Protein kinase C regulates the expression of cell wall-related genes in RlmA-dependent and independent manners in Aspergillus nidulans

References

• Latgé JP. The cell wall: a carbohydrate armour for the fungal cell. Mol. Microbiol. 2007;66:279–290.10.1111/mmi.2007.66.issue-2
   PubMed Web of Science ®Google Scholar
• de Groot PW, Brandt BW, Horiuchi H, Ram AF, de Koster CG, Klis FM. Comprehensive genomic analysis of cell wall genes in Aspergillus nidulans. Fungal Genet. Biol. 2009;46:S72–S81.10.1016/j.fgb.2008.07.022
   Google Scholar
• Horiuchi H. Functional diversity of chitin synthases of Aspergillus nidulans in hyphal growth, conidiophore development and septum formation. Med. Mycol. 2009;47:S47–S52.10.1080/13693780802213332
   PubMed Web of Science ®Google Scholar
• 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. Eukaryot. Cell. 2009;6:1497–1510.
   Web of Science ®Google Scholar
• Yoshimi A, Sano M, Inaba A, Kokubun Y, Fujioka T, Mizutani O, Hagiwara D, Fujikawa T, Nishimura M, Yano S, Kasahara S, Shimizu K, Yamaguchi M, Kawakami K, Abe K. Functional analysis of the α-1,3-glucan synthase genes agsA and agsB in Aspergillus nidulans: AgsB is the major α-1,3-glucan synthase in this fungus. PLoS ONE. 2013;8:e54893.10.1371/journal.pone.0054893
   PubMedGoogle Scholar
• Firon A, Beauvais A, Latgé JP, Couvé E, Grosjean-Cournoyer MC, D’Enfert C. Characterization of essential genes by parasexual genetics in the human fungal pathogen Aspergillus fumigatus: impact of genomic rearrangements associated with electroporation of DNA. Genetics. 2002;161:1077–1087.
   PubMed Web of Science ®Google Scholar
• Yanai K, Kojima N, Takaya N, Horiuchi H, Ohta A, Takagi M. Isolation and characterization of two chitin synthase genes from Aspergillus nidulans. Biosci. Biotechnol. Biochem. 1994;58:1828–1835.10.1271/bbb.58.1828
   PubMed Web of Science ®Google Scholar
• Borgia PT, Iartchouk N, Riggle PJ, Winter KR, Koltin Y, Bulawa CE. The chsB gene of Aspergillus nidulans is necessary for normal hyphal growth and development. Fungal Genet. Biol. 1996;20:193–203.10.1006/fgbi.1996.0035
   PubMed Web of Science ®Google Scholar
• 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;8:945–956.10.1128/EC.00326-08
   PubMed Web of Science ®Google Scholar
• Ichinomiya M, Motoyama T, Fujiwara M, Takagi M, Horiuchi H, Ohta A. Repression of chsB expression reveals the functional importance of class IV chitin synthase gene chsD in hyphal growth and conidiation of Aspergillus nidulans. Microbiology. 2002;148:1335–1347.
   PubMed Web of Science ®Google Scholar
• Takeshita N, Ohta A, Horiuchi H. csmA, a gene encoding a class V chitin synthase with a myosin motor-like domain of Aspergillus nidulans, is translated as a single polypeptide and regulated in response to osmotic conditions. Biochem. Biophys. Res. Commun. 2002;298:103–109.10.1016/S0006-291X(02)02418-X
   PubMed Web of Science ®Google Scholar
• 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;59:1380–1394.10.1111/j.1365-2958.2006.05030.x
   PubMed Web of Science ®Google Scholar
• Fujiwara M, Ichinomiya M, Motoyama T, Horiuchi H, Ohta A, Takagi M. Evidence that the Aspergillus nidulans class I and II chitin synthase genes, chsC and chsA, share critical roles in hyphal wall integrity and conidiophore development. J. Biochem. 2000;127:359–366.10.1093/oxfordjournals.jbchem.a022616
   PubMed Web of Science ®Google Scholar
• Ichinomiya M, Yamada E, Yamashita S, Ohta A, Horiuchi H. Class I and class II chitin synthases are involved in septum formation in the filamentous fungus Aspergillus nidulans. Eukaryot. Cell. 2005;4:1125–1136.10.1128/EC.4.6.1125-1136.2005
   PubMed Web of Science ®Google Scholar
• Levin DE. Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 2005;69:262–291.10.1128/MMBR.69.2.262-291.2005
   PubMed Web of Science ®Google Scholar
• Levin DE. Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics. 2011;189:1145–1175.10.1534/genetics.111.128264
   PubMed Web of Science ®Google Scholar
• Jung US, Levin DE. Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signalling pathway. Mol. Microbiol. 1999;34:1049–1057.10.1046/j.1365-2958.1999.01667.x
   PubMed Web of Science ®Google Scholar
• Ichinomiya M, Uchida H, Koshi Y, Ohta A, Horiuchi H. A protein kinase C-encoding gene, pkcA, is essential to the viability of the filamentous fungus Aspergillus nidulans. Biosci. Biotechnol. Biochem. 2007;71:2787–2799.10.1271/bbb.70409
   PubMed Web of Science ®Google Scholar
• Ronen R, Sharon H, Levdansky E, Romano J, Shadkchan Y, Osherov N. The Aspergillus nidulans pkcA gene is involved in polarized growth, morphogenesis and maintenance of cell wall integrity. Curr. Genet. 2007;51:321–329.10.1007/s00294-007-0129-y
   PubMed Web of Science ®Google Scholar
• Teepe AG, Loprete DM, He Z, Hoggard TA, Hill TW. The protein kinase C orthologue PkcA plays a role in cell wall integrity and polarized growth in Aspergillus nidulans. Fungal Genet. Biol. 2007;44:554–562.10.1016/j.fgb.2006.10.001
   PubMed Web of Science ®Google Scholar
• Herrmann M, Spröte P, Brakhage AA. Protein kinase C (PkcA) of Aspergillus nidulans is involved in penicillin production. Appl. Environ. Microbiol. 2006;72:2957–2970.10.1128/AEM.72.4.2957-2970.2006
   PubMed Web of Science ®Google Scholar
• Chellegatti MA, Yuvamoto PD, Said S. Role of phospholipase C and protein kinase C in Aspergillus nidulans during growth on pectin or glucose: effects on germination and duplication cycle. Folia Microbiol. 2010;55:228–232.10.1007/s12223-010-0033-6
   PubMed Web of Science ®Google Scholar
• Colabardini AC, de Castro PA, de Gouvêa PF, Savoldi M, Malavazi I, Goldman MH, Goldman GH. Involvement of the Aspergillus nidulans protein kinase C with farnesol tolerance is related to the unfolded protein response. Mol. Microbiol. 2010;78:1259–1279.10.1111/j.1365-2958.2010.07403.x
   PubMed Web of Science ®Google Scholar
• Katayama T, Uchida H, Ohta A, Horiuchi H. Involvement of protein kinase C in the suppression of apoptosis and in polarity establishment in Aspergillus nidulans under conditions of heat stress. PLoS ONE. 2012;7:e50503.10.1371/journal.pone.0050503
   Google Scholar
• Futagami T, Seto K, Kajiwara Y, Takashita H, Omori T, Takegawa K, Goto M. The putative stress sensor protein MtlA is required for conidia formation, cell wall stress tolerance, and cell wall integrity in Aspergillus nidulans. Biosci. Biotechnol. Biochem. 2014;78:326–335.10.1080/09168451.2014.878218
   PubMed Web of Science ®Google Scholar
• Rowlands RT, Turner G. Nuclear and extranuclear inheritance of oligomycin resistance in Aspergillus nidulans. Mol. Gen. Genet. 1973;126:201–216.10.1007/BF00267531
   PubMedGoogle Scholar
• Yu JH, Hamari Z, Han KH, Seo JA, Reyes-Domínguez Y, Scazzocchio C. Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet. Biol. 2004;41:973–981.10.1016/j.fgb.2004.08.001
   PubMed Web of Science ®Google Scholar
• Oakley CE, Weil CF, Kretz PL, Oakley BR. Cloning of the riboB locus of Aspergillus nidulans. Gene. 1987;53:293–298.10.1016/0378-1119(87)90019-9
   PubMed Web of Science ®Google Scholar
• Horiuchi H, Fujiwara M, Yamashita S, Ohta A, Takagi M. 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. 1999;181:3721–3729.
   PubMed Web of Science ®Google Scholar
• Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–685.10.1038/227680a0
   PubMed Web of Science ®Google Scholar
• Watanabe M, Chen CY, Levin DE. Saccharomyces cerevisiae PKC1 encodes a protein kinase C (PKC) homolog with a substrate specificity similar to that of mammalian PKC. J. Biol. Chem. 1994;269:16829–16836.
   PubMed Web of Science ®Google Scholar
• Kovács Z, Szarka M, Kovács S, Boczonádi I, Emri T, Abe K, Pócsi I, Pusztahelyi T. Effect of cell wall integrity stress and RlmA transcription factor on asexual development and autolysis in Aspergillus nidulans. Fungal Genet. Biol. 2013;54:1–14.10.1016/j.fgb.2013.02.004
   PubMed Web of Science ®Google Scholar
• Nonaka H, Tanaka K, Hirano H, Fujiwara T, Kohno H, Umikawa M, Mino A, Takai Y. A downstream target of RHO1 small GTP-binding protein is PKC1, a homolog of protein kinase C, which leads to activation of the MAP kinase cascade in Saccharomyces cerevisiae. EMBO J. 1995;14:5931–5938.
   PubMed Web of Science ®Google Scholar
• Schmitz HP, Jöckel J, Block C, Heinisch JJ. Domain shuffling as a tool for investigation of protein function: substitution of the cysteine-rich region of Raf kinase and PKC η for that of yeast Pkc1p. J. Mol. Biol. 2001;311:1–7.10.1006/jmbi.2001.4848
   PubMed Web of Science ®Google Scholar
• Schmitz HP, Heinisch JJ. Evolution, biochemistry and genetics of protein kinase C in fungi. Curr. Genet. 2003;43:245–254.10.1007/s00294-003-0403-6
   PubMed Web of Science ®Google Scholar
• Han KH, Prade RA. Osmotic stress-coupled maintenance of polar growth in Aspergillus nidulans. Mol. Microbiol. 2002;43:1065–1078.10.1046/j.1365-2958.2002.02774.x
   PubMed Web of Science ®Google Scholar
• Fortwendel JR, Juvvadi PR, Perfect BZ, Rogg LE, Perfect JR, Steinbach WJ. Transcriptional regulation of chitin synthases by calcineurin controls paradoxical growth of Aspergillus fumigatus in response to caspofungin. Antimicrob. Agents Chemother. 2010;54:1555–1563.10.1128/AAC.00854-09
   PubMed Web of Science ®Google Scholar
• Pinchai N, Perfect BZ, Juvvadi PR, Fortwendel JR, Cramer RA Jr, Asfaw YG, Heitman J, Perfect JR, Steinbach WJ. Aspergillus fumigatus calcipressin cbpa is involved in hyphal growth and calcium homeostasis. Eukaryot. Cell. 2009;8:511–519.10.1128/EC.00336-08
   PubMed Web of Science ®Google Scholar
• Hagiwara D, Kondo A, Fujioka T, Abe K. Functional analysis of C2H2 zinc finger transcription factor CrzA involved in calcium signaling in Aspergillus nidulans. Curr. Genet. 2008;54:325–338.10.1007/s00294-008-0220-z
   PubMed Web of Science ®Google Scholar
• Yamada E, Ichinomiya M, Ohta A, Horiuchi H. The class V chitin synthase gene csmA is crucial for the growth of the chsA chsC double mutant in Aspergillus nidulans. Biosci. Biotechnol. Biochem. 2005;69:87–97.10.1271/bbb.69.87
   PubMed Web of Science ®Google Scholar
• 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;16:1961–1970.10.1091/mbc.E04-09-0761
   PubMed Web of Science ®Google Scholar
• 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;73:1163–1167.10.1271/bbb.90074
   PubMed Web of Science ®Google Scholar
• Tsuizaki M, Ohta A, Horiuchi H. Myosin motor-like domain of class VI chitin synthase CsmB of Aspergillus nidulans is not functionally equivalent to that of class V chitin synthase CsmA. Biosci. Biotechnol. Biochem. 2013;77:369–374.
   PubMed Web of Science ®Google Scholar
• Mellado E, Dubreucq G, Mol P, Sarfati J, Paris S, Diaquin M, Holden DW, Rodriguez-Tudela JL, Latgé JP. Cell wall biogenesis in a double chitin synthase mutant (chsG-/chsE-) of Aspergillus fumigatus. Fungal Genet. Biol. 2003;38:98–109.10.1016/S1087-1845(02)00516-9
   PubMed Web of Science ®Google Scholar
• Damveld RA, vanKuyk PA, Arentshorst M, Klis FM, van den Hondel CA, Ram AF. Expression of agsA, one of five 1,3-α-D-glucan synthase-encoding genes in Aspergillus niger, is induced in response to cell wall stress. Fungal Genet. Biol. 2005;42:165–177.10.1016/j.fgb.2004.11.006
   PubMed Web of Science ®Google Scholar