Chitin synthesis and fungal pathogenesis

Current Opinion in Microbiology

Volumn 13, Issue 4, 2010, Pages 416-423

  Lenardon, Megan D ^a   Munro, Carol A ^a   Gow, Neil A R ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFUNGAL AGENT; CELL WALL SYNTHASE INHIBITOR; CHITIN; CHS1 PROTEIN; CHS10 PROTEIN; CHS2 PROTEIN; CHS3 PROTEIN; CHS4 PROTEIN; CHS5 PROTEIN; CHS6 PROTEIN; CHS7 PROTEIN; CHS8 PROTEIN; CHS9 PROTEIN; CHSA PROTEIN; CHSB PROTEIN; CHSD PROTEIN; CHSF PROTEIN; CHSG PROTEIN; CHSMB PROTEIN; FUNGAL PROTEIN; GLUCAN SYNTHASE INHIBITOR; NIKKOMYCIN; RO 093143; UNCLASSIFIED DRUG;

ASPERGILLUS FUMIGATUS; ASPERGILLUS NIDULANS; CANDIDA ALBICANS; CRYPTOCOCCUS NEOFORMANS; FUNGUS; FUNGUS GROWTH; NONHUMAN; PATHOGENESIS; PHYCOMYCES BLAKESLEEANUS; PROTEIN SYNTHESIS; REVIEW; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION; USTILAGO MAYDIS;

ANIMALS; ANTIFUNGAL AGENTS; BETA-GLUCANS; CELL WALL; CHITIN; DRUG DESIGN; FUNGI; GENE EXPRESSION REGULATION, FUNGAL; HOST-PATHOGEN INTERACTIONS; HUMANS; MYCOSES;

FUNGI; VERTEBRATA;

EID: 77955419127     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2010.05.002     Document Type: Review

References (68)

1. Munro C.A., Gow N.A.R. Chitin synthesis in human pathogenic fungi. Med Mycol 2001, 39 S1:41-53.
2. Latge J.P. The cell wall: a carbohydrate armour for the fungal cell. Mol Microbiol 2007, 66:279-290.
3. Klis F.M., Boorsma A., De Groot P.W. Cell wall construction in Saccharomyces cerevisiae. Yeast 2006, 23:185-202.
4. Baker L.G., Specht C.A., Donlin M.J., Lodge J.K. Chitosan, the deacetylated form of chitin, is necessary for cell wall integrity in Cryptococcus neoformans. Eukaryot Cell 2007, 6:855-867.
5. Bartnicki-Garcia S. Cell wall chemistry, morphogenesis, and taxonomy of fungi. Annu Rev Microbiol 1968, 22:87-108.
6. Niño-Vega G.A., Carrero L., San-Blas G. Isolation of the CHS4 gene of Paracoccidioides brasiliensis and its accommodation in a new class of chitin synthases. Med Mycol 2004, 42:51-57.
7. Roncero C. The genetic complexity of chitin synthesis in fungi. Curr Genet 2002, 41:367-378.
8. Chigira Y., Abe K., Gomi K., Nakajima T. chsZ, a gene for a novel class of chitin synthase from Aspergillus oryzae. Curr Genet 2002, 41:261-267.
9. Choquer M., Boccara M., Goncalves I.R., Soulie M.C., Vidal-Cros A. Survey of the Botrytis cinerea chitin synthase multigenic family through the analysis of six euascomycetes genomes. Eur J Biochem 2004, 271:2153-2164.
10. Munro C.A., Winter K., Buchan A., Henry K., Becker J.M., Brown A.J., Bulawa C.E., Gow N.A.R. Chs1 of Candida albicans is an essential chitin synthase required for synthesis of the septum and for cell integrity. Mol Microbiol 2001, 39:1414-1426.
11. Bulawa C.E., Miller D.W., Henry L.K., Becker J.M. Attenuated virulence of chitin-deficient mutants of Candida albicans. Proc Natl Acad Sci U S A 1995, 92:10570-10574.
12. Sheu Y.J., Barral Y., Snyder M. Polarized growth controls cell shape and bipolar bud site selection in Saccharomyces cerevisiae. Mol Cell Biol 2000, 20:5235-5247.
13. Fischer R., Zekert N., Takeshita N. Polarized growth in fungi-interplay between the cytoskeleton, positional markers and membrane domains. Mol Microbiol 2008, 68:813-826.
14. Bulawa C.E. Genetics and molecular biology of chitin synthesis in fungi. Annu Rev Microbiol 1993, 47:505-534.
15. Spellman P.T., Sherlock G., Zhang M.Q., Iyer V.R., Anders K., Eisen M.B., Brown P.O., Botstein D., Futcher B. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell 1998, 9:3273-3297.
16. Côte P., Hogues H., Whiteway M. Transcriptional analysis of the Candida albicans cell cycle. Mol Biol Cell 2009, 20:3363-3373.
17. Walker L.A., Gow N.A.R., Munro C.A. Fungal echinocandin resistance. Fungal Genet Biol 2010, 47:117-126.
18. Garcia R., Bermejo C., Grau C., Perez R., Rodriguez-Pena J.M., Francois J., Nombela C., Arroyo J. The global transcriptional response to transient cell wall damage in Saccharomyces cerevisiae and its regulation by the cell integrity signaling pathway. J Biol Chem 2004, 279:15183-15195.
19. Bermejo C., Rodriguez E., Garcia R., Rodriguez-Pena J.M., Rodriguez de la Concepcion M.L., Rivas C., Arias P., Nombela C., Posas F., Arroyo J. The sequential activation of the yeast HOG and SLT2 pathways is required for cell survival to cell wall stress. Mol Biol Cell 2008, 19:1113-1124.
20. 2+ signalling pathways co-ordinately regulate chitin synthesis in Candida albicans. Mol Microbiol 2007, 63:1399-1413.
21. Lenardon M.D., Lesiak I., Munro C.A., Gow N.A.R. Dissection of the Candida albicans class I chitin synthase promoters. Mol Genet Genomics 2009, 281:459-471.
22. Walker L.A., Munro C.A., de Bruijn I., Lenardon M.D., McKinnon A., Gow N.A.R. Stimulation of chitin synthesis rescues Candida albicans from echinocandins. PLoS Pathog 2008, 4:e1000040.
23. 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. Antimicrob Agents Chemother 2010, 54:1555-1563.
24. Lenardon M.D., Whitton R.K., Munro C.A., Marshall D., Gow N.A.R. Individual chitin synthase enzymes synthesize microfibrils of differing structure at specific locations in the Candida albicans cell wall. Mol Microbiol 2007, 66:1164-1173.
25. Fukuda K., Yamada K., Deoka K., Yamashita S., Ohta A., Horiuchi H. Class III chitin synthase ChsB of Aspergillus nidulans localizes at the sites of polarized cell wall synthesis and is required for conidial development. Eukaryot Cell 2009, 8:945-956.
26. Blankenship J.R., Fanning S., Hamaker J.J., Mitchell A.P. An extensive circuitry for cell wall regulation in Candida albicans. PLoS Pathog 2010, 6:e1000752.
27. Teh E.M., Chai C.C., Yeong F.M. Retention of Chs2p in the ER requires N-terminal CDK1-phosphorylation sites. Cell Cycle 2009, 8:2965-2976.
28. Martinez-Rucobo F.W., Eckhardt-Strelau L., Terwisscha van Scheltinga A.C. Yeast chitin synthase 2 activity is modulated by proteolysis and phosphorylation. Biochem J 2009, 417:547-554.
29. Beltrao P., Trinidad J.C., Fiedler D., Roguev A., Lim W.A., Shokat K.M., Burlingame A.L., Krogan N.J. Evolution of phosphoregulation: comparison of phosphorylation patterns across yeast species. PLoS Biol 2009, 7:e1000134.
30. Lenardon M.D., Milne S.A., Mora-Montes H.M., Kaffarnik F.A.R., Peck S.C., Brown A.J.P., Munro C.A., Gow N.A.R. Phosphorylation regulates polarisation of chitin synthesis in Candida albicans. J Cell Sci 2010, 10.1242/jcs.060210.
31. Chuang J.S., Schekman R.W. Differential trafficking and timed localization of two chitin synthase proteins. Chs2p and Chs3p. J Cell Biol 1996, 135:597-610.
32. Bartnicki-Garcia S. Chitosomes: past, present and future. FEMS Yeast Res 2006, 6:957-965.
33. Schorr M., Then A., Tahirovic S., Hug N., Mayinger P. The phosphoinositide phosphatase Sac1p controls trafficking of the yeast Chs3p chitin synthase. Curr Biol 2001, 11:1421-1426.
34. Reyes A., Sanz M., Duran A., Roncero C. Chitin synthase III requires Chs4p-dependent translocation of Chs3p into the plasma membrane. J Cell Sci 2007, 120:1998-2009.
35. DeMarini D.J., Adams A.E., Fares H., De Virgilio C., Valle G., Chuang J.S., Pringle J.R. A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall. J Cell Biol 1997, 139:75-93.
36. Kozubowski L., Panek H., Rosenthal A., Bloecher A., DeMarini D.J., Tatchell K. A Bni4-Glc7 phosphatase complex that recruits chitin synthase to the site of bud emergence. Mol Biol Cell 2003, 14:26-39.
37. Larson J.R., Bharucha J.P., Ceaser S., Salamon J., Richardson C.J., Rivera S.M., Tatchell K. Protein phosphatase type 1 directs chitin synthesis at the bud neck in Saccharomyces cerevisiae. Mol Biol Cell 2008, 19:3040-3051.
38. Larson J.R., Kozubowski L., Tatchell K. Changes in Bni4 localization induced by cell stress in Saccharomyces cerevisiae. J Cell Sci 2010, 123:1050-1059.
39. Liu H., Kauffman S., Becker J.M., Szaniszlo P.J. Wangiella (Exophiala) dermatitidis WdChs5p, a class V chitin synthase, is essential for sustained cell growth at temperature of infection. Eukaryot Cell 2004, 3:40-51.
40. 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. Mol Microbiol 2006, 59:1380-1394.
41. Fujiwara M., Horiuchi H., Ohta A., Takagi M. A novel fungal gene encoding chitin synthase with a myosin motor-like domain. Biochem Biophys Res Commun 1997, 236:75-78.
42. Abramczyk D., Park C., Szaniszlo P.J. Cytolocalization of the class V chitin synthase in the yeast, hyphal and sclerotic morphotypes of Wangiella (Exophiala) dermatitidis. Fungal Genet Biol 2009, 46:28-41.
43. 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. Biosci Biotechnol Biochem 2009, 73:1163-1167.
44. Takeshita N., Ohta A., Horiuchi H. CsmA, a class V chitin synthase with a myosin motor-like domain, is localized through direct interaction with the actin cytoskeleton in Aspergillus nidulans. Mol Biol Cell 2005, 16:1961-1970.
45. Reid D.M., Gow N.A.R., Brown G.D. Pattern recognition: recent insights from Dectin-1. Curr Opin Immunol 2009, 21:30-37.
46. Netea M.G., Gow N.A.R., Munro C.A., Bates S., Collins C., Ferwerda G., Hobson R.P., Bertram G., Hughes H.B., Jansen T., et al. Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J Clin Invest 2006, 116:1642-1650.
47. Netea M.G., Brown G.D., Kullberg B.J., Gow N.A.R. An integrated model of the recognition of Candida albicans by the innate immune system. Nat Rev Microbiol 2008, 6:67-78.
48. Rappleye C.A., Eissenberg L.G., Goldman W.E. Histoplasma capsulatum alpha-(1,3)-glucan blocks innate immune recognition by the beta-glucan receptor. Proc Natl Acad Sci U S A 2007, 104:1366-1370.
49. Lee C.G., Da Silva C.A., Lee J.Y., Hartl D., Elias J.A. Chitin regulation of immune responses: an old molecule with new roles. Curr Opin Immunol 2008, 20:684-689.
50. Da Silva C.A., Chalouni C., Williams A., Hartl D., Lee C.G., Elias J.A. Chitin is a size-dependent regulator of macrophage TNF and IL-10 production. J Immunol 2009, 182:3573-3582.
51. Da Silva C.A., Hartl D., Liu W., Lee C.G., Elias J.A. TLR-2 and IL-17A in chitin-induced macrophage activation and acute inflammation. J Immunol 2008, 181:4279-4286.
52. Zhu Z., Zheng T., Homer R.J., Kim Y.K., Chen N.Y., Cohn L., Hamid Q., Elias J.A. Acidic mammalian chitinase in asthmatic Th2 inflammation and IL-13 pathway activation. Science 2004, 304:1678-1682.
53. Gordon-Thomson C., Kumari A., Tomkins L., Holford P., Djordjevic J.T., Wright L.C., Sorrell T.C., Moore G.P. Chitotriosidase and gene therapy for fungal infections. Cell Mol Life Sci 2009, 66:1116-1125.
54. Lee C.G. Chitin, chitinases and chitinase-like proteins in allergic inflammation and tissue remodeling. Yonsei Med J 2009, 50:22-30.
55. Reese T.A., Liang H.E., Tager A.M., Luster A.D., Van Rooijen N., Voehringer D., Locksley R.M. Chitin induces accumulation in tissue of innate immune cells associated with allergy. Nature 2007, 447:92-96.
56. de Jonge R., Thomma B.P. Fungal LysM effectors: extinguishers of host immunity?. Trends Microbiol 2009, 17:151-157.
57. Cash H.L., Whitham C.V., Behrendt C.L., Hooper L.V. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 2006, 313:1126-1130.
58. Xu X.L., Lee R.T., Fang H.M., Wang Y.M., Li R., Zou H., Zhu Y., Wang Y. Bacterial peptidoglycan triggers Candida albicans hyphal growth by directly activating the adenylyl cyclase Cyr1p. Cell Host Microbe 2008, 4:28-39.
59. Schlosser A., Thomsen T., Moeller J.B., Nielsen O., Tornoe I., Mollenhauer J., Moestrup S.K., Holmskov U. Characterization of FIBCD1 as an acetyl group-binding receptor that binds chitin. J Immunol 2009, 183:3800-3809.
60. Villiers C., Chevallet M., Diemer H., Couderc R., Freitas H., Van Dorsselaer A., Marche P.N., Rabilloud T. From secretome analysis to immunology: chitosan induces major alterations in the activation of dendritic cells via a TLR4-dependent mechanism. Mol Cell Proteomics 2009, 8:1252-1264.
61. Munro C.A., Gow N.A.R. Chitin biosynthesis as a target for antifungals. Antifungal Agents: Discovery and Mode of Action 1995, 161-171. Bios Scientific. G.K. Dixon, L.G. Copping, D.W. Hollomon (Eds.).
62. 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. J Bacteriol 1994, 176:5857-5860.
63. Sudoh M., Yamazaki T., Masubuchi K., Taniguchi M., Shimma N., Arisawa M., Yamada-Okabe H. Identification of a novel inhibitor specific to the fungal chitin synthase. Inhibition of chitin synthase 1 arrests the cell growth, but inhibition of chitin synthase 1 and 2 is lethal in the pathogenic fungus Candida albicans. J Biol Chem 2000, 275:32901-32905.
64. Carotti C., Ferrario L., Roncero C., Valdivieso M.H., Duran A., Popolo L. Maintenance of cell integrity in the gas1 mutant of Saccharomyces cerevisiae requires the Chs3p-targeting and activation pathway and involves an unusual Chs3p localization. Yeast 2002, 19:1113-1124.
65. 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. Eukaryot Cell 2003, 2:1200-1210.
66. Cota J.M., Grabinski J.L., Talbert R.L., Burgess D.S., Rogers P.D., Edlind T.D., Wiederhold N.P. Increases in SLT2 expression and chitin content are associated with incomplete killing of Candida glabrata by caspofungin. Antimicrob Agents Chemother 2008, 52:1144-1146.
67. Fortwendel J.R., Juvvadi P.R., Pinchai N., Perfect B.Z., Alspaugh J.A., Perfect J.R., Steinbach W.J. Differential effects of inhibiting chitin and 1,3-(beta)-d-glucan synthesis in ras and calcineurin mutants of Aspergillus fumigatus. Antimicrob Agents Chemother 2009, 53:476-482.
68. Steinbach W.J., Reedy J.L., Cramer R.A., Perfect J.R., Heitman J. Harnessing calcineurin as a novel anti-infective agent against invasive fungal infections. Nat Rev Microbiol 2007, 5:418-430.