Transcriptomic comparison of Aspergillus niger growing on two different sugars reveals coordinated regulation of the secretory pathway

BMC Genomics

Volumn 10, Issue , 2009, Pages

  Jørgensen, Thomas R ^a,b   Goosen, Theo ^b,c   van den Hondel, Cees A M J J ^b   Ram, Arthur F J ^b   Iversen, Jens J L ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b LEIDEN UNIVERSITY   (Netherlands)

^c HAN UNIVERSITY OF APPLIED SCIENCES   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MALTOSE; TRANSCRIPTOME; XYLOSE; FUNGAL PROTEIN; FUNGAL RNA;

ARTICLE; ASPERGILLUS NIGER; CELL FUNCTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; FUNGAL STRAIN; FUNGUS GROWTH; GENE EXPRESSION PROFILING; GENE SEQUENCE; GENE TRANSLOCATION; GENETIC TRANSCRIPTION; GOLGI COMPLEX; MYCELIUM; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; PROTEIN SECRETION; PROTEIN TRANSPORT; TRANSCRIPTION REGULATION; UPREGULATION; COMPARATIVE STUDY; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PROTEIN SYNTHESIS; SECRETION;

ASPERGILLUS NIGER; FUNGI;

ASPERGILLUS NIGER; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; MALTOSE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN BIOSYNTHESIS; RNA, FUNGAL; SECRETORY PATHWAY; XYLOSE;

EID: 60549083506     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-10-44     Document Type: Article

References (50)

1. De Vries RP Visser J Aspergillus enzymes involved in degradation of plant cell wall polysaccharides Microbiol Mol Biol Rev 2001, 65:497-522. 99039 11729262 10.1128/MMBR.65.4.497-522.2001
2. Yuan XL Goosens C Kools H Maarel van der MJ Hondel van den CA Dijkhuizen L Ram AF Database mining and transcriptional analysis of genes encoding inulin-modifying enzymes of Aspergillus niger Microbiol 2006, 152:3061-3073. 10.1099/mic.0.29051-0
3. Pel HJ de Winde JH Archer DB Dyer PS Hofmann G Schaap PJ Turner G de Vries RP Albang R Albermann K Andersen MR Bendtsen JD Benen JA Berg van den M Breestraat S Caddick MX Contreras R Cornell M Coutinho PM Danchin EG Debets AJ Dekker P van Dijck PW van Dijk A Dijkhuizen L Driessen AJ d'Enfert C Geysens S Goosen C Groot GS de Groot PW Guillemette T Henrissat B Herweijer M Hombergh van den JP Hondel van den CA Heijden van der RT Kaaij van der RM Klis FM Kools HJ Kubicek CP van Kuyk PA Lauber J Lu X Maarel van der MJ Meulenberg R Menke H Mortimer MA Nielsen J Oliver SG Olsthoorn M Pal K van Peij NN Ram AF Rinas U Roubos JA Sagt CM Schmoll M Sun J Ussery D Varga J Vervecken W Vondervoort van de PJ Wedler H Wösten HA Zeng AP van Ooyen AJ Visser J Stam H Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88 Nat Biotechnol 2007, 25:221-231. 10.1038/nbt1282 17259976
4. Andersen MR Vongsangnak W Panagiotou G Salazar MP Lehmann L Nielsen J A trispecies Aspergillus microarray: Comparative transcriptomics of three Aspergillus species Proc Natl Acad Sci USA 2008, 18:4387-4392. 10.1073/ pnas.0709964105
5. Pitt JI Toxigenic fungi: Which are important? Med Mycol 2000, 38:17-22. 11204142
6. Cary JW Ehrlich K Aflatoxigenicity in Aspergillus: Molecular genetics, phylogenetic relationships and evolutionary implications Mycopathol 2006, 162:167-177. 10.1007/s11046-006-0051-8
7. Jørgensen TR Identification and toxigenic potential of the industrially important fungi, Aspergillus oryzae and Aspergillus sojae J Food Prot 2007, 70:2916-2934. 18095455
8. Schuster E Dunn-Coleman N Frisvad JC van Dijck PWM On the safety of Aspergillus niger - a review Appl Microbiol Biotechnol 2002, 59:426-435. 10.1007/s00253-002-1032-6 12172605
9. Frisvad JC Smedsgaard J Samson RA Larsen TO Thrane U Fumonisin B2 production by Aspergillus niger J Agric Food Chem 2007, 55:9727-9732. 10.1021/jf0718906 17929891
10. Conesa A Punt PJ van Luijk N Hondel van den CAMJJ The secretion pathway in filamentous fungi: A biotechnological view Fungal Genet Biol 2001, 33:155-171. 10.1006/fgbi.2001.1276 11495573
11. Helenius A Aebi M Roles of N-linked glycans in the endoplasmic reticulum Annu Rev Biochem 2004, 73:1019-1049. 10.1146/ annurev.biochem.73.011303.073752 15189166
12. Sato K Nakano A Mechanisms of COPII vesicle formation and protein sorting FEBS Lett 2007, 581:2076-2082. 10.1016/j.febslet.2007.01.091 17316621
13. van Anken E Braakman I Versatility of the endoplasmic reticulum protein folding factory Crit Rev Biochem Mol Biol 2005, 40:191-228. 10.1080/ 10409230591008161 16126486
14. Wallis GLF Swift RJ Hemming FW Trinci APJ Peberdy JF Glucoamylase overexpression and secretion in Aspergillus niger: Analysis of glycosylation Biochim Biophys Acta 1999, 1472:576-586. 10564772
15. Guillemette T van Peij NNME Goosen T Lanthaler K Robson GD Hondel van den CAMJJ Stam H Archer DB Genomic analysis of the secretion stress response in the enzyme-producing cell factory Aspergillus niger BMC Genomics 2007, 8:158. 1894978 17561995 10.1186/1471-2164-8-158
16. Piper MDW Daran-Lapujade P Bro C Regenberg B Knudsen S Nielsen J Pronk JT Reproducibility of oligonucleotide microarray transcriptome analyses - an interlaboratory comparison using chemostat cultures of Saccharomyces cerevisiae J Biol Chem 2001, 277:37001-37008. 10.1074/ jbc.M204490200
17. Ruepp A Zollner A Maier D Albermann K Hani J Mokrejs M Tetko I Güldener U Mannhaupt G Münsterkötter M Mewes HW The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes Nucleic Acids Res 2004, 32:5539-5545. 524302 15486203 10.1093/nar/gkh894
18. Yuan XL Kaaij van der RM Hondel van den CA Punt PJ Maarel van der MJ Dijkhuizen L Ram AF Aspergillus niger genome-wide analysis reveals a large number of novel alpha-glucan acting enzymes with unexpected expression profiles Mol Genet Genomics 2008, 279:545-561. 2413074 18320228 10.1007/s00438-008-0332-7
19. van Peij NN Gielkens MM de Vries RP Visser J de Graaff LH The transcriptional activator XlnR regulates both xylanolytic and endoglucanase gene expression in Aspergillus niger Appl Environ Microbiol 1998, 64:3615-3619. 106473 9758775
20. Wang X Devaiah SP Zhang W Welti R Signaling functions of phosphatidic acid Prog Lipid Res 2006, 45:250-278. 10.1016/j.plipres.2006.01.005 16574237
21. Punt PJ van Gemeren IA Drint-Kuijvenhoven J Hessing JG van Mijlwijk-Harteveld GM Beijersbergen A Verrips CT Hondel van den CA Analysis of the role of the gene bipA, encoding the major endoplasmic reticulum chaperone protein in the secretion of homologous and heterologous proteins in black Aspergilli Appl Microbiol Biotechnol 1998, 50:447-454. 10.1007/s002530051319 9830095
22. Ngiam C Jeenes DJ Punt PJ Hondel van den CAMJJ Archer DB Characterization of a foldase, protein disulfide isomerase A, in the protein secretory pathway of Aspergillus niger Appl Environ Microbiol 2000, 66:775-782. 91895 10653750 10.1128/AEM.66.2.775-782.2000
23. Shoji J Arioka M Kitamoto K Dissecting cellular components of the secretory pathway in filamentous fungi: Insights into their application for protein production Biotechnol Lett 2008, 30:7-14. 10.1007/ s10529-007-9516-1 17846708
24. Saloheimo M Lund M Penttilä ME The protein disulfide isomerase gene of the fungus Trichoderma reesei is induced by endoplasmic reticulum stress and regulated by the carbon source Mol Gen Genet 1999, 262:35-45. 10.1007/s004380051057 10503534
25. Webb GC Akbar MS Zhao C Steiner DF Expression profiling of pancreatic β cells: Glucose regulation of secretory and metabolic pathway genes Proc Natl Acad Sci USA 2000, 7:5773-5778. 10.1073/pnas.100126597
26. Shaffer AL Shapiro-Shelef M Iwakoshi NN Lee AH Qian SB Zhao H Yu X Yang L Tan BK Rosenwald A Hurt EM Petroulakis E Sonenberg N Yewdell JW Calame K Glimcher LH Staudt LM Xbp1, downstream of Blimp-1, expands the secretory pathway apparatus and other organelles, and increases protein synthesis in plasma membrane cell differentiation Immunity 2004, 21:81-93. 10.1016/j.immuni.2004.06.010 15345222
27. Gass JN Gifford NM Brewer JW Activation of an unfolded protein response during differentiation of antibody-secreting B cells J Biol Chem 2002, 277:49047-49054. 10.1074/jbc.M205011200 12374812
28. Travers KJ Patil CK Wodicka L Lochhart DJ Weissmann JS Walter P Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation Cell 2000, 101:249-258. 10.1016/S0092-8674(00)80835-1 10847680
29. Kitama Y Ishiwata-Kitama Y Yamada S Kohno K Yeast unfolded protein response pathway regulates expression of genes for anti-oxidative stress and cell surface proteins Genes Cells 2006, 11:59-69. 10.1111/ j.1365-2443.2005.00921.x 16371132
30. Chang HJ Jesch SA Gaspar ML Henry SA Role of the unfolded protein response pathway in secretory stress and regulation of ino1 expression in Saccharomyces cerevisiae Genetics 2004, 168:1899-1913. 1448725 15371354 10.1534/genetics.104.032961
31. Goodman AG Smith JA Balachandran S Perwitasari O Proll SC Thomas MJ Korth Mj Barber GN Schiff LA Katze MG The cellular protein P58IPK regulates influenza virus mRNA translation and replication through a PKR-mediated mechanism J Virol 2007, 81:2221-2230. 1865913 17166899 10.1128/JVI.02151-06
32. Tvegård T Soltani H Skjølberg HC Krohn M Nilssen EA Kearsey BG Grallert B Boye E A novel checkpoint mechanism regulating the G1/S transition Genes Dev 2007, 21:649-654. 1820939 17369398 10.1101/ gad.421807
33. Tournu H Tripathi G Bertram G Macaskill S Mavor A Walker L Odds FC Gow NAR Brown AJP Global role of the protein kinase Gcn2 in the human pathogen Candida albicans Eukaryotic Cell 2005, 4:1687-1696. 1265895 16215176 10.1128/EC.4.10.1687-1696.2005
34. Patil CK Li H Walter P Gcn4p and novel upstream activating sequences regulate targets of the unfolded protein response PLOS biol 2004, 2:e246. 509306 15314660 10.1371/journal.pbio.0020246
35. Broadhurst MK Lee RSF Hawkins S Wheeler T The p100 EBNA-2 coactivator: A highly conserved protein found in a range of exocrine and endocrine cells and tissues in cattle Biochim Biophys Acta 2005, 1681:126-133. 15627504
36. Keenan TW Winter S Rackwitz HR Heid HW Nuclear coactivator protein p100 is present in endoplasmic reticulum and lipid droplets of milk secreting cells Biochim Biophys Acta 2000, 1523:84-90. 11099861
37. Arvas M Pakula T Lanthaler K Saloheimo M Valkonen M Suortti T Robson G Penttilä M Common features and interesting transcriptional responses to secretion stress in the fungi Trichoderma reesei and Saccharomyces cerevisiae BMC Genomics 7:32. 1397821 16504068 10.1186/ 1471-2164-7-32
38. Van Gorcom RFM Analysis of gene expression in Aspergillus PhD thesis University of Amsterdam 1997.
39. Frenken LG Hessing JG Hondel van den CA Verrips CT Recent advances in the large-scale production of antibody fragments using lower eukaryotic microorganisms Res Immunol 1998, 149:589-599. 10.1016/ S0923-2494(98)80011-4 9835423
40. Vishniac W Santer M The thiobacilli Bacteriol Rev 1957, 21:195-213. 180898 13471458
41. Larsen B Rask Poulsen B Eriksen NT Lønsmann Iversen JJ Homogeneous batch cultures of Aspergillus oryzae by elimination of wall growth in the Variomixing bioreactor Appl Microbiol Biotechnol 2004, 64:192-198. 10.1007/s00253-003-1437-x 14556039
42. Jørgensen TR vanKuyk PA Poulsen BR Ruijter GJG Visser J Iversen JJL Glucose uptake and growth of glucose-limited chemostat cultures of Aspergillus niger and a disruptant lacking MstA, a high-affinity glucose transporter Microbiology 2007, 153:1963-1973. 10.1099/mic.0.2006/ 005090-0 17526853
43. Iversen JJL Thomsen JK Cox RP On-line growth measurements in bioreactors by titrating metabolic proton exchange Appl Microbiol Biotechnol 1994, 42:256-262. 10.1007/BF00902726
44. Iversen JJL A rapid sampling valve with minimal dead space for laboratory scale fermenters Biotechnol Bioeng 1981, 23:437-440. 10.1002/ bit.260230218
45. Standing CN Fredrickson AG Tsuchiya HM Batch- and continuous-culture transients for two substrate systems Appl Microbiol 1972, 23:354-359. 380344 4552891
46. Beutler HO Maltose Methods of Enzymatic Analysis Weinheim: Verlag Chemie Bergmeyer HU 1983, VI:119-126.
47. Bergmeyer HU Bernt E Schmidt F Stork H Glucose Methods of Enzymatic Analysis New York: Academic Press Bergmeyer HU 1974, 3:1196-1201.
48. Kristensen E Andersen FØ Determination of organic carbon in marine sediments: A comparison of two CHN-analyzer methods J Exp Mar Biol Ecol 1987, 109:15-23. 10.1016/0022-0981(87)90182-1
49. GeneChip Expression Analysis Technical Manual Affymetrix, inc 2002
50. Benjamini Y Hochberg Y Controlling the False Discovery Rate: A practical and powerful approach to multiple testing J Royal Stat Soc B 1995, 57:289-300.