Effect of cell wall integrity stress and RlmA transcription factor on asexual development and autolysis in Aspergillus nidulans

Fungal Genetics and Biology

Volumn 54, Issue , 2013, Pages 1-14

  Kovács, Zsuzsanna ^a   Szarka, Máté ^a   Kovács, Szilvia ^a   Boczonádi, Imre ^a   Emri, Tamás ^a   Abe, Keietsu ^b   Pócsi, István ^a   Pusztahelyi, Tünde ^a  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

Aspergillus nidulans; Autolysis; Cell wall; Cell wall integrity; Conidiophore; Oxidative stress

Indexed keywords

BIOPOLYMER; CHITINASE; CONGO RED; GLUCAN GLUCOSIDASE; RLMA PROTEIN; SWI4 PROTEIN; SWI6 PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; ASEXUAL DEVELOPMENT; ASPERGILLUS NIDULANS; AUTOLYSIS; BIOSYNTHESIS; BRLA GENE; CELL STRESS; CELL WALL; CHIA GENE; CHIB GENE; COMPUTER ANALYSIS; CONIDIOPHORE; CONTROLLED STUDY; ENGA GENE; FUNGAL GENE; FUNGUS GROWTH; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC ANALYSIS; HYDROLYSIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RLMA GENE; SRRA GENE; UGMA GENE;

ASPERGILLUS NIDULANS; AUTOLYSIS; CELL WALL; CHITINASE; CONGO RED; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; REPRODUCTION, ASEXUAL; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

EMERICELLA NIDULANS;

EID: 84877050409     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2013.02.004     Document Type: Article

References (62)

1. Adams D.J. Fungal cell wall chitinases and glucanases. Microbiology 2004, 150:2029-2035.
2. Adams T.H., Weiser J.K., Yu J.H. Asexual sporulation in Aspergillus nidulans. Microbiol. Mol. Biol. Rev. 1998, 62:35-54.
3. Arnaud M.B., Chibucos M.C., Costanzo M.C., Crabtree J., Inglis D.O., Lotia A., Orvis J., Shah P., Skrzypek M.S., Binkley G., Miyasato S.R., Wortman J.R., Sherlock G. The Aspergillus Genome Database, a curated comparative genomics resource for gene, protein and sequence information for the Aspergillus research community. Nucleic Acids Res. 2010, 38:D420-D427.
4. Baetz K., Moffat J., Haynes J., Chang M., Andrews B. Transcriptional coregulation by the cell integrity mitogen-activated protein kinase Slt2 and the cell cycle regulator Swi4. Mol. Cell. Biol. 2001, 21:6515-6528.
5. Barratt R.W., Johnson G.B., Ogata W.N. Wild-type and mutant stocks of Aspergillus nidulans. Genetics 1965, 52:233-246.
6. Bartnicki-Garcia S., Persson J., Chanzy H. An electron microscope and electron diffraction study of the effect of calcofluor and Congo red on the biosynthesis of chitin in vitro. Arch. Biochem. Biophys. 1994, 310:6-15.
7. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
8. Bussink H.J., Osmani S.A. A mitogen-activated protein kinase (MPKA) is involved in polarized growth in the filamentous fungus, Aspergillus nidulans. FEMS Microbiol. Lett. 1999, 173:117-125.
9. Carbon S., Ireland A., Mungall C.J., Shu S., Marshall B., Lewis S., AmiGO Hub, Web Presence Working Group AmiGO: online access to ontology and annotation data. Bioinformatics 2009, 25:288-289.
10. Choi C.J., Ju H.J., Park B.H., Qin R., Jahng K.Y., Han D.M., Chae K.S. Isolation and characterization of the Aspergillus nidulans eglC gene encoding a putative beta-1,3-endoglucanase. Fungal Genet. Biol. 2005, 42:590-600.
11. Chomczynski P. A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. BioTechniques 1993, 15:532-536.
12. Damveld R.A., Arentshorst M., Franken A., vanKuyk P.A., Klis F.M., van den Hondel C.A., Ram A.F. The Aspergillus niger MADS-box transcription factor RlmA is required for cell wall reinforcement in response to cell wall stress. Mol. Microbiol. 2005, 58:305-319.
13. de Groot P.W., Brandt B.W., Horiuchi H., Ram A.F., de Koster C.G., Klis F.M. Comprehensive genomic analysis of cell wall genes in Aspergillus nidulans. Fungal Genet. Biol. 2009, 46(Suppl. 1):S72-S81.
14. Dodou E., Treisman R. The Saccharomyces cerevisiae MADS-box transcription factor Rlm1 is a target for the Mpk1 mitogen-activated protein kinase pathway. Mol. Cell. Biol. 1997, 17:1848-1859.
15. Emri T., Molnár Z., Pusztahelyi T., Pócsi I. Physiological and morphological changes in autolyzing Aspergillus nidulans cultures. Folia Microbiol. 2004, 49:277-284.
16. Emri T., Molnár Z., Pusztahelyi T., Varecza Z., Pócsi I. The fluG-BrlA pathway contributes to the initialization of autolysis in submerged Aspergillus nidulans cultures. Mycol. Res. 2005, 109:757-763.
17. Emri T., Molnár Z., Veres T., Pusztahelyi T., Dudás G., Pócsi I. Glucose-mediated repression of autolysis and conidiogenesis in Emericella nidulans. Mycol. Res. 2006, 110:1172-1178.
18. Emri T., Molnár Z., Szilágyi M., Pócsi I. Regulation of autolysis in Aspergillus nidulans. Appl. Biochem. Biotechnol. 2008, 151:211-220.
19. Erdei é., Pusztahelyi T., Miskei M., Barna T., Pócsi I. Characterization and heterologous expression of an age-dependent fungal/bacterial type chitinase of Aspergillus nidulans. Acta Microbiol. Immunol. Hung. 2008, 55:351-361.
20. Extebeste O., Garzia A., Espeso E.A., Ugalde U. Aspergillus nidulans asexual development: making the most of cellular modules. Trends Microbiol. 2010, 18:569-576.
21. Fontaine T., Simenel C., Dubreucq G., Adam O., Delepierre M., Lemoine J., Vorgias C.E., Diaquin M., Latge J.P. Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. J. Biol. Chem. 2000, 275:27594-27607.
22. Fuchs B.B., Mylonakis E. Our paths might cross: the role of the fungal cell wall integrity pathway in stress response and cross talk with other stress response pathways. Eukaryot. Cell 2009, 8:1616-1625.
23. Fujioka T., Mizutani O., Furukawa K., Sato N., Yoshimi A., Yamagata Y., Nakajima T., Abe K. MpkA-dependent and -independent cell wall integrity signaling in Aspergillus nidulans. Eukaryotic Cell 2007, 6:1497-1510.
24. Furukawa K., Katsuno Y., Urao T., Yabe T., Yamada-Okabe T., Yamada-Okabe H., Yamagata Y., Abe K., Nakajima T. Isolation and functional analysis of a gene, tcsB, encoding a transmembrane hybrid type histidine kinase from Aspergillus nidulans. Appl. Environ. Microbiol. 2002, 68:5304-5310.
25. García R., Bermejo C., Grau C., Perez R., Rodríguez-Peña 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.
26. Garcia-Rodriguez L.J., Durán A., Roncero C. 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. 2000, 182:2428-2437.
27. Gomi K., Iimura Y., Hara S. Integrative transformation of Aspergillus oryzae with a plasmid containing the Aspergillus nidulans argB gene. Agric. Biol. Chem. 1987, 51:2549-2555.
28. Hagiwara D., Asano Y., Marui J., Furukawa K., Kanamaru K., Kato M., Abe K., Kobayashi T., Yamashino T., Mizuno T. The SskA and SrrA response regulators are implicated in oxidative stress responses of hyphae and asexual spores in the phosphorelay signaling network of Aspergillus nidulans. Biosci. Biotechnol. Biochem. 2007, 71:1003-1014.
29. Igual J.C., Johnson A.L., Johnston L.H. 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. 1996, 15:5001-5013.
30. Iyer V.R., Horak C.E., Scafek C.S., Botsteink D., Snyder M., Brown P.O. Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature 2001, 409:533-538.
31. Jung U.S., Levin D.E. Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signaling pathway. Mol. Microbiol. 1999, 34:1049-1057.
32. Kim S., Matsuo I., Ajisaka K., Nakajima H., Kitamoto K. Cloning and characterization of the nagA gene that encodes beta-N-acetylglucosaminidase from Aspergillus nidulans and its expression in Aspergillus oryzae. Biosci. Biotechnol. Biochem. 2002, 66:2168-2175.
33. Kopecka M., Gabriel M. The influence of Congo Red on the cell wall and (1-3) β-d-glucan in Saccharomyces cerevisiae. Arch. Microbiol. 1992, 158:115-126.
34. Lagorce A., Hauser N.C., Labourdette D., Rodriguez C., Martin-Yken H., Arroyo J., Hoheisel J.D., Francois J. Genome-wide analysis of the response to cell wall mutations in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 2003, 278:20345-20357.
35. Leary N.O., Pembroke A., Duggan P.F. Improving accuracy of glucose oxidase procedure for glucose determinations on discrete analyzers. Clin. Chem. 1992, 38:298-302.
36. Lee H.U., Park J.B., Lee H., Chae K.S., Han D.M., Jahng K.Y. Predicting the chemical composition and structure of Aspergillus nidulans hyphal wall surface by atomic force microscopy. J. Microbiol. 2010, 48:243-248.
37. -) of Aspergillus fumigatus. Fungal Genet. Biol. 2003, 38:98-109.
38. Miskei M., Karányi Z., Pócsi I. Annotation of stress-response proteins in the aspergilli. Fungal Genet. Biol. 2009, 46:S105-S120.
39. Ogawa K., Hatano M. Circular dichroism of the complex of a (1-3)-β-d-glucan with Congo Red. Carbohydr. Res. 1978, 67:527-535.
40. Pancaldi S., Poli F., Dall'Olio G., Vannini G.L. Morphological anomalies induced by Congo Red in Aspergillus niger. Arch. Microbiol. 1984, 137:185-187.
41. Pócsi I., Pusztahelyi T., Bogáti M.S., Szentirmai A. The formation of N-acetyl-ß-d-hexosaminidase is repressed by glucose in Penicillium chrysogenum. J. Basic Microbiol. 1993, 33:259-267.
42. 2 and menadione exposed Aspergillus nidulans cultures - linking genome-wide transcriptional changes to cellular physiology. BMC Genom. 2005, 6. Article No. 182.
43. Pócsi I., Leiter E., Kwon N.J., Shin K.S., Kwon G.S., Pusztahelyi T., Emri T., Abuknesha R.A., Price R.G., Yu J.H. Asexual sporulation signaling regulates autolysis of Aspergillus nidulans via modulating the chitinase ChiB production. J. Appl. Microbiol. 2009, 107:514-523.
44. Pusztahelyi T., Pócsi I., Szentirmai A. Aging of Penicillium chrysogenum cultures under carbon starvation: II. Protease and N-acetyl-β-d-hexosaminidase production. Biotechnol. Appl. Biochem. 1997, 25:87-93.
45. Pusztahelyi T., Molnár Z., Emri T., Klement E., Miskei M., Kerékgyártó J., Balla J., Pócsi I. Comparative studies of differential expression of chitinolytic enzymes encoded by chiA, chiB, chiC and nagA genes in Aspergillus nidulans. Folia Microbiol. 2006, 51:547-554.
46. Ram A.F.J., Arentshorst M., Damveld R.A., vanKuyk P.A., Klis F.M., van den Hondel C.A.M.J.J. The cell wall stress response in Aspergillus niger involves increased expression of the glutamine: fructose-6-phosphate amidotransferase-encoding gene (gfaA) and increased deposition of chitin in the cell wall. Microbiology 2004, 150:3315-3326.
47. Roemer T., Paáravicini G., Payton M.A., Bussey H. Characterization of the yeast (1-6)-beta-glucan biosynthetic components, Kre6p and Skn1p, and genetic interactions between the PKC1 pathway and extracellular matrix assembly. J. Cell Biol. 1994, 127:567-579.
48. Roncero C., Duran A. Effect of Calcofluor white and Congo red on fungal wall morphogenesis: in vivo activation of chitin polymerization. J. Bacteriol. 1985, 163:1180-1185.
49. Sato I., Shimizu M., Hoshino T., Takaya N. The glutathione system of Aspergillus nidulans involves a fungus-specific glutathione S-transferase. J. Biol. Chem. 2009, 284:8042-8053.
50. T method. Nat. Prot. 2008, 3:1101-1108.
51. Shamrock V.J., Duval J.F.L., Lindsey G.G., Gaboriaud F. The role of the heat shock protein Hsp12p in the dynamic response of Saccharomyces cerevisiae to the addition of Congo red. FEMS Yeast Res. 2009, 9:391-399.
52. 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. Antimicrob. Agents Chemother. 2006, 50:3160-3161.
53. Szilágyi M., Kwon N.J., Dorogi C., Pócsi I., Yu J.H., Emri T. The extracellular β-1,3-endoglucanase EngA is involved in autolysis of Aspergillus nidulans. J. Appl. Microbiol. 2010, 109:1498-1508.
54. Takahashi T., Hatamoto O., Koyama Y., Abe K. Efficient gene disruption in the koji-mold Aspergillus sojae using a novel variation of the positive-negative method. Mol. Genet. Genom. 2004, 272:344-352.
55. Takaya N., Yamazaki D., Horiuchi H., Ohta A., Takagi M. Cloning and characterization of a chitinase-encoding gene (chiA) from Aspergillus nidulans, disruption of which decreases germination frequency and hyphal growth. Biosci. Biotechnol. Biochem. 1998, 62:60-65.
56. Valiante V., Heinekamp T., Jain R., Härtl A., Brakhage A.A. The mitogen-activated protein kinase MpkA of Aspergillus fumigatus regulates cell wall signaling and oxidative stress response. Fungal Genet. Biol. 2008, 45:618-627.
57. Valiante V., Jain R., Heinekamp T., Brakhage A.A. The MpkA MAP kinase module regulates cell wall integrity signaling and pyomelanin formation in Aspergillus fumigatus. Fungal Genet. Biol. 2009, 46:909-918.
58. Vannini G.L., Poli F., Donini A., Pancaldi S. Effects of Congo Red on wall synthesis and morphogenesis in Saccharomyces cerevisiae. Plant Sci. Lett. 1983, 31:9-17.
59. Vargas-Pérez I., Sánchez O., Kawasaki L., Georgellis D., Aguirre J. Response regulators SrrA and SskA are central components of a phosphorelay system involved in stress signal transduction and asexual sporulation in Aspergillus nidulans. Eukaryotic Cell 2007, 6:1570-1583.
60. Watanabe Y., Takaesu G., Hagiwara M., Irie K., Matsumoto K. Characterization of a serum response factor-like protein in Saccharomyces cerevisiae, Rlm1, which has transcriptional activity regulated by the Mpk1 (Slt2) mitogen-activated protein kinase pathway. Mol. Cell. Biol. 1997, 17:2615-2623.
61. Yamazaki H., Yamazaki D., Takaya N., Takagi M., Ohta A., Horiuchi H. A chitinase gene, chiB, involved in the autolytic process of Aspergillus nidulans. Curr. Genet. 2007, 51:89-98.
62. Yamazaki H., Tanaka A., Kaneko J., Ohta A., Horiuchi H. Aspergillus nidulans ChiA is a glycosylphosphatidylinositol (GPI)-anchored chitinase specifically localized at polarized growth sites. Fungal Genet. Biol. 2008, 45:963-972.