1,888
Views
2
CrossRef citations to date
0
Altmetric
Biochemistry & Molecular Biology

Proteomic analysis on Aspergillus strains that are useful for industrial enzyme production

ORCID Icon, &
Pages 2241-2252 | Received 08 Apr 2020, Accepted 06 Jul 2020, Published online: 21 Jul 2020

References

  • Schuster E, Dunn-Coleman N, Frisvad J, et al. On the safety of Aspergillus niger - a review. Appl Microbiol Biotechnol. 2002;59(4–5):426–435.
  • van Dijck PWM, Selten GCM, Hempenius RA. On the safety of a new generation of DSM Aspergillus niger enzyme production strains. Regul Toxicol Pharmacol. 2003;38(1):27–35.
  • Andersen MR, Salazar MP, Schaap PJ, et al. Comparative genomics of citric-acid-producing Aspergillus niger ATCC 1015 versus enzyme-producing CBS 513.88. Genome Res. 2011;21(6):885–897.
  • de Vries RP, Visser J. Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiol Mol Biol Rev. 2001 Dec;65(4):497–522.
  • Berka RM, Dunn-Coleman N, Ward M. Industrial enzymes from Aspergillus species. In: Bennett JW, Klich MA, editors. Aspergillus, biology and industrial applications. Stoneham (MA): Butterworth-Heinemann; 1992. p. 155–202.
  • Lubertozzi D, Keasling JD. Developing Aspergillus as a host for heterologous expression. Biotechnol Adv. 2009;27(8):53–75.
  • Gouka RJ, Punt PJ, van den Hondel CA Efficient production of secreted proteins by Aspergillus: progress, limitations and prospects. Appl Microbiol Biotechnol. 1997;47(1):1–11.
  • Punt PJ, van Biezen N, Conesa A, et al. Filamentous fungi as cell factories for heterologous protein production. Trends Biotechnol. 2002 May;20(5):200–206.
  • Fleer A, Dersch P. Expression and export: recombinant protein production systems for Aspergillus. Appl Microbiol Biotechnol. 2010;87(4):1255–1270.
  • Jacobs DI, Olsthoorn MM, Maillet I, et al. Effective lead selection for improved protein production in Aspergillus niger based on integrated genomics. Fungal Genet Biol. 2009;46(1):141–152.
  • Lombrana M, Moralejo FJ, Pinto R, et al. Modulation of Aspergillus awamori thaumatin secretion by modification of bipA gene expression. Appl Environ Microbiol. 2004;70(9):5145–5152.
  • Carvalho ND, Arentshorst M, Kooistra R, et al. Effects of a defective ERAD pathway on growth and heterologous protein production in Aspergillus niger. Appl Microbiol Biotechnol. 2011;89(1):357–373.
  • Fiedler MRM, Barthel L, Kubisch C, et al. Construction of an improved Aspergillus niger platform for enhanced glucoamylase secretion. Microb Cell Fact. 2018;17(1):95.
  • Meyer V, Wu B, Ram AFJ. Aspergillus as a multi-purpose cell factory: current status and perspectives. Biotechnol Lett. 2011;33(3):469–476.
  • Liu L, Feizi A, Österlund T, et al. Genome-scale analysis of the high-efficient protein secretion system of Aspergillus oryzae. BMC Syst Biol. 2014;8(16):73.
  • Knuf C, Nielsen J. Aspergilli: systems biology and industrial applications. Biotechnol J. 2012;7(9):1147–1155.
  • Andersen MR, Nielsen J. Current status of systems biology in Aspergilli. Fungal Genet Biol. 2009;46:180–190.
  • Andersen M, Nielsen M, Nielsen J. Metabolic model integration of the bibliome, genome, metabolome and reactome of Aspergillus niger. Mol Syst Biol. 2008;4(1):78.
  • Pel H, de Winde J, Archer D, et al. Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol. 2007;25(2):221–231.
  • Guillemette T, van Peij NN, Goosen T, et al. Genomic analysis of the secretion stress response in the enzyme-producing cell factory Aspergillus niger. BMC Genomics. 2007;8(1):158.
  • Jorgensen TR, Goosen T, van den Hondel CA, et al. Transcriptomic comparison of Aspergillus niger growing on two different sugars reveals coordinated regulation of the secretory pathway. BMC Genomics. 2009;10(1):44.
  • Lu X, Sun J, Nimtz M, et al. The intra- and extracellular proteome of Aspergillus niger growing on defined medium with xylose or maltose as carbon substrate. Microb Cell Fact. 2010;9(17):23.
  • Miguel J, de Oliveira PF, van Passel MWJ, et al. Shotgun proteomics of Aspergillus niger microsomes upon D-Xylose induction. Appl Environ Microbiol. 2010 July;76(13):4421–4429.
  • Miguel J, de Oliveira PF, van Passel MWJ, et al. Proteomic analysis of the secretory response of Aspergillus niger to D-Maltose and D-Xylose. PLoS ONE. 2011;6(6):e20865.
  • Carvalho NDSP, Jorgensen TR, Arentshorst M, et al. Genome-wide expression analysis upon constitutive activation of the HacA bZIP transcription factor in Aspergillus niger reveals a coordinated cellular response to counteract ER stress. BMC Genomics. 2012;13(1):350–366.
  • Lu H, Cao W, Liu X, et al. Multi-omics integrative analysis with genome-scale metabolic model simulation reveals global cellular adaptation of Aspergillus niger under industrial enzyme production condition. Sci Rep. 2018;8(16):14404.
  • Sloothaak J, Odoni DI, de Graaff LH, et al. Aspergillus niger membrane-associated proteome analysis for the identification of glucose transporters. Biotechnol Biofuels. 2015;8(1):150.
  • Udagawa H, Landvik S, Ihara M, et al. Inventors; Novozymes A/S, Novozymes North America, Inc. assignee. Polypeptides having glucoamylase activity and polynucleotides encoding the same. US patent 8148127 B2. 2012 Apr 3.
  • Udagawa H Inventor; Novozymes A/S, assignee. Simultaneous site-specific integrations of multiple gene-copies in filamentous fungi. 2012 Nov. 29. PCT application WO2012/160093.
  • Pedersen H, Beyer M, Nielsen J. Glucoamylase production in batch, chemostat and fed-batch cultivations by an industrial strain of Aspergillus niger. Appl Microbiol Biotechnol. 2000;53(3):272–277.
  • Tatusov RL, Fedorova ND, Jackson JD, et al. The COG database: an updated version includes eukaryotes. BMC Bioinformatics. 2003 Sep 11;4(1):1–4. (KOG).
  • van Gemeren IA, Punt PJ, Drint-Kuyvenhoven A, et al. The ER chaperone encoding bipA gene of black Aspergilli is induced by heat shock and unfolded proteins. Gene. 1997 Oct;198(1–2):43–52.
  • Mori K. Signaling pathways in the unfolded protein response: development from yeast to mammals. J Biochem. 2009;146(6):743–750.
  • Ngiam C, Jeenes DJ, Punt PJ, et al. Characterization of a foldase, protein disulfide isomerase A, in the protein secretory pathway of Aspergillus niger. Appl Environ Microbiol. 2000;66(2):775–782.
  • Moralejo FJ, Watson AJ, Jeenes DJ, et al. A defined level of protein disulfide isomerase expression is required for optimal secretion of thaumatin by Aspergillus awamori. Mol Genet Enom. 2001;266:245–253.
  • Zapun A, Darby NJ, Tessier DC, et al. Enhanced catalysis of ribonuclease B folding by the interaction of calnexin or calreticulin with ERp57. J Biol Chem. 1998;273(11):6009–6012.
  • Schroder M, Kaufman RJ. ER stress and the unfolded protein response. Mutat Res. 2005;569(1–2):29–63.
  • Sims AH, Gent ME, Lanthaler K, et al. Transcriptome analysis of recombinant protein secretion by Aspergillus nidulans and the unfolded-protein response in vivo. Appl Environ Microbiol. 2005 May;71(5):2737–2747.
  • Mulder HJ, Saloheimo M, Penttilä M, et al. The transcription factor HACA mediates the unfolded protein response in Aspergillus niger, and up-regulates its own transcription. Mol Gen Genet. 2004;271(2):130–140.
  • Kwon MJ, Jogensen TR, Nitsche BM, et al. The transcriptomic fingerprint of glucoamylase over-expression in Aspergillus niger. BMC Genomics. 2012;13(1):701.
  • Travers KJ, Patil CK, Wodicka L, et al. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell. 2000 Apr 28;101(3):249–258.
  • Bodnar N1, Rapoport T1. Toward an understanding of the Cdc48/p97 ATPase. F1000Res. 2017 Aug 3;6:1318.
  • Ye Y, Meyer HH, Rapoport TA. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature. 2001;414(6864):652–656.
  • Jarosch E, Taxis C, Volkwein C, et al. Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nat Cell Biol. 2002;4(2):134–139.
  • Wu X, Rapoport TA. Mechanistic insights into ER-associated protein degradation. Curr Opin Cell Biol. 2018 Aug;53:22–28.
  • Hoseki J, Ushioda R, Nagata K. Mechanism and components of endoplasmic reticulum-associated degradation. J Biochem. 2010;147(1):19–25.
  • Al-Sheikh H, Watson AJ, Lacey GA, et al. Endoplasmic reticulum stress leads to the selective transcriptional downregulation of the glucoamylase gene in Aspergillus niger. Mol Microbiol. 2004;53(6):1731–1742.
  • Pakula TM, Laxell M, Huuskonen A, et al. The Effects of drugs inhibiting protein secretion in the filamentous fungus Trichoderma reesei. J Biol Chem. 2003;278(45):45011–45020.
  • Oliver BG, Panepinto JC, Fortwendel JR, et al. Cloning and expression of pkaC and pkaR, the genes encoding the cAMP-dependent protein kinase of Aspergillus fumigatus. Mycopathologia. 2002;154(2):85–91.
  • Ribeiro LFC, Chelius C, Boppidi KR, et al. Comprehensive analysis of Aspergillus nidulans PKA phosphorylome identifies a novel mode of CreA regulation. mBio. 2019 Apr 30;10(2). DOI:10.1128/mBio.02825-18
  • Saudohar M, Bencina M, van de Vondervoort PJI, et al. Cyclic AMP-dependent protein kinase is involved in morphogenesis of Aspergillus niger. Microbiology. 2002 Aug;148(Pt 8):2635–2645.
  • Jernejc K, Bencina M. Lipid composition of cAMP-dependent protein kinase mutants of Aspergillus niger. FEMS Microbiol Lett. 2003 Aug;225(2):291–297.
  • Fuller KK, Richie DL, Feng X, et al. Divergent protein Kinase A isoforms co-ordinately regulate conidial germination, carbohydrate metabolism and virulence in Aspergillus fumigatus. Mol Microbiol. 2011;79(4):1045–1062.
  • Liebmann B, Müller M, Braun A, et al. The cyclic AMP-Dependent protein Kinase A network regulates development and virulence in Aspergillus fumigatus. Infect Immun. 2004;72(9):5193–5203.
  • Shin Y, Lee S, Ku M, et al. Cytochrome c peroxidase regulates intracellular reactive oxygen species and methylglyoxal via enzyme activities of erythroascorbate peroxidase and glutathione-related enzymes in Candida albicans. Int J Biochem Cell Biol. 2017 Nov;92:183–201.
  • Keiner M, Harvey LM, McNeil B. Morphological and enzymatic responses of a recombinant Aspergillus niger to oxidative stressors in chemostat cultures. J Biotechnol. 2003;100(3):251–260.
  • Peisker K, Chiabudini M, Rospert S. The ribosome-bound Hsp70 homolog Ssb of Saccharomyces cerevisiae. Biochim Biophys Acta. 2010;1803(6):662–672.
  • Kang P-J, Ostermann J, Shilling J, et al. Requirement for hsp70 in the mitochondrial matrix for translocation and folding of precursor proteins. Nature. 1990;348(6297):137–143.
  • Liu Q, Krzewska J, Liberek K, et al. Mitochondrial Hsp70 Ssc1: role in protein folding. J Biol Chem. 2000;276(9):6112–6118.
  • Gumiero A, Conz C, Valentín G, et al. Interaction of the cotranslational Hsp70 Ssb with ribosomal proteins and rRNA depends on its lid domain. Nat Commun. 2016;7(1):13563.
  • Döring K, Ahmed N, Riemer T, et al. Profiling Ssb-Nascent chain interactions reveals principles of Hsp70-assisted folding. Cell. 2017 Jul 13;170(2):298–311.
  • von Plehwe U, Berndt U, Conz C, et al. The Hsp70 homolog Ssb is essential for glucose sensing via the SNF1 kinase network. Genes Dev. 2009 Sep 1;23(17):2102–2115.
  • Hübscher V, Mudholkar K, Chiabudini M, et al. The Hsp70 homolog Ssb and the 14-3-3 protein Bmh1 jointly regulate transcription of glucose repressed genes in Saccharomyces cerevisiae. Nucleic Acids Res. 2016 Jul;44(12):5629–5645.
  • Dombek KM, Kacherovsky N, Young ET. The Reg1-interacting proteins, Bmh1, Bmh2, Ssb1, and Ssb2, have roles in maintaining glucose repression in Saccharomyces cerevisiae. J Biol Chem. 2004 Sep 10;279(37):39165–39174.
  • Kraus PR, Hofmann AF, Harris SD. Characterization of the Aspergillus nidulans 14-3-3 homologue, ArtA. FEMS Microbiol Lett. 2002 Apr 23;210(1):61–66.
  • Chughtai ZS, Rassadi R, Matusiewicz N, et al. Starvation promotes nuclear accumulation of the hsp70 Ssa4p in yeast cells. J Biol Chem. 2001 Jun;276(23):20261–20266.
  • Quan X, Rassadi R, Rabie B, et al. Regulated nuclear accumulation of the yeast hsp70 Ssa4p in ethanol-stressed cells is mediated by the N-terminal domain, requires the nuclear carrier Nmd5p and protein kinase C. Faseb J. 2004 May;18(7):899–901.
  • Quan XX, Tsoulos P, Kuritzky A, et al. The carrier Msn5p/KAp142p promotes nuclear export of the hsp70 Ssa4p and relocates in response to stress. Mol Microbiol. 2006;62(2):592–609.
  • Bommer UA, Thiele BJ. The translationally controlled tumour protein (TCTP). Int J Biochem Cell Biol. 2001 Mar;36(3):379–385.
  • Rinnerthaler M, Lejskova R, Grousl T, et al. Mmi1, the yeast homologue of mammalian TCTP, associates with stress granules in heat-shocked cells and modulates proteasome activity. PLoS One. 2013 Oct;8(10):e77791.
  • Vojtova J, Hasek J. Mmi1, the yeast ortholog of mammalian translationally controlled tumor protein (TCTP), negatively affects rapamycin-induced autophagy in post-diauxic growth phase. Cells. 2020 Jan;9(1):E138.
  • Oh YT, Ahn CS, Jeong YJ, et al. Aspergillus nidulans translationally controlled tumor protein has a role in the balance between asexual and sexual differentiation and normal hyphal branching. FEMS Microbiol Lett. 2013 Jun;343(1):20–25.
  • Hesselberth JR, Miller JP, Golob A, et al. Comparative analysis of saccharomyces cerevisiae WW domains and their interacting proteins. Genome Biol. 2006;7(4):R30.
  • Musacchio A, Gibson T, Rice P, et al. The PH domain: a common piece in the structural patchwork of signaling proteins. Trends Biochem Sci. 1993 Sep;18(9):343–348.
  • Dhavale T, Jedd G. The fungal Woronin body. In: Howard RJ, Gow NAR, editors. Biology of the fungal cell. 2nd ed. Berlin: Springer; 2007. p. 87–94.
  • Lim D, Hains P, Walsh B, et al. Proteins associated with the cell envelope of Trichoderma reesei: a proteomic approach. Proteomics. 2001;1:899–910.
  • Maruyama J, Juvvadi PR, Ishi K, et al. Three-dimensional image analysis of plugging at the septal pore by Woronin body during hypotonic shock inducing hyphal tip bursting in the filamentous fungus Aspergillus oryzae. Biochem Biophys Res Commun. 2005;331(4):1081–1088.
  • Tey WK, North AJ, Peyes JL, et al. Polarized gene expression determines Woronin body formation at the leading edge of the fungal colony. Mol Biol Cell. 2005 June;16(6):2651–2659.
  • Gunning PW, Hardeman EC, Lappalainen P, et al. Tropomyosin - master regulator of actin filament function in the cytoskeleton. J Cell Sci. 2015 Aug;128(16):2965–2974.
  • Bergs A, Ishitsuka Y, Evangelinosa M, et al. Dynamics of actin cables in polarized growth of the filamentous fungus Aspergillus nidulans. Front Microbiol. 2016;7:682.
  • Takeshita N, Evangelinosa M, Zhoud L, et al. Pulses of Ca2+ coordinate actin assembly and exocytosis for stepwise cell extension. PNAS. 2017 May;114(22):5701–5706.
  • Taheri-Talesh N, Horio T, Araujo-Baza´n L, et al. The tip growth apparatus of Aspergillus nidulans. Mol Biol Cell. 2008 April;19(4):1439–1449.
  • Gordon CL, Archer DB, Jeenes DJ, et al. A glucoamylase: GFP gene fusion to study protein secretion by individual hyphae of Aspergillus niger. J Microbiol Methods. 2006;42(1):39–48.
  • Hayakawa Y, Ishikawa E, Shoji J, et al. Septum-directed secretion in the filamentous fungus Aspergillus oryzae. Mol Microbiol. 2011;81(1):40–55.
  • Zhang S, Sato H, Ichinose S, et al. Cell wall α-1,3-glucan prevents α-amylase adsorption onto fungal cell in submerged culture of Aspergillus oryzae. J Biosci Bioeng. 2017;124(1):47–53.