Skip to main content

Advertisement

SpringerLink
Log in

The CreB deubiquitinating enzyme does not directly target the CreA repressor protein in Aspergillus nidulans

  • Original Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

Ubiquitination/deubiquitination pathways are now recognized as key components of gene regulatory mechanisms in eukaryotes. The major transcriptional repressor for carbon catabolite repression in Aspergillus nidulans is CreA, and mutational analysis led to the suggestion that a regulatory ubiquitination/deubiquitination pathway is involved. A key unanswered question is if and how this pathway, comprising CreB (deubiquitinating enzyme) and HulA (ubiquitin ligase) and other proteins, is involved in the regulatory mechanism. Previously, missense alleles of creA and creB were analysed for genetic interactions, and here we extended this to complete loss-of-function alleles of creA and creB, and compared morphological and biochemical phenotypes, which confirmed genetic interaction between the genes. We investigated whether CreA, or a protein in a complex with it, is a direct target of the CreB deubiquitination enzyme, using co-purifications of CreA and CreB, first using strains that overexpress the proteins and then using strains that express the proteins from their native promoters. The Phos-tag system was used to show that CreA is a phosphorylated protein, but no ubiquitination was detected using anti-ubiquitin antibodies and Western analysis. These findings were confirmed using mass spectrometry, which confirmed that CreA was differentially phosphorylated but not ubiquitinated. Thus, CreA is not a direct target of CreB, and nor are proteins that form part of a stable complex with CreA a target of CreB. These results open up new questions regarding the molecular mechanism of CreA repressing activity, and how the ubiquitination pathway involving CreB interacts with this regulatory network.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Arst HNJ (1981) Aspects of the control of gene expression in fungi. In: Glover SW, Hopwood DA (eds) Symposium of the society for general microbiology, pp 131–160

  • Arst HN, Cove DJ (1973) Nitrogen metabolite repression in Aspergillus nidulans. Mol Gen Genet 126:111–141. doi:10.1007/bf00330988

    Article  CAS  PubMed  Google Scholar 

  • Arst HN, Tollervey D, Dowzer CE, Kelly JM (1990) An inversion truncating the creA gene of Aspergillus nidulans results in carbon catabolite derepression. Mol Microbiol 4:851–854

    Article  CAS  PubMed  Google Scholar 

  • Bailey C, Arst HN (1975) Carbon catabolite repressionin Aspergillus nidulans. Eur J Biochem 51:573–577. doi:10.1111/j.1432-1033.1975.tb03958.x

    Article  CAS  PubMed  Google Scholar 

  • Bayram O, Bayram OS, Valerius O, Johnk B, Braus GH (2012) Identification of protein complexes from filamentous fungi with tandem affinity purification. Methods Mol Biol (Clifton, NJ) 944. doi:10.1007/978-1-62703-122-6_14

  • Boase NA, Kelly JM (2004) A role for creD, a carbon catabolite repression gene from Aspergillus nidulans, in ubiquitination. Mol Microbiol 53:929–940. doi:10.1111/j.1365-2958.2004.04172.x

    Article  CAS  PubMed  Google Scholar 

  • Boase NA, Lockington RA, Adams JRJ, Rodbourn L, Kelly JM (2003) Molecular characterization and analysis of the acrB gene of Aspergillus nidulans: a gene identified by genetic interaction as a component of the regulatory network that includes the CreB deubiquitination enzyme. Genetics 164:95–104

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brosch G, Loidl P, Graessle S (2008) Histone modifications and chromatin dynamics: a focus on filamentous fungi. FEMS Microbiol Rev 32:409–439. doi:10.1111/j.1574-6976.2007.00100.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown NA, de Gouvea PF, Krohn NG, Savoldi M, Goldman GH (2013) Functional characterisation of the non-essential protein kinases and phosphatases regulating Aspergillus nidulans hydrolytic enzyme production. Biotechnol Biofuels 6. doi:10.1186/1754-6834-6-91

  • Chen X, Zhang B, Fischer JA (2002) A specific protein substrate for a deubiquitinating enzyme: liquid facets is the substrate of fat facets. Genes Dev 16:289–294. doi:10.1101/gad.961502

    Article  PubMed  PubMed Central  Google Scholar 

  • Chu X-L, Feng M-G, Ying S-H (2016) Qualitative ubiquitome unveils the potential significances of protein lysine ubiquitination in hyphal growth of Aspergillus nidulans. Curr Genet 62:191–201. doi:10.1007/s00294-015-0517-7

    Article  CAS  PubMed  Google Scholar 

  • Cove DJ (1966) Induction and repression of nitrate reductase in fungus Aspergillus nidulans. Biochim Biophys Acta, pp 51–56

  • Cziferszky A, Mach RL, Kubicek CP (2002) Phosphorylation positively regulates DNA binding of the carbon catabolite repressor Cre1 of Hypocrea jecorina (Trichoderma reesei). J Biol Chem 277:14688–14694. doi:10.1074/jbc.M200744200

    Article  CAS  PubMed  Google Scholar 

  • Cziferszky A, Seiboth B, Kubicek CP (2003) The Snf1 kinase of the filamentous fungus Hypocrea jecorina phosphorylates regulation-relevant serine residues in the yeast carbon catabolite repressor Mig1 but not in the filamentous fungal counterpart Cre1. Fungal Genet Biol 40:166–175. doi:10.1016/s1087-1845(03)00082-3

    Article  CAS  PubMed  Google Scholar 

  • DeVit MJ, Johnston M (1999) The nuclear exportin Msn5 is required for nuclear export of the Mig1 glucose repressor of Saccharomyces cerevisiae. Curr Biol 9:1231–1241. doi:10.1016/s0960-9822(99)80503-x

    Article  CAS  PubMed  Google Scholar 

  • DeVit MJ, Waddle JA, Johnston M (1997) Regulated nuclear translocation of the Mig1 glucose repressor. Mol Biol Cell 8:1603–1618

    Article  CAS  Google Scholar 

  • Dowzer CEA, Kelly JM (1989) Cloning of the creA gene from Aspergillus nidulans—a gene involved in carbon catabolite repression. Curr Genet 15:457–459. doi:10.1007/bf00376804

    Article  CAS  PubMed  Google Scholar 

  • Dowzer CEA, Kelly JM (1991) Analysis of the creA gene, a regulator of carbon catabolite repression in Aspergillus nidulans. Mol Cell Biol 11:5701–5709. doi:10.1128/MCB.11.11.5701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edmondson DG, Smith MM, Roth SY (1996) Repression domain of the yeast global repressor Tup1 interacts directly with histones H3 and H4. Genes Dev 10:1247–1259. doi:10.1101/gad.10.10.1247

    Article  CAS  PubMed  Google Scholar 

  • Emre NCT, Ingvarsdottir K, Wyce A, Wood A, Krogan NJ, Henry KW, Li KQ, Marmorstein R, Greenblatt JF, Shilatifard A, Berger SL (2005) Maintenance of low histone ubiquitylation by Ubp10 correlates with telomere-proximal Sir2 association and gene silencing. Mol Cell 17:585–594. doi:10.1016/j.molcel.2005.01.007

    Article  CAS  PubMed  Google Scholar 

  • Espeso EA, Fernandezcanon JM, Penalva MA (1995) Carbon regulation of penicillin biosynthesis in Aspergillus nidulans—a minor effect of mutations in creB and creC. FEMS Microbiol Lett 126:63–67. doi:10.1111/j.1574-6968.1995.tb07391.x

    Article  CAS  PubMed  Google Scholar 

  • Flipphi M, van de Vondervoort PJI, Ruijter GJG, Visser J, Arst HN, Felenbok A (2003) Onset of carbon catabolite repression in Aspergillus nidulans—parallel involvement of hexokinase and glucokinase in sugar signaling. J Biol Chem 278:11849–11857. doi:10.1074/jbc.M209443200

    Article  CAS  PubMed  Google Scholar 

  • Gancedo JM (1998) Yeast carbon catabolite repression. Microbiol Mol Biol Rev 62:334–361

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia I, Gonzalez R, Gomez D, Scazzocchio C (2004) Chromatin Rearrangements in the prnD-prnB bidirectional promoter: dependence on transcription factors. Eukaryot Cell 3:144–156. doi:10.1128/ec.3.1.144-156.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia I, Mathieu M, Nikolaev I, Felenbok B, Scazzocchio C (2008) Roles of the Aspergillus nidulans homologues of Tup1 and Ssn6 in chromatin structure and cell viability. FEMS Microbiol Lett 289:146–154. doi:10.1111/j.1574-6968.2008.01379.x

    Article  CAS  PubMed  Google Scholar 

  • Georgakopoulos P, Lockington RA, Kelly JM (2012) SAGA complex components and acetate repression in Aspergillus nidulans. G3-genes genomes. Genetics 2:1357–1367. doi:10.1534/g3.112.003913

    CAS  Google Scholar 

  • Georgakopoulos P, Lockington RA, Kelly JM (2013) The Spt-Ada-Gcn5 acetyltransferase (SAGA) complex in Aspergillus nidulans. Plos One 8. doi:10.1371/journal.pone.0065221

  • Goldberg AL (2003) Protein degradation and protection against misfolded or damaged proteins. Nature 426:895–899. doi:10.1038/nature02263

    Article  CAS  PubMed  Google Scholar 

  • Hicks J, Lockington RA, Strauss J, Dieringer D, Kubicek CP, Kelly J, Keller N (2001) RcoA has pleiotropic effects on Aspergillus nidulans cellular development. Mol Microbiol 39:1482–1493. doi:10.1046/j.1365-2958.2001.02332.x

    Article  CAS  PubMed  Google Scholar 

  • Hunter AJ, Morris TA, Jin B, Saint CP, Kelly JM (2013) Deletion of creB in Aspergillus oryzae increases secreted hydrolytic enzyme activity. Appl Environ Microbiol 79:5480–5487. doi:10.1128/aem.01406-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hynes MJ (1975) Studies on the role of areA gene in regulation of nitrogen catabolism in Aspergillus nidulans. Aust J Biol Sci 28:301–313

    Article  CAS  PubMed  Google Scholar 

  • Hynes MJ, Kelly JM (1977) Pleiotropic mutants of Aspergillus nidulans altered in carbon metabolism. Mol Gen Genet 150:193–204. doi:10.1007/bf00695399

    Article  CAS  PubMed  Google Scholar 

  • Ichinose S, Tanaka M, Shintani T, Gomi K (2014) Improved alpha-amylase production by Aspergillus oryzae after a double deletion of genes involved in carbon catabolite repression. Appl Microbiol Biotechnol 98:335–343. doi:10.1007/s00253-013-5353-4

    Article  CAS  PubMed  Google Scholar 

  • Ilmen M, Thrane C, Penttila M (1996) The glucose repressor gene cre1 of Trichoderma: isolation and expression of a full-length and a truncated mutant form. Mol Gen Genet 251:451–460. doi:10.1007/bf02172374

    CAS  PubMed  Google Scholar 

  • Kaiser P, Huang L (2005) Global approaches to understanding ubiquitination. Genome Biol 6. doi:10.1186/gb-2005-6-10-233

  • Kamlangdee N (2008) Indentifying target proteins of CreB deubiquitination enzyme in the fungus Aspergillus nidulans. PhD thesis, The University of Adelaide

  • Kayikci O, Nielsen J (2015) Glucose repression in Saccharomyces cerevisiae. Fems Yeast Res 15:OV68–OV68. doi:10.1093/femsyr/fov068

  • Kelly JM (1980) Pleiotropic mutants of Aspergillus nidulans affected in carbon metabolism. PhD Thesis, The University of Melbourne

  • Kelly JM (2004) The regulation of carbon metabolism in filamentous fungi. In: Esser K (ed) Biochemistry and molecular biology, pp 385–401

  • Kelly JM, Hynes MJ (1977) Increased and decreased sensitivity to carbon catabolite repression of enzymes of acetate metabolism in mutants of Aspergillus nidulans. Mol Gen Genet 156:87–92. doi:10.1007/bf00272256

    Article  CAS  PubMed  Google Scholar 

  • Kelly JM, Katz ME (2010) Glucose. In: Borkovich KA, Ebbole DJ (eds) Cellular and molecular biology of filamentous fungi, pp 291–311

  • Kinoshita E, Kinoshita-Kikuta E, Koike T (2009a) Separation and detection of large phosphoproteins using Phos-tag SDS-PAGE. Nat Protoc 4:1513–1521. doi:10.1038/nprot.2009.154

    Article  CAS  PubMed  Google Scholar 

  • Kinoshita E, Kinoshita-Kikutal E, Matsubara M, Aoki Y, Ohie S, Mouri Y, Koike T (2009b) Two-dimensional phosphate-affinity gel electrophoresis for the analysis of phosphoprotein isotypes. Electrophoresis 30:550–559. doi:10.1002/elps.200800386

    Article  CAS  PubMed  Google Scholar 

  • Kraft C, Peter M, Hofmann K (2010) Selective autophagy: ubiquitin-mediated recognition and beyond. Nat Cell Biol 12:836–841

    Article  CAS  PubMed  Google Scholar 

  • Kulmburg P, Sequeval D, Lenouvel F, Mathieu M, Felenbok B (1992) Identification of the promoter region involved in the autoregulation of the transcriptional activator ALCR in Aspergillus nidulans. Mol Cell Biol 12:1932–1939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kulmburg P, Mathieu M, Dowzer C, Kelly J, Felenbok B (1993) Specific binding sites in the alcR and alcA promoters of the ethanol regulon for the CreA repressor mediating carbon catabolite repression in Aspergillus nidulans. Mol Microbiol 7:847–857. doi:10.1111/j.1365-2958.1993.tb01175.x

    Article  CAS  PubMed  Google Scholar 

  • Li MY, Chen DL, Shiloh A, Luo JY, Nikolaev AY, Qin J, Gu W (2002) Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 416:648–653. doi:10.1038/nature737

    Article  CAS  PubMed  Google Scholar 

  • Lockington RA, Kelly JM (2001) Carbon catabolite repression in Aspergillus nidulans involves deubiquitination. Mol Microbiol 40:1311–1321. doi:10.1046/j.1365-2958.2001.02474.x

    Article  CAS  PubMed  Google Scholar 

  • Lockington RA, Kelly JM (2002) The WD40-repeat protein CreC interacts with and stabilizes the deubiquitinating enzyme CreB in vivo in Aspergillus nidulans. Mol Microbiol 43:1173–1182. doi:10.1046/j.1365-2958.2002.02811.x

    Article  CAS  PubMed  Google Scholar 

  • Lockington RA, Sealylewis HM, Scazzocchio C, Davies RW (1985) Cloning and characterization of the ethanol utilization regulon in Aspergillus nidulans. Gene 33:137–149. doi:10.1016/0378-1119(85)90088-5

    Article  CAS  PubMed  Google Scholar 

  • Lockington RA, Rodbourn L, Barnett S, Carter CJ, Kelly JA (2002) Regulation by carbon and nitrogen sources of a family of cellulases in Aspergillus nidulans. Fungal Genet Biol 37:190–196. doi:10.1016/s1087-1845(02)00504-2

    Article  CAS  PubMed  Google Scholar 

  • Mathieu M, Nikolaev I, Scazzocchio C, Felenbok B (2005) Patterns of nucleosomal organization in the alc regulon of Aspergillus nidulans: roles of the AlcR transcriptional activator and the CreA global repressor. Mol Microbiol 56:535–548. doi:10.1111/j.1365-2958.2005.04559.x

    Article  CAS  PubMed  Google Scholar 

  • Meding S, Martin K, Gustafsson OJR, Eddes JS, Hack S, Oehler MK, Hoffmann P (2013) Tryptic peptide reference data sets for MALDI imaging mass spectrometry on formalin-fixed ovarian cancer tissues. J Proteome Res 12. doi:10.1021/pr300996x

  • Nayak T, Szewczyk E, Oakley CE, Osmani A, Ukil L, Murray SL, Hynes MJ, Osmani SA, Oakley BR (2006) A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics 172:1557–1566. doi:10.1534/genetics.105.052563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • New AM, Cerulus B, Govers SK, Perez-Samper G, Zhu B, Boogmans S, Xavier JB, Verstrepen KJ (2014) Different levels of catabolite repression optimize growth in stable and variable environments. Plos Biol 12. doi:10.1371/journal.pbio.1001764

  • Nguyen LK, Kolch W, Kholodenko BN (2013) When ubiquitination meets phosphorylation: a systems biology perspective of EGFR/MAPK signalling. Cell Commun Signal 11. doi:10.1186/1478-811x-11-52

  • Nijman SMB, Huang TT, Dirac AMG, Brummelkamp TR, Kerkhoven RM, D’Andrea AD, Bernards R (2005) The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol Cell 17:331–339. doi:10.1016/j.molcel.2005.01.008

    Article  CAS  PubMed  Google Scholar 

  • Pateman JA, Rever BM, Cove DJ (1967) Genetic and biochemical studies of nitrate reduction in Aspergillus nidulans. Biochem J 104:103–111. doi:10.1042/bj1040103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pateman JA, Doy CH, Olsen JE, Norris U, Creaser EH, Hynes M (1983) Regulation of alcohol dehydrogenase (ADH) and aldehyde dehydrogenase (ALDDH) in Aspergillus nidulans. Proc R Soc Ser B Biol Sci 217:243–264. doi:10.1098/rspb.1983.0009

    Article  CAS  Google Scholar 

  • Penalva MA, Tilburn J, Bignell E, Arst HN (2008) Ambient pH gene regulation in fungi: making connections. Trends Microbiol 16:291–300. doi:10.1016/j.tim.2008.03.006

    Article  CAS  PubMed  Google Scholar 

  • Pilsyk S, Natorff R, Sienko M, Skoneczny M, Paszewski A, Brzywczy J (2015) The Aspergillus nidulans metZ gene encodes a transcription factor involved in regulation of sulfur metabolism in this fungus and other Eurotiales. Curr Genet 61:115–125. doi:10.1007/s00294-014-0459-5

    Article  CAS  PubMed  Google Scholar 

  • Portnoy T, Margeot A, Linke R, Atanasova L, Fekete E, Sandor E, Hartl L, Karaffa L, Druzhinina IS, Seiboth B, Le Crom S, Kubicek CP (2011) The CRE1 carbon catabolite repressor of the fungus Trichoderma reesei: a master regulator of carbon assimilation. Bmc Genomics 12. doi:10.1186/1471-2164-12-269

  • Punt PJ, Dingemanse MA, Kuyvenhoven A, Soede RDM, Pouwels PH, Vandenhondel C (1990) Functional elements in the promoter region of the Aspergillus nidulans gpdA gene encoding glyceraldehyde-3-phosphate dehydrogenase. Gene 93:101–109. doi:10.1016/0378-1119(90)90142-e

    Article  CAS  PubMed  Google Scholar 

  • Reyes-Dominguez Y, Narendja F, Berger H, Gallmetzer A, Fernandez-Martin R, Garcia I, Scazzocchio C, Strauss J (2008) Nucleosome positioning and histone H3 acetylation are independent processes in the Aspergillus nidulans prnD-prnB bidirectional promoter. Eukaryot Cell 7:656–663. doi:10.1128/ec.00184-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reyes-Turcu FE, Ventii KH, Wilkinson KD (2009) Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 78:363–397. doi:10.1146/annurev.biochem.78.082307.091526

    Article  CAS  PubMed  Google Scholar 

  • Ries L, Belshaw NJ, Ilmen M, Penttila ME, Alapuranen M, Archer DB (2014) The role of CRE1 in nucleosome positioning within the cbh1 promoter and coding regions of Trichoderma reesei. Appl Microbiol Biotechnol 98:749–762. doi:10.1007/s00253-013-5354-3

    Article  CAS  PubMed  Google Scholar 

  • Ries LNA, Beattie SR, Espeso EA, Cramer RA, Goldman GH (2016) Diverse regulation of the CreA carbon catabolite repressor in Aspergillus nidulans. Genetics. doi:10.1534/genetics.116.187872

    PubMed  PubMed Central  Google Scholar 

  • Roy P, Lockington RA, Kelly JM (2008) CreA-mediated repression in Aspergillus nidulans does not require transcriptional auto-regulation, regulated intracellular localisation or degradation of CreA. Fungal Genet Biol 45:657–670. doi:10.1016/j.fgb.2007.10.016

    Article  CAS  PubMed  Google Scholar 

  • Ruijter GJG, Visser J (1997) Carbon repression in Aspergilli. FEMS Microbiol Lett 151:103–114. doi:10.1111/j.1574-6968.1997.tb12557.x

    Article  CAS  PubMed  Google Scholar 

  • Semighini CP, Marins M, Goldman MHS, Goldman GH (2002) Quantitative analysis of the relative transcript levels of ABC transporter Atr genes in Aspergillus nidulans by real-time reverse transcription-PCR assay. Appl Environ Microbiol 68:1351–1357. doi:10.1128/aem.68.3.1351-1357.2002

    Article  CAS  PubMed  Google Scholar 

  • Shilatifard A (2006) Chromatin modifications by methylation and ubiquitination: Implications in theregulation of gene expression. Annu Rev Biochem 75:243–269. doi:10.1146/annurev.biochem.75.103004.142422

    Article  CAS  PubMed  Google Scholar 

  • Shroff RA, Lockington RA, Kelly JM (1996) Analysis of mutations in the creA gene involved in carbon catabolite repression in Aspergillus nidulans. Can J Microbiol 42:950–959. doi:10.1139/m96-122

    Article  CAS  PubMed  Google Scholar 

  • Shroff RA, Oconnor SM, Hynes MJ, Lockington RA, Kelly JM (1997) Null alleles of creA, the regulator of carbon catabolite repression in Aspergillus nidulans. Fungal Genet Biol 22:28–38. doi:10.1006/fgbi.1997.0989

    Article  CAS  PubMed  Google Scholar 

  • Strauss J, Horvath HK, Abdallah BM, Kindermann J, Mach RL, Kubicek CP (1999) The function of CreA, the carbon catabolite repressor of Aspergillus nidulans, is regulated at the transcriptional and post-transcriptional level. Mol Microbiol 32:169–178. doi:10.1046/j.1365-2958.1999.01341.x

    Article  CAS  PubMed  Google Scholar 

  • Szewczyk E, Nayak T, Oakley CE, Edgerton H, Xiong Y, Taheri-Talesh N, Osmani SA, Oakley BR (2006) Fusion PCR and gene targeting in Aspergillus nidulans. Nat Protoc 1:3111–3120. doi:10.1038/nprot.2006.405

    Article  CAS  PubMed  Google Scholar 

  • Szilagyi M, Miskei M, Karanyi Z, Lenkey B, Pocsi I, Emri T (2013) Transcriptome changes initiated by carbon starvation in Aspergillus nidulans. Microbiology (Reading, England) 159:176–190. doi:10.1099/mic.0.062935-0

  • Tilburn J, Scazzocchio C, Taylor GG, Zabickyzissman JH, Lockington RA, Davies RW (1983) Transformation by integration in Aspergillus nidulans. Gene 26:205–221. doi:10.1016/0378-1119(83)90191-9

    Article  CAS  PubMed  Google Scholar 

  • Todd RB, Lockington RA, Kelly JM (2000) The Aspergillus nidulans creC gene involved in carbon catabolite repression encodes a WD40 repeat protein. Mol Gen Genet 263:561–570. doi:10.1007/s004380051202

    Article  CAS  PubMed  Google Scholar 

  • Todd RB, Greenhalgh JR, Hynes MJ, Andrianopoulos A (2003) TupA, the Penicillium marneffei Tup1p homologue, represses both yeast and spore development. Mol Microbiol 48:85–94. doi:10.1046/j.1365-2958.2003.03426.x

    Article  CAS  PubMed  Google Scholar 

  • Todd RB, Davis MA, Hynes MJ (2007) Genetic manipulation of Aspergillus nidulans: meiotic progeny for genetic analysis and strain construction. Nat Protoc 2:811–821. doi:10.1038/nprot.2007.112

    Article  CAS  PubMed  Google Scholar 

  • Vautard-Mey G, Fevre M (2000) Mutation of a putative AMPK phosphorylation site abolishes the repressor activity but not the nuclear targeting of the fungal glucose regulator CRE1. Curr Genet 37:328–332. doi:10.1007/s002940050535

    Article  CAS  PubMed  Google Scholar 

  • Wong KH, Hynes MJ, Davis MA (2008) Recent advances in nitrogen regulation: a comparison between Saccharomyces cerevisiae and filamentous fungi. Eukaryot Cell 7:917–925. doi:10.1128/ec.00076-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu JS, Suka N, Carlson M, Grunstein M (2001) TUP1 utilizes histone H3/H2B-specific HDA1 deacetylase to repress gene activity in yeast. Mol Cell 7:117–126. doi:10.1016/s1097-2765(01)00160-5

    Article  CAS  PubMed  Google Scholar 

  • Yamashiro CT, Ebbole DJ, Lee BU, Brown RE, Bourland C, Madi L, Yanofsky C (1996) Characterization of rco-1 of Neurospora crassa, a pleiotropic gene affecting growth and development that encodes a homolog of Tup1 of Saccharomyces cerevisiae. Mol Cell Biol 16:6218–6228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshikawa M, Tamaki M, Sugimoto E, Chiba H (1974) Effect of dephosphorylation on self-association and precipitation of beta-casein. Agric Biol Chem 38:2051–2052. doi:10.1271/bbb1961.38.2051

    CAS  Google Scholar 

  • Yu J, Son H, Park AR, Lee SH, Choi GJ, Kim JC, Lee YW (2014) Functional characterization of sucrose non-fermenting 1 protein kinase complex genes in the Ascomycete Fusarium graminearum. Curr Genet 60:35–47. doi:10.1007/s00294-013-0409-7

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Robin Lockington, Jai Denton, Adrian Hunter and Vivian Georgakopoulos for helpful insights into the research and manuscript. MAA was supported by an Australian Commonwealth Research Scholarship; NK was supported by a scholarship from the Thai Government; research was supported by the School of Biological Science, The University of Adelaide.

Author information

Author notes

  1. Niyom Kamlangdee

    Present address: Walailak University, 222 Thaiburi Thasala, Nakhonsithamrat, Nakhon Si Thammarat, 80160, Thailand

Authors and Affiliations

  1. Department of Genetics and Evolution, The University of Adelaide, Adelaide, 5005, Australia

    Md Ashiqul Alam, Niyom Kamlangdee & Joan M. Kelly

Authors
  1. Md Ashiqul Alam
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Niyom Kamlangdee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joan M. Kelly
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joan M. Kelly.

Additional information

Communicated by M. Kupiec.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 738 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alam, M.A., Kamlangdee, N. & Kelly, J.M. The CreB deubiquitinating enzyme does not directly target the CreA repressor protein in Aspergillus nidulans . Curr Genet 63, 647–667 (2017). https://doi.org/10.1007/s00294-016-0666-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-016-0666-3

Keywords

Search

Navigation