 glucan interaction at the donor and acceptor sites of the fungal glucosyltransferase encoded by the BGL2 gene. European Journal of Biochemistry 1995, 227:372-378.
56. Gow N.A.R., Robbins P.W., Lester J.W., Brown A.J.P., Fonzi W.A., Chapman T., et al. A hyphal-specific chitin synthase gene (CHS2) is not essential for growth, dimorphism, or virulence of Candida albicans. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:6216-6220.
57. Gregori C., Glaser W., Frohner I.E., Reinoso-Martin C., Rupp S., Schuller C., et al. Efg1 Controls caspofungin-induced cell aggregation of Candida albicans through the adhesin Als1. Eukaryotic Cell 2011, 10:1694-1704.
58. Hao B., Cheng S., Clancy C.J., Nguyen M.H. Caspofungin kills Candida albicans by causing both cellular apoptosis and necrosis. Antimicrobial Agents and Chemotherapy 2013, 57:326-332.
59. Hartland R.P., Fontaine T., Debeaupuis J.P., Simenel C., Delepierre M., Latge J.P. A novel beta-(1-3)-glucanosyltransferase from the cell wall of Aspergillus fumigatus. Journal of Biological Chemistry 1996, 271:26843-26849.
60. Hector R.F., Braun P.C. Synergistic action of nikkomycins X and Z with papulacandin B on whole cells and regenerating protoplasts of Candida albicans. Antimicrobial Agents and Chemotherapy 1986, 29:389-394.
61. Hector R.F., Schaller K. Positive interaction of nikkomycins and azoles against Candida albicans in vitro and in vivo. Antimicrobial Agents and Chemotherapy 1992, 36:1284-1289.
62. Hector R.F., Zimmer B.L., Pappagianis D. Evaluation of Nikkomycins X and Z in murine models of coccidioidomycosis, histoplasmosis, and blastomycosis. Antimicrobial Agents and Chemotherapy 1990, 34:587-593.
63. Hochstenbach F., Klis F.M., van den E.H., van Donselaar E., Peters P.J., Klausner R.D. Identification of a putative alpha-glucan synthase essential for cell wall construction and morphogenesis in fission yeast. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:9161-9166.
64. Hogan D.A., Sundstrom P. The Ras/cAMP/PKA signaling pathway and virulence in Candida albicans. Future Microbiology 2009, 4:1263-1270.
65. Hong Z., Mann P., Brown N.H., Tran L.E., Shaw K.J., Hare R.S., et al. Cloning and characterization of KNR4, a yeast gene involved in (1,3)-beta-glucan synthesis. Methods in Molecular and Cellular Biology 1994, 14:1017-1025.
66. Hurtado-Guerrero R., Schuttelkopf A.W., Mouyna I., Ibrahim A.F., Shepherd S., Fontaine T., et al. Molecular mechanisms of yeast cell wall glucan remodelling. Journal of Biological Chemistry 2008.
67. Igual J.C., Johnson A.L., Johnston L.H. Coordinated regulation of gene expression by the cell cycle transcription factor SW14 and the protein kinase C MAP kinase pathway for yeast cell integrity. EMBO Journal 1996, 15:5001-5013.
68. Inglis D.O., Arnaud M.B., Binkley J., Shah P., Skrzypek M.S., Wymore F., et al. The Candida genome database incorporates multiple Candida species: multispecies search and analysis tools with curated gene and protein information for Candida albicans and Candida glabrata. Nucleic Acids Research 2012, 40:D667-D674.
69. Ishihara S., Hirata A., Nogami S., Beauvais A., Latge J.P., Ohya Y. Homologous subunits of 1,3-beta-glucan synthase are important for spore wall assembly in Saccharomyces cerevisiae. Eukaryotic Cell 2007, 6:143-156.
70. Kamada Y., Qadota H., Python C.P., Anraku Y., Ohya Y., Levin D.E. Activation of yeast protein kinase C by Rho1 GTPase. Journal of Biological Chemistry 1996, 271:9193-9196.
71. Kim J.E., Lee H.J., Lee J., Kim K.W., Yun S.H., Shim W.B., et al. Gibberella zeae chitin synthase genes, GzCHS5 and GzCHS7, are required for hyphal growth, perithecia formation, and pathogenicity. Current Genetics 2009, 55:449-459.
72. Kim M.K., Park H.S., Kim C.H., Park H.M., Choi W. Inhibitory effect of nikkomycin Z on chitin synthases in Candida albicans. Yeast 2002, 19:341-349.
73. Kitagaki H., Wu H., Shimoi H., Ito K. Two homologous genes, DCW1 (YKL046c) and DFG5, are essential for cell growth and encode glycosylphosphatidylinositol (GPI)-anchored membrane proteins required for cell wall biogenesis in Saccharomyces cerevisiae. Molecular Microbiology 2002, 46:1011-1022.
74. Klis F.M., Boorsma A., De Groot P.W. Cell wall construction in Saccharomyces cerevisiae. Yeast 2006, 23:185-202.
75. Klis F.M., Brul S., de Groot P.W.J. Covalently linked wall proteins in ascomycetous fungi. Yeast 2010, 27:489-493.
76. Klis F.M., Sosinska G.J., De Groot P.W., Brul S. Covalently linked cell wall proteins of Candida albicans and their role in fitness and virulence. FEMS Yeast Research 2009, 9:1013-1028.
77. Kondoh O., Tachibana Y., Ohya Y., Arisawa M., Watanabe T. Cloning of the RHO1 gene from Candida albicans and its regulation of beta-1,3-glucan synthesis. Journal of Bacteriology 1997, 179:7734-7741.
78. Kong L.A., Yang J., Li G.T., Qi L.L., Zhang Y.J., Wang C.F., et al. Different chitin synthase genes are required for various developmental and plant infection processes in the rice blast fungus Magnaporthe oryzae. PLoS Pathogens 2012, 8:e1002526.
79. Lagorce A., Hauser C.N., Labourdette D., Martin-Yken H., Arroyo J., Hoheisel J.D., et al. Genome-wide analysis of the response to cell wall mutations in the yeast Saccharomyces cerevisiae. Journal of Biological Chemistry 2003, 278:20345-20357.
80. Larson T.M., Kendra D.F., Busman M., Brown D.W. Fusarium verticillioides chitin synthases CHS5 and CHS7 are required for normal growth and pathogenicity. Current Genetics 2011, 57:177-189.
81. Lee K.K., MacCallum D.M., Jacobsen M.D., Walker L.A., Odds F.C., Gow N.A.R., et al. Elevated cell wall chitin in Candida albicans confers echinocandin resistance in vivo. Antimicrobial Agents and Chemotherapy 2011, 56:208-217.
82. Lee K.K., MacCallum D.M., Jacobsen M.D., Walker L.A., Odds F.C., Gow N.A., et al. Elevated cell wall chitin in Candida albicans confers echinocandin resistance in vivo. Antimicrobial Agents and Chemotherapy 2012, 56:208-217.
83. Lenardon M.D., Milne S.A., Mora-Montes H.M., Kaffarnik.F.A., Peck S.C., Brown A.J.P., et al. Phosphorylation regulates polarisation of chitin synthesis in Candida albicans. Journal of Cell Science 2010, 123:2199-2206.
84. Lenardon M.D., Munro C.A., Gow N.A. Chitin synthesis and fungal pathogenesis. Current Opinion in Microbiology 2010, 13:416-423.
85. Lenardon M.D., Whitton R.K., Munro C.A., Marshall D., Gow N.A. Individual chitin synthase enzymes synthesize microfibrils of differing structure at specific locations in the Candida albicans cell wall. Molecular Microbiology 2007, 66:1164-1173.
86. Lesage G., Bussey H. Cell wall assembly in Saccharomyces cerevisiae. Microbiology and Molecular Biology Reviews 2006, 70:317-343.
87. Lesage G., Sdicu A.M., Menard P., Shapiro J., Hussein S., Bussey H. Analysis of beta-1,3-glucan assembly in Saccharomyces cerevisiae using a synthetic interaction network and altered sensitivity to caspofungin. Genetics 2004, 167:35-49.
88. Levin D.E. Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 2011, 189:1145-1175.
89. Li R.K., Rinaldi M.G. In vitro antifungal activity of nikkomycin Z in combination with fluconazole or itraconazole. Antimicrobial Agents and Chemotherapy 1999, 43:1401-1405.
90. Madden K., Snyder M. Cell polarity and morphogenesis in budding yeast. Annual Review of Microbiology 1998, 52:687-744.
91. Madrid M.P., Di Pietro A., Roncero M.I. Class V chitin synthase determines pathogenesis in the vascular wilt fungus Fusarium oxysporum and mediates resistance to plant defence compounds. Molecular Microbiology 2003, 47:257-266.
92. Martin-Urdiroz M., Roncero M.I., Gonzalez-Reyes J.A., Ruiz-Roldan C. ChsVb, a class VII chitin synthase involved in septation, is critical for pathogenicity in Fusarium oxysporum. Eukaryotic Cell 2008, 7:112-121.
93. Martin-Yken H., Dagkessamanskaia A., Basmaji F., Lagorce A., Francois J. The interaction of Slt2 MAP kinase with Knr4 is necessary for signalling through the cell wall integrity pathway in Saccharomyces cerevisiae. Molecular Microbiology 2003, 49:23-35.
94. Martinez-Rucobo F.W., Eckhardt-Strelau L., Terwisscha van Scheltinga A.C. Yeast chitin synthase 2 activity is modulated by proteolysis and phosphorylation. Biochemical Journal 2009, 417:547-554.
95. Maubon D., Park S., Tanguy M., Huerre M., Schmitt C., Prevost M.C., et al. AGS3, an alpha(1-3)glucan synthase gene family member of Aspergillus fumigatus, modulates mycelium growth in the lung of experimentally infected mice. Fungal Genetics and Biology 2006, 43:366-375.
96. Mazur P., Morin N., Baginsky W., el Sherbeini M., Clemas J.A., Nielsen J.B., et al. Differential expression and function of two homologous subunits of yeast 1,3-beta-D-glucan synthase. Molecular and Cellular Biology 1995, 15:5671-5681.
97. McCarthy P.J., Troke P.F., Gull K. Mechanism of action of nikkomycin and the peptide transport system of Candida albicans. Journal of General Microbiology 1985, 131:775-780.
98. McLellan C.A., Whitesell L., King O.D., Lancaster A.K., Mazitschek R., Lindquist S. Inhibiting GPI anchor biosynthesis in fungi stresses the endoplasmic reticulum and enhances immunogenicity. ACS Chemical Biology 2012, 7:1520-1528.
99. Milewski S., Kuszczak D., Jedrzejczak R., Smith R.J., Brown A.J.P., Gooday G.W. Oligomeric structure and regulation of Candida albicans glucosamine-6-phosphate synthase. Journal of Biological Chemistry 1999, 274:4000-4008.
100. Milewski S., Mignini F., Borowski E. Synergistic action of nikkomycin X/Z with azole antifungals on Candida albicans. Journal of General Microbiology 1991, 137:2155-2161.
101. Mio T., Yabe T., Sudoh M., Satoh Y., Nakajima T., Arisawa M., et al. Role of three chitin synthase genes in the growth of Candida albicans. Journal of Bacteriology 1996, 178:2416-2419.
102. Monheit J.E., Cowan D.F., Moore D.G. Rapid detection of fungi in tissues using calcofluor white and fluorescence microscopy. Archives of Pathology & Laboratory Medicine 1984, 108:616-618.
103. Morcx S., Kunz C., Choquer M., Assie S., Blondet E., Simond-Cote E., et al. Disruption of Bcchs4, Bcchs6 or Bcchs7 chitin synthase genes in Botrytis cinerea and the essential role of class VI chitin synthase (Bcchs6). Fungal Genetics and Biology 2012.
104. Mouyna I., Hartland R.P., Fontaine T., Diaquin M., Simenel C., Delepierre M., et al. A 1,3-beta-glucanosyltransferase isolated from the cell wall of Aspergillus fumigatus is a homologue of the yeast Bgl2p. Microbiology 1998, 144:3171-3180.
105. Mouyna I., Morelle W., Vai M., Monod M., Lechenne B., Fontaine T., et al. Deletion of GEL2 encoding for a beta(1-3)glucanosyltransferase affects morphogenesis and virulence in Aspergillus fumigatus. Molecular Microbiology 2005, 56:1675-1688.
106. Mrsa V., Klebl F., Tanner W. Purification and characterization of the Saccharomyces cerevisiae BGL2 gene product, a cell wall endo-beta-1,3-glucanase. Journal of Bacteriology 1993, 175:2102-2106.
107. Munro C.A. Candida albicans cell wall mediated virulence. Handbook of pathogenic yeasts 2009, Springer-Verlag, Berlin, Germany. R. Ashbee, E. Bignell (Eds.).
108. Munro C.A., Gow N.A.R. Chitin biosynthesis as a target for antifungals. Antifungal agents: Discovery and mode of action 1995, Bios Scientific, Oxford, UK. G.K. Dixon (Ed.).
109. Munro C.A., Gow N.A. Chitin synthesis in human pathogenic fungi. Medical Mycology 2001, 39(Suppl. 1):41-53.
110. Munro C.A., Richard M.L. The cell wall; glycoproteins, remodeling and regulation. Candida and candidiasis 2012, ASM Press, Washington DC, USA. 2nd ed. R.A. Calderone, C.J. Clancy (Eds.).
111. Munro C.A., Schofield D.A., Gooday G.W., Gow N.A.R. Regulation of chitin synthesis during dimorphic growth of Candida albicans. Microbiology 1998, 144:391-401.
112. 2+ signalling pathways co-ordinately regulate chitin synthesis in Candida albicans. Molecular Microbiology 2007, 63:1399-1413.
113. Munro C.A., Whitton R.K., Hughes H.B., Rella M., Selvaggini S., Gow N.A. CHS8-a fourth chitin synthase gene of Candida albicans contributes to in vitro chitin synthase activity, but is dispensable for growth. Fungal Genetics and Biology 2003, 40:146-158.
114. Munro C.A., Winter K., Buchan A., Henry K., Becker J.M., Brown A.J., et al. Chs1 of Candida albicans is an essential chitin synthase required for synthesis of the septum and for cell integrity. Molecular Microbiology 2001, 39:1414-1426.
115. Namiki Y., Ueno K., Mitani H., Virtudazo E.V., Ohkusu M., Shimizu K., et al. Scanning and negative-staining electron microscopy of protoplast regeneration of a wild-type and two chitin synthase mutants in the pathogenic yeast Candida glabrata. Journal of Electron Microscopy (Tokyo) 2011, 60:157-165.
116. Negishi T., Ohya Y. The cell wall integrity checkpoint: coordination between cell wall synthesis and the cell cycle. Yeast 2010, 27:513-519.
117. Netea M.G., Gow N.A., Munro C.A., Bates S., Collins C., Ferwerda G., et al. Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and toll-like receptors. Journal of Clinical Investigation 2006, 116:1642-1650.
118. Nett J., Andes D. Candida albicans biofilm development, modeling a host-pathogen interaction. Current Opinion in Microbiology 2006, 9:340-345.
119. Nett J.E., Crawford K., Marchillo K., Andes D.R. Role of Fks1p and matrix glucan in Candida albicans biofilm resistance to an echinocandin, pyrimidine, and polyene. Antimicrobial Agents and Chemotherapy 2010, 54:3505-3508.
120. Nett J.E., Sanchez H., Cain M.T., Andes D.R. Genetic basis of Candida biofilm resistance due to drug-sequestering matrix glucan. Journal of Infectious Diseases 2010, 202:171-175.
121. Nett J.E., Sanchez H., Cain M.T., Ross K.M., Andes D.R. Interface of Candida albicans biofilm matrix-associated drug resistance and cell wall integrity regulation. Eukaryotic Cell 2011, 10:1660-1669.
122. Oh Y., Chang K.J., Orlean P., Wloka C., Deshaies R., Bi E. Mitotic exit kinase Dbf2 directly phosphorylates chitin synthase Chs2 to regulate cytokinesis in budding yeast. Molecular Biology of the Cell 2012, 23:2445-2456.
123. Orlean P., Menon A. Thematic review series: Lipid Posttranslational Modifications. GPI anchoring of protein in yeast and mammalian cells, or: how we learned to stop worrying and love glycophospholipids. Journal of Lipid Research 2007, 48:993-1011.
124. Pardini G., De Groot P.W., Coste A.T., Karababa M., Klis F.M., De Koster C.G., et al. The CRH family coding for cell wall glycosylphosphatidylinositol proteins with a predicted transglycosidase domain affects cell wall organization and virulence of Candida albicans. Journal of Biological Chemistry 2006, 281:40399-40411.
125. Parent S.A., Nielsen J.B., Morin N., Chrebet G., Ramadan N., Dahl A.M., et al. Calcineurin-dependent growth of an FK506 -and CsA-hypersensitive mutant of Saccharomyces cerevisiae. Journal of General Microbiology 1993, 139:2973-2984.
126. Park S., Kelly R., Kahn J.N., Robles J., Hsu M.J., Register E., et al. Specific substitutions in the echinocandin target Fks1p account for reduced susceptibility of rare laboratory and clinical Candida sp. isolates. Antimicrobial Agents and Chemotherapy 2005, 49:3264-3273.
127. Perlin D.S. Current perspectives on echinocandin class drugs. Future Microbiology 2011, 6:441-457.
128. Pitarch A., Jimenez A., Nombela C., Gil C. Decoding serological response to Candida cell wall immunome into novel diagnostic, prognostic, and therapeutic candidates for systemic candidiasis by proteomic and bioinformatic analyses. Molecular & Cellular Proteomics 2006, 5:79-96.
129. Plaine A., Walker L., Da Costa G., Mora-Montes H.M., McKinnon A., Gow N.A., et al. Functional analysis of Candida albicans GPI-anchored proteins: roles in cell wall integrity and caspofungin sensitivity. Fungal Genetics and Biology 2008, 45:1404-1414.
130. Pruyne D., Gao L., Bi E., Bretscher A. Stable and dynamic axes of polarity use distinct formin isoforms in budding yeast. Molecular Biology of the Cell 2004, 15:4971-4989.
131. Qadota H., Python C.P., Inoue S.B., Arisawa M., Anraku Y., Zheng Y., et al. Identification of yeast Rho1p GTPase as a regulatory subunit of 1,3- beta-glucan synthase. Science 1996, 272:279-281.
132. Ramage G., Mowat E., Jones B., Williams C., Lopez-Ribot J. Our current understanding of fungal biofilms. Critical Reviews in Microbiology 2009, 35:340-355.
133. Ram A.F., Klis F.M. Identification of fungal cell wall mutants using susceptibility assays based on calcofluor white and Congo red. Nature Protocols 2006, 1:2253-2256.
134. Rappleye C.A., Eissenberg L.G., Goldman W.E. Histoplasma capsulatum alpha-(1,3)-glucan blocks innate immune recognition by the beta-glucan receptor. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:1366-1370.
135. Reinoso-Martin C., Schuller C., Schuetzer-Muehlbauer M., Kuchler K. The yeast protein kinase C cell integrity pathway mediates tolerance to the antifungal drug caspofungin through activation of Slt2p mitogen-activated protein kinase signaling. Eukaryotic Cell 2003, 2:1200-1210.
136. Reyes A., Sanz M., Duran A., Roncero C. Chitin synthase III requires Chs4p-dependent translocation of Chs3p into the plasma membrane. Journal of Cell Science 2007, 120:1998-2009.
137. Riquelme M., Bartnicki-Garcia S., Gonzalez-Prieto J.M., Sanchez-Leon E., Verdin-Ramos J.A., Beltran-Aguilar A., et al. Spitzenkorper localization and intracellular traffic of green fluorescent protein-labeled CHS-3 and CHS-6 chitin synthases in living hyphae of Neurospora crassa. Eukaryotic Cell 2007, 6:1853-1864.
138. Rodriguez-Pena J.M., Garcia R., Nombela C., Arroyo J. The high-osmolarity glycerol (HOG) and cell wall integrity (CWI) signalling pathways interplay: a yeast dialogue between MAPK routes. Yeast 2010, 27:495-502.
139. Roncero C. The genetic complexity of chitin synthesis in fungi 2002, (pp. 367-378). 41 ed.
140. Roncero C., Duran A. Effect of Calcofluor white and Congo red on fungal cell wall morphogenesis: in vivo activation of chitin polymerization. Journal of Bacteriology 1985, 163:1180-1185.
141. Roncero C., Valdivieso M.H., Ribas J.C., Duran A. Effect of calcofluor white on chitin synthases from Saccharomyces cerevisiae. Journal of Bacteriology 1988, 170:1945-1949.
142. Ruiz-Herrera J., Gonzalez-Prieto J.M., Ruiz-Medrano R. Evolution and phylogenetic relationships of chitin synthases from yeasts and fungi. FEMS Yeast Research 2002, 1:247-256.
143. Sanchez-Leon E., Verdin J., Freitag M., Roberson R.W., Bartnicki-Garcia S., Riquelme M. Traffic of chitin synthase 1 (CHS-1) to the Spitzenkorper and developing septa in hyphae of Neurospora crassa: actin dependence and evidence of distinct microvesicle populations. Eukaryotic Cell 2011, 10:683-695.
144. Sandovsky-Losica H., Shwartzman R., Lahat Y., Segal E. Antifungal activity against Candida albicans of nikkomycin Z in combination with caspofungin, voriconazole or amphotericin B. Journal of Antimicrobial Chemotherapy 2008, 62:635-637.
145. Santos B., Snyder M. Targeting of chitin synthase 3 to polarized growth sites in yeast requires Chs5p and Myo2p. Journal of Cell Biology 1997, 136:95-110.
146. Sanz M., Carrano L., Jimenez C., Candiani G., Trilla J.A., Duran A., et al. Candida albicans strains deficient in CHS7, a key regulator of chitin synthase III, exhibit morphogenetic alterations and attenuated virulence. Microbiology 2005, 151:2623-2636.
147. Sanz M., Trilla J.A., Duran A., Roncero C. Control of chitin synthesis through Shc1p, a functional homologue of Chs4p specifically induced during sporulation. Molecular Microbiology 2002, 43:1183-1195.
148. Saputo S., Chabrier-Rosello Y., Luca F.C., Kumar A., Krysan D.J. The RAM network in pathogenic fungi. Eukaryotic Cell 2012, 11:708-717.
149. Sarthy A.V., McGonigal T., Coen M., Frost D.J., Meulbroek J.A., Goldman R.C. Phenotype in Candida albicans of a disruption of the BGL2 gene encoding a 1,3-b-glucosyltransferase. Microbiology 1997, 143:367-376.
150. Schuster M., Treitschke S., Kilaru S., Molloy J., Harmer N.J., Steinberg G. Myosin-5, kinesin-1 and myosin-17 cooperate in secretion of fungal chitin synthase. EMBO Journal 2012, 31:214-227.
151. Selitrennikoff C.P. Calcofluor white inhibits Neurospora chitin synthetase activity. Experimental Mycology 1984, 8:269-272.
152. Shields R.K., Nguyen M.H., Du C., Press E., Cheng S., Clancy C.J. Paradoxical effect of caspofungin against Candida bloodstream isolates is mediated by multiple pathways but eliminated in human serum. Antimicrobial Agents and Chemotherapy 2011, 55:2641-2647.
153. Sohn K., Urban C., Brunner H., Rupp S. EFG1 is a major regulator of cell wall dynamics in Candida albicans as revealed by DNA microarrays. Molecular Microbiology 2003, 47:89-102.
154. Sorgo A.G., Heilmann C.J., Dekker H.L., Brul S., De Koster C.G., Klis F.M. Mass spectrometric analysis of the secretome of Candida albicans. Yeast 2010, 27:661-672.
155. Soulie M.C., Perino C., Piffeteau A., Choquer M., Malfatti P., Cimerman A., et al. Botrytis cinerea virulence is drastically reduced after disruption of chitin synthase class III gene (Bcchs3a). Cellular Microbiology 2006, 8:1310-1321.
156. Soulie M.C., Piffeteau A., Choquer M., Boccara M., Vidal-Cros A. Disruption of Botrytis cinerea class I chitin synthase gene Bcchs1 results in cell wall weakening and reduced virulence. Fungal Genetics and Biology 2003, 40:38-46.
157. Spreghini E., Davis D.A., Subaran R., Kim M., Mitchell A.P. Roles of Candida albicans Dfg5p and Dcw1p cell surface proteins in growth and hypha formation. Eukaryotic Cell 2003, 2:746-755.
158. Stevens D.A. Drug interaction studies of a glucan synthase inhibitor (LY 303366) and a chitin synthase inhibitor (Nikkomycin Z) for inhibition and killing of fungal pathogens. Antimicrobial Agents and Chemotherapy 2000, 44:2547-2548.
159. Stevens D.A., Calderon L., Martinez M., Clemons K.V., Wilson S.J., Selitrennikoff C.P. Zeamatin, clotrimazole and nikkomycin Z in therapy of a Candida vaginitis model. Journal of Antimicrobial Chemotherapy 2002, 50:361-364.
160. Stevens D.A., Espiritu M., Parmar R. Paradoxical effect of caspofungin: reduced activity against Candida albicans at high drug concentrations. Antimicrobial Agents and Chemotherapy 2004, 48:3407-3411.
161. Stevens D.A., Ichinomiya M., Koshi Y., Horiuchi H. Escape of Candida from caspofungin inhibition at concentrations above the MIC (paradoxical effect) accomplished by increased cell wall chitin; evidence for beta-1,6-glucan synthesis inhibition by caspofungin. Antimicrobial Agents and Chemotherapy 2006, 50:3160-3161.
162. Strahl-Bolsinger S., Gentzsch M., Tanner W. Protein O-mannosylation. Biochimica et Biophysica Acta 1999, 1426:297-307.
163. Sudbery P. Fluorescent proteins illuminate the structure and function of the hyphal tip apparatus. Fungal Genetics and Biology 2011, 48:849-857.
164. Sudoh M., Tatsuno K., Ono N., Ohta A., Chibana H., Yamada-Okabe H., et al. The Candida albicans CHS4 gene complements a Saccharomyces cerevisiae skt5/chs4 mutation and is involved in chitin biosynthesis. Microbiology 1999, 145:1613-1622.
165. Sudoh M., Yamazaki T., Masubuchi K., Taniguchi M., Shimma N., Arisawa M., et al. Identification of a novel inhibitor specific to the fungal chitin synthase; inhibition of chitin synthase 1 arrests the cell growth, but that of chitin synthase 1 and 2 is lethal in the pathogenic fungus Candida albicans. Journal of Biological Chemistry 2000, 275:32901-32905.
166. Taff H.T., Nett J.E., Zarnowski R., Ross K.M., Sanchez H., Cain M.T., et al. A Candida biofilm-induced pathway for matrix glucan delivery: implications for drug resistance. PLoS Pathogens 2012, 8:e1002848.
167. Takeshita N., Yamashita S., Ohta A., Horiuchi H. Aspergillus nidulans class V and VI chitin synthases CsmA and CsmB, each with a myosin motor-like domain, perform compensatory functions that are essential for hyphal tip growth. Molecular Microbiology 2006, 59:1380-1394.
168. Teh E.M., Chai C.C., Yeong F.M. Retention of Chs2p in the ER requires N-terminal CDK1-phosphorylation sites. Cell Cycle 2009, 8:2964-2974.
169. Treitschke S., Doehlemann G., Schuster M., Steinberg G. The myosin motor domain of fungal chitin synthase V is dispensable for vesicle motility but required for virulence of the maize pathogen Ustilago maydis. Plant Cell 2010, 22:2476-2494.
170. Trilla J.A., Cos T., Duran A., Roncero C. Characterization of CHS4 (CAL2), a gene of Saccharomyces cerevisiae involved in chitin biosynthesis and allelic to SKT5 and CSD4. Yeast 1997, 13:795-807.
171. Trilla J.A., Duran A., Roncero C. Chs7p, a new protein involved in the control of protein export from the endoplasmic reticulum that is specifically engaged in the regulation of chitin synthesis in Saccharomyces cerevisiae. Journal of Cell Biology 1999, 145:1153-1163.
172. Tsuizaki M., Takeshita N., Ohta A., Horiuchi H. Myosin motor-like domain of the class VI chitin synthase CsmB is essential to its functions in Aspergillus nidulans. Bioscience, Biotechnology, and Biochemistry 2009, 73:1163-1167.
173. Villegas L.R., Kottom T.J., Limper A.H. Chitinases in Pneumocystis carinii pneumonia. Medical Microbiology and Immunology 2012, 201:337-348.
174. Vollmer W., Blanot D., de Pedro M.A. Peptidoglycan structure and architecture. FEMS Microbiology Reviews 2008, 32:149-167.
175. Walker L.A., Gow N.A., Munro C.A. Fungal echinocandin resistance. Fungal Genetics and Biology 2010, 47:117-126.
176. Walker L.A., Gow N.A., Munro C.A. Elevated chitin content reduces the susceptibility of Candida species to caspofungin. Antimicrobial Agents and Chemotherapy 2013, 57:146-154.
177. Walker L.A., Munro C.A., de Bruijn I., Lenardon M.D., McKinnon A., Gow N.A. Stimulation of chitin synthesis rescues Candida albicans from echinocandins. PLoS Pathogens 2008, 4:e1000040.
178. Wang Z., Zheng L., Liu H., Wang Q., Hauser M., Kauffman S., et al. WdChs2p, a class I chitin synthase, together with WdChs3p (class III) contributes to virulence in Wangiella (Exophiala) dermatitidis. Infection and Immunity 2001, 69:7517-7526.
179. Watanabe N.A., Miyazaki M., Horii T., Sagane K., Tsukahara K., Hata K. E1210, a new broad-spectrum antifungal, suppresses Candida albicans hyphal growth through inhibition of glycosylphosphatidylinositol biosynthesis. Antimicrobial Agents and Chemotherapy 2012, 56:960-971.
180. Werner S., Sugui J.A., Steinberg G., Deising H.B. A chitin synthase with a myosin-like motor domain is essential for hyphal growth, appressorium differentiation, and pathogenicity of the maize anthracnose fungus Colletotrichum graminicola. Molecular Plant-Microbe Interactions 2007, 20:1555-1567.
181. Wheeler R.T., Kombe D., Agarwala S.D., Fink G.R. Dynamic, morphotype-specific Candida albicans beta-glucan exposure during infection and drug treatment. PLoS Pathogens 2008, 4:e1000227.
182. Wiederhold N.P. Attenuation of echinocandin activity at elevated concentrations: a review of the paradoxical effect. Current Opinion in Infectious Diseases 2007, 20:574-578.
183. Wiederhold N.P. Paradoxical echinocandin activity: a limited in vitro phenomenon?. Medical Mycology 2009, 47(Suppl. 1):S369-S375.
184. Wiederhold N.P., Kontoyiannis D.P., Prince R.A., Lewis R.E. Attenuation of the activity of caspofungin at high concentrations against Candida albicans: possible role of cell wall integrity and calcineurin pathways. Antimicrobial Agents and Chemotherapy 2005, 49:5146-5148.
185. Xu Y.B., Li H.P., Zhang J.B., Song B., Chen F.F., Duan X.J., et al. Disruption of the chitin synthase gene CHS1 from Fusarium asiaticum results in an altered structure of cell walls and reduced virulence. Fungal Genetics and Biology 2010, 47:205-215.
186. Yadan J.C., Gonneau M., Sarthou P., Le Goffic F. Sensitivity to nikkomycin Z in Candida albicans: role of peptide permeases. Journal of Bacteriology 1984, 160:884-888.
187. Yamochi W., Tanaka K., Nonaka H., Maeda A., Musha T., Takai Y. Growth site localization of Rho1 small GTP-binding protein and its involvement in bud formation in Saccharomyces cerevisiae. Journal of Cell Biology 1994, 125:1077-1093.
188. Yoshimoto H., Saltsman K., Gasch A.P., Li H.X., Ogawa N., Botstein D., et al. Genome-wide analysis of gene expression regulated by the calcineurin/Crz1p signaling pathway in Saccharomyces cerevisiae. Journal of Biological Chemistry 2002, 277:31079-31088.
189. Zhang Z., Liu X., Lv X., Lin J. Variation in genotype and higher virulence of a strain of Sporothrix schenckii causing disseminated cutaneous sporotrichosis. Mycopathologia 2011, 172:439-446.
190. Ziman M., Chuang J.S., Tsung M., Hamamoto S., Schekman R. Chs6p-dependent anterograde transport of Chs3p from the chitosome to the plasma membrane in Saccharomyces cerevisiae. Molecular Biology of the Cell 1998, 9:1565-1576.