The genetic complexity of chitin synthesis in fungi

Current Genetics

Volumn 41, Issue 6, 2002, Pages 367-378

  Roncero, Cesar ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

Cell wall; Chitin; Chitin synthases; CHS genes; Fungi

Indexed keywords

CHITIN; CHITIN SYNTHASE; ISOENZYME;

ARTICLE; ASPERGILLUS FUMIGATUS; CARBOHYDRATE SYNTHESIS; FUNGAL GENETICS; GENETIC VARIABILITY; GENOMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REGULATORY MECHANISM; SCHIZOSACCHAROMYCES POMBE; YEAST CELL;

CELL WALL; CHITIN SYNTHASE; FUNGI; GENES, FUNGAL; GENOME, FUNGAL; ISOENZYMES; PHYLOGENY;

ASPERGILLUS; ASPERGILLUS FUMIGATUS; FUNGI; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE;

EID: 0036935611     PISSN: 01728083     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00294-002-0318-7     Document Type: Article

References (81)

1. Appeltauer U, Achstetter T (1989) Hormone-induced expression of the CHS1 gene from Saccharomyces cerevisiae. Eur J Biochem 181:243-247
2. Arellano JM, Cartagena-Lirola H, Nasser-Hajibagheri MA, Duran A, Valdivieso MH (2000) Proper ascospore maturation requires the chs1 + chitin synthase gene in Schizosaccharomyces pombe. Mol Microbiol 35:79-89
3. Aufauvre-Brown A, Mellado E, Gow NA, Holden DW (1997) Aspergillus fumigatus chsE: a gene related to CHS3 of Saccharomyces cerevisiae and important for hyphal growth and conidiophore development but not pathogenicity. Fungal Genet Biol 21:141-152
4. Bartnicki-Garcia S (1968) Cell wall, chemistry, morphogenesis and taxonomy of fungi. Annu Rev Microbiol 22:87-108
5. Bateman A, Chothia C (1996) Fibronectin III domain in yeast detected by a hidden Markov model. Curr Biol 6:1544-1547
6. Borgia PT, Iartchouk N, Riggle PJ, Winter KR, Koltin Y, Bulawa CE (1996) The chsB gene of Aspergillus nidulans is necessary for normal hyphal growth and development. Fungal Genet Biol 20:193-203
7. Bulawa CE (1992) 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. Mol Cell Biol 12:1764-1776
8. Bulawa CE (1993) Genetics and molecular biology of chitin synthesis in fungi. Annu Rev Microbiol 47:505-534
9. Bulawa CE, Osmond BC (1990) Chitin synthase I and chitin synthase II are not required for chitin synthesis in vivo in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 87:7424-7428
10. Bulawa CE, Wasco W (1991) Chitin and nodulation. Nature 353:710
11. Bulawa CE, Slater M, Cabib E, Au-Young J, Sburlati A, Adair WLJ, Robbins PW (1986) The S. cerevisiae structural gene for chitin synthase is not required for chitin synthesis in vivo. Cell 46:213-225
12. Bulawa CE, Miller DW, Henry LK, Becker JM (1995) Attenuated virulence of chitin-deficient mutants of Candida albicans. Proc Natl Acad Sci USA 92:10570-10574
13. Cabib E, Roberts R, Bowers B (1982) Synthesis of the yeast cell wall and its regulation. Annu Rev Biochem 51:763-793
14. Cabib E, Sburlati A, Bowers B, Silverman SJ (1989) Chitin synthase 1, an auxiliary enzyme for chitin synthesis in Saccharomyces cerevisiae. J Cell Biol 108:1665-1672
15. Cabib E, Silverman SJ, Shaw JA (1992) Chitinase and chitin synthase 1: counterbalancing activities in cell separation of Saccharomyces cerevisiae. J Gen Microbiol 138:97-102
16. Cabib E, Shaw JA, Mol PC, Bowers B, Choi WJ (1996) Chitin biosynthesis and morphogenetic processes. In: Brambl R, Marzluf GA (eds) The Mycota. Biochemistry and molecular biology, vol 3. Springer, Berlin Heidelberg New York, pp 243-267
17. Chen-Wu JL, Zwicker J, Bowen AR, Robbins PW (1992) Expression of chitin synthase genes during yeast and hyphal growth phases of Candida albicans. Mol Microbiol 6:497-502
18. Chigira Y, Abe K, Gomi K, Nakajima T (2002) chsZ, a gene for a novel class of chitin synthase from Aspergillus oryzae. Curr Genet (in press)
19. Choi W, Cabib E (1994) The use of divalent cations and pH for the determination of specific yeast chitin synthases. Anal Biochem 219:368-372
20. Choi W, Santos B, Duran A, Cabib E (1994a) Are yeast chitin synthases regulated at the transcriptional or the posttranslational level? Mol Cell Biol 14:7685-7694
21. Choi W, Sburlati A, Cabib E (1994b) Chitin synthase 3 from yeast has zymogenic properties that depend on both the CAL1 and CAL3 genes. Proc Natl Acad Sci USA 91:4727-4730
22. Chuang JS, Schekman RW (1996) Differential trafficking and timed localization of two chitin synthase proteins, Chs2p and Chs3p. J Cell Biol 135:597-610
23. Cos T, Ford RA, Trilla JA, Duran A, Cabib E, Roncero C (1998) Molecular analysis of Chs3p participation in chitin synthase III activity. Eur J Biochem 256:419-426
24. Culp DW, Dodge CL, Miao Y, Li L, Sag-Ozkal D, Borgia PT (2000) The chsA gene from Aspergillus nidulans is necessary for maximal conidiation. FEMS Microbiol Lett 182:349-353
25. DeMarini DJ, Adams AEM, Fares H, De Virgilio C, Valle G, Chuang JS, Pringle JR (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
26. Din AB, Yarden O (1994) The Neurospora crassa chs-2 gene encodes a non-essential chitin synthase. Microbiology 140:2189-2197
27. Din AB, Specht CA, Robbins PW, Yarden O (1996) chs-4, a class IV chitin synthase gene from Neurospora crassa. Mol Gen Genet 250:214-222
28. Fujiwara M, Ichinomiya M, Motoyama T, Horiuchi H, Ohta A, Takagi M (2000) Evidence that the Aspergillus nidulans Class I and Class II chitin synthase genes, chsC and chsA, share critical roles in hyphal wall integrity and conidiophore development. J Biochem 127:359-366
29. Gagou ME, Kapsetaki M, Turberg A, Kafetzopoulos D (2002) Stage-specific expression of the chitin synthase DmeChSA and DmeChSB genes during the onset of Drosophila melanogaster. Insect Biochem Mol Biol 32:141-146
30. Garcia-Rodriguez LJ, Trilla JA, Castro C, Valdivieso A, Duran A, Roncero C (2000) Characterization of the chitin biosynthesis process as a compensatory mechanism in the fks1 mutant of Saccharomyces cerevisiae. FEBS Lett 478:84-88
31. Georgopapadakou N (2001) Update on antifungals targeted to the cell wall: focus on beta-1,3-glucan synthase inhibitors. Expert Opin Invest Drugs 10:269-280
32. Gold SE, Kronstad JW (1994) Disruption of two genes for chitin synthase in the phytopathogenic fungus Ustilago maydis. Mol Microbiol 11:897-902
33. Gow NAR, Robbins PW, Lester JW, Brown AJP, Fonzi WA, Chapman T, Kinsman OS (1994) A hyphal-specific chitin synthase gene (CHS2) is not essential for growth, dimorphism, or virulence of Candida albicans. Proc Natl Acad Sci USA 91:6216-6220
34. Grant B, Greenwald I (1996) The Caenorhabditis elegans sel-1 gene, a negative regulator of lin-12 and glp-1, encodes a predicted extracellular protein. Genetics 143:237-247
35. Holthuis JC, Nichols BJ, Pelham HR (1998) The syntaxin Tlg1p mediates trafficking of chitin synthase III to polarized growth sites in yeast. Mol Cell Biol 9:3383-3397
36. Horiuchi H, Fujiwara M, Yamashita S, Ohta A, Takagi M (1999) Proliferation of intrahyphal hyphae caused by disruption of csmA, which encodes a class V chitin synthase with a myosin motor-like domain in Aspergillus nidulans. J Bacteriol 181:3721
37. Igual JC, Johnson AL, Johnston LH (1996) Coordinated regulation of gene expression by the cell cycle transcription factor SWI4 and the protein kinase C MAP kinase pathway for yeast cell integrity. EMBO J 15:5001-5013
38. Kawamoto S, Nomura N, Ohno T (1992) Cloning and characterization of SKT5, a Saccharomyces cerevisiae gene that affects protoplast regeneration and resistance to killer toxin of Kluyveromyces lactis. J Ferment Bioeng 74:199-108
39. Lagorce A, Le Berre-Anton V, Aguilar-Uscanga B, Martin-Yken H, Dagkessamanskaia A, Francois J (2002) Involvement of GFA1, which encodes glutamine-fructose-6-phosphate amido-transferase, in the activation of the chitin synthesis pathway in response to cell-wall defects in Saccharomyces cerevisiae. Eur J Biochem 269:1697-1707
40. Liu H, Wang Z, Zheng L, Hauser M, Kauffman S, Becker JM, Szanislo PJ (2001) Relevance of chitin and chitin synthases to virulence in Wangiella (Exophiala) dermatitidis, a model melanized pathogen of humans. In: Muzarelli RAA (ed) Chitin enzymology 2001. Atec Edizioni, Rome, pp 463-472
41. Mellado E, Aufauvre BA, Gow, NAR, Holden DW (1996a) The Aspergillus fumigatus chsC and chsG genes encode class III chitin synthases with different functions. Mol Microbiol 20:667-679
42. Mellado E, Specht CA, Robbins PW, Holden DW (1996b) Cloning and characterization of chsD, a chitin synthase-like gene of Aspergillus fumigatus. FEMS Microbiol Lett 143:69-76
43. Mio T, Yabe T, Sudoh M, Satoh Y, Nakajima T, Arisawa M, Yamada-Okabe H (1996) Role of three chitin synthase genes in the growth of Candida albicans. J Bacteriol 178:2416-4219
44. Motoyama T, Fujiwara M, Kojima N, Horiuchi H, Ohta A, Takagi M (1997) The Aspergillus nidulans genes chsA and chsD encode chitin synthases which have redundant functions in conidia formation. Mol Gen Genet 253:520-528
45. Munro CA, Gow NAR (2001) Chitin synthesis in human pathogenic fungi. Med Mycol 39 [Suppl 1]:41-53
46. Munro CA, Schofield DA, Gooday GW, Gow NAR (1998) Regulation of chitin synthesis during dimorphic growth of Candida albicans. Microbiology 144:391-401
47. Munro CA, Winter K, Buchan A, Henry K, Becker JM, Brown AJ, Bulawa CE, Gow NAR (2001) Chs1 of Candida albicans is an essential chitin synthase required for synthesis at the septum and for cell integrity. Mol Microbiol 39:1414-1426
48. Ono N, Yabe T, Sudoh M, Nakajima T, Yamada-Okabe T, Arisawa M, Yamada-Okabe H (2000) The yeast Chs4p protein stimulates the trypsin-sensitive activity of chitin synthase 3 through an apparent protein-protein interaction. Microbiology 146:385-391
49. Orlean P (1997) Biogenesis of yeast wall and surface components. In: Pringle JR, Broach JR, Jones EW (eds) Cell cycle and cell biology. (The molecular and cellular biology of the yeast Saccharomyces, vol 3) Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y., pp 229-362
50. Pammer M, Briza P, Ellinger A, Schuster T, Stucka R, Bteintenbach M (1992) DIT101 (CSD2, CAL1), a cell cycle-regulated yeast gene required for synthesis of chitin in cell walls and chitosan in spore walls. Yeast 9:1089-1099
51. Popolo L, Gualtieri T, Ragni E (2001) The yeast cell-wall salvage pathway. Med Mycol 39 [Suppl 1]:111-121
52. Roncero C, Valdivieso M, Ribas JC, Duran A (1988) Isolation and characterization of Saccharomyces cerevisiae mutants resistant to calcofluor white. J Bacteriol 170:1950-1954
53. Santos B, Snyder M (1997) Targeting of chitin synthase 3 to polarized growth sites in yeast requires Chs5p and Myo2p. J Cell Biol 136:95-110
54. Santos B, Duran A, Valdivieso MH (1997) CHS5, a gene involved in chitin synthesis and mating in Saccharomyces cerevisiae. Mol Cell Biol 17:2485-2496
55. Sanz M, Trilla JA, Duran A, Roncero C (2002) Control of chitin synthesis through Shc1p, a functional homologue of Chs4p specifically induced during sporulation. Mol Microbiol 43:1183-1195
56. Sburlati A, Cabib E (1986) Chitin synthase 2, a presumptive participant in septum formation in Saccharomyces cerevisiae. J Biol Chem 261:15147-15152
57. Schmidt M, Bowers B, Varma A, Roh DH, Cabib E (2002) In budding yeast, contraction of the actomyosin ring and formation of the primary septum at cytokinesis depend on each other. J Cell Sci 115:293-302
58. Semino CE, Specht CA, Raimondi A, Robbins PW (1996) Homologs of the Xenopus developmental gene DG42 are present in zebrafish and mouse and are involved in the synthesis of Nod-like chitin oligosaccharides during early embryogenesis. Proc Natl Acad Sci USA 93:4548-4553
59. Shaw JA, Mol PC, Bowers B, Silverman SJ, Valdivieso MH, Duran A, Cabib E (1991) The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle. J Cell Biol 114:111-123
60. Silverman SJ, Sburlati A, Slater ML, Cabib E (1988) Chitin synthase 2 is essential for septum formation and cell division in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 85:4735-4739
61. Smits GJ, Kapteyn JC, Ende H van den, Klis FM (1999) Cell wall dynamics in yeast. Curr Opin Microbiol 2:348-352
62. Smits GJ, Ende H van den, Klis FM (2001) Differential regulation of cell wall biogenesis during growth and development in yeast. Microbiology 147:781-784
63. Specht CA, Liu Y, Robbins PW, Bulawa CE, Iartchouk N, Winter KR, Riggle PJ, Rhodes JC, Dodge CL, Culp DW, Borgia PT (1996) The chsD and chsE genes of Aspergillus nidulans and their roles in chitin synthesis. Fungal Genet Biol 20:153-167
64. Sudoh M, Tatsuno K, Ono N, Chibana H, Yamada-Okabe H, Arisawa M (1999) The Candida albicans CHS4 gene complements a Saccharomyces cerevisiae skt5/chs4 mutation and is involved in chitin biosynthesis. Microbiology 145:1613-1622
65. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680
66. Tkacz JS, DiDomenico B (2001) Antifungals: what's in the pipeline. Curr Opin Microbiol 4:540-545
67. Trilla JA, Cos T, Duran A, Roncero C (1997) Characterisation of CHS4 (CAL2), a gene of Saccharomyces cerevisiae involved in chitin biosynthesis and allelic to SKT5 and CSD4. Yeast 13:795-807
68. Trilla JA, Duran A, Roncero C (1999) 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. J Cell Biol 145:1153-1163
69. Valdivia RH, Baggot D, Chuang JS, Schekman R (2002) The yeast Clathrin adaptor protein complex 1 is required for the efficient retention of a subset of late Golgi membrane proteins. Dev Cell 2:283-294
70. Valdivieso MH, Mol PC, Shaw JA, Cabib E, Duran A (1991) CAL1, a gene required for activity of chitin synthase 3 in Saccharomyces cerevisiae. J Cell Biol 114:101-109
71. Valdivieso MH, Duran A, Roncero C (1999) Chitin synthases in yeast and fungi. In: Jolles P, Muzarelli RAA (eds) Chitin and chitinases. Birkhauser, Basel, pp 53-67
72. Valdivieso MH, Ferrario L, Vai M, Duran A, Popolo L (2000) Chitin synthesis in a gas1 mutant of Saccharomyces cerevisiae. J Bacteriol 182:4752-4757
73. Veronico P, Gray LJ, Jones JT, Bazzicalupo P, Arbucci S, Cortese MR, Di Vito M, De Giorgi C (2001) Nematode chitin synthases: gene structure, expression and function in Caenorhabditis elegans and the plant parasitic nematode Meloidogyne artiella. Mol Genet Genom 266:28-34
74. Wang Z, Szanislo PJ (2000) WdCHS3, a gene that encodes a class III chitin synthase in Wangiella (Exophiala) dermatitidis, is expressed differentially under stress conditions. J Bacteriol 182:874-881
75. Wang Z, Zheng L, Hauser M, Becker JM, Szanislo PJ (1999) WdCHS4, a homolog of chitin synthase 3 in Saccharomyces cerevisiae, alone cannot support growth of Wangiella (Exophiala) dermatitidis at the temperature of infection. Infect Immun 67:6619-6630
76. Wang Z, Zheng L, Liu H, Wang Q, Hauser M, Kauffman S, Becker JM, Szanislo PJ (2001) WdCHS2p, a class I chitin synthase, together with WdCHS3p (Class III) contributes to virulence in Wangiella (Exophiala) dermatitidis. Infect Immun 69:7517-7526
77. Xoconostle-Cazares B, Leon-Ramirez C, Ruiz-Herrera J (1996) Two chitin synthase genes from Ustilago maydis. Microbiology 142:377-387
78. Xoconostle-Cazares B, Specht CA, Robbins PW, Liu Y, Leon C, Ruiz-Herrera J (1997) Umchs5, a gene coding for a class IV chitin synthase in Ustilago maydis. Fungal Genet Biol 22:199-208
79. Yarden O, Yanofsky C (1991) Chitin synthase 1 plays a major role in cell wall biogenesis in Neurospora crassa. Genes Dev 5:2420-2430
80. Ziman M, Chuang JS, Schekman RW (1996) Chs1p and Chs3p, two proteins involved in chitin synthesis, populate a compartment of the Saccharomyces cerevisiae endocytic pathway. Mol Biol Cell 7:1909-1919
81. Ziman M, Chuang JS, Tsung M, Hamamoto S, Schekman R (1998) Chs6p-dependent anterograde transport of Chs3p from the chitosome to the plasma membrane in Saccharomyces cerevisiae. Mol Biol Cell 9:1565-1576