A carrier fusion significantly induces unfolded protein response in heterologous protein production by Aspergillus oryzae

Applied Microbiology and Biotechnology

Volumn 92, Issue 6, 2011, Pages 1197-1206

  Ohno, Ayako ^a   Maruyama, Jun Ichi ^a   Nemoto, Takashi ^a   Arioka, Manabu ^a   Kitamoto, Katsuhiko ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Aspergillus oryzae; Carrier; ER; Heterologous protein production; UPR

Indexed keywords

ASPERGILLUS ORYZAE; CARRIER; CHYMOSIN; CLEAVAGE SITES; DNA MICROARRAY ANALYSIS; EARLY GROWTH; ENDOPLASMIC RETICULUM; EXTRACELLULAR; FILAMENTOUS FUNGI; GENE EXPRESSION PATTERNS; HETEROLOGOUS PROTEIN PRODUCTION; HOST STRAIN; PHYSIOLOGICAL EFFECTS; PRODUCTION LEVEL; PRODUCTION YIELD; TARGET PROTEINS; UNFOLDED PROTEIN RESPONSE; UPR;

ASPERGILLUS; CELL MEMBRANES; ERBIUM; GENE EXPRESSION; PHYSIOLOGY;

PROTEINS;

AMYLASE; CHYMOSIN;

FUNGUS; GENE EXPRESSION; GENETIC ANALYSIS; MOLECULAR ANALYSIS; PHYSIOLOGICAL RESPONSE; PROTEIN; SECRETION;

ARTICLE; ASPERGILLUS ORYZAE; CONTROLLED STUDY; DNA MICROARRAY; ENDOPLASMIC RETICULUM; GENE EXPRESSION; GENE FUSION; GOLGI COMPLEX; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN MICROARRAY; PROTEIN SECRETION; UNFOLDED PROTEIN RESPONSE;

ANIMALS; ASPERGILLUS ORYZAE; CATTLE; CHYMOSIN; ENDOPLASMIC RETICULUM; GENE EXPRESSION; GENE EXPRESSION REGULATION, FUNGAL; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; UNFOLDED PROTEIN RESPONSE;

ASPERGILLUS ORYZAE; BOVINAE; FUNGI;

EID: 82455210919     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-011-3487-9     Document Type: Article

References (38)

1. T Akao M Sano O Yamada T Akeno K Fujii K Goto S Ohashi-Kunihiro K Takase M Yasukawa-Watanabe K Yamaguchi Y Kurihara J Maruyama PR Juvvadi A Tanaka Y Hata Y Koyama S Yamaguchi N Kitamoto K Gomi K Abe M Takeuchi T Kobayashi H Horiuchi K Kitamoto Y Kashiwagi M Machida O Akita 2007 Analysis of expressed sequence tags from the fungus Aspergillus oryzae cultured under different conditions DNA Res 14 47 57 10.1093/dnares/dsm008 1:CAS:528:DC%2BD2sXot1OktLY%3D
2. M Arvas T Pakula K Lanthaler M Saloheimo M Valkonen T Suortti G Robson M Penttilä 2006 Common features and interesting differences in transcriptional responses to secretion stress in the fungi Trichoderma reesei and Saccharomyces cerevisiae BMC Genomics 7 32 10.1186/1471-2164-7-32 (Pubitemid 43380727)
3. NJ Bryant A Boyd 1993 Immunoisolation of Kex2p-containing organelles from yeast demonstrates colocalisation of three processing proteinases to a single Golgi compartment J Cell Sci 106 815 822 1:CAS:528:DyaK2cXivFelt74%3D (Pubitemid 23346794)
4. RJ Gouka PJ Punt CA van den Hondel 1997 Glucoamylase gene fusions alleviate limitations for protein production in Aspergillus awamori at the transcriptional and (post) translational levels Appl Environ Microbiol 63 488 497 1:CAS:528:DyaK2sXhtVKktbo%3D (Pubitemid 27121329)
5. T Guillemette NN van Peij T Goosen K Lanthaler GD Robson CA van den Hondel H Stam DB Archer 2007 Genomic analysis of the secretion stress response in the enzyme-producing cell factory Aspergillus niger BMC Genomics 8 158 10.1186/1471-2164-8-158 (Pubitemid 46993520)
6. K Ito T Asakura Y Morita K Nakajima A Koizumi A Shimizu-Ibuka K Masuda M Ishiguro T Terada J Maruyama K Kitamoto T Misaka K Abe 2007 Microbial production of sensory-active miraculin Biochem Biophys Res Commun 360 407 411 10.1016/j.bbrc.2007.06.064 1:CAS:528:DC%2BD2sXnslSqtbo%3D (Pubitemid 47030359)
7. R Jalving PJ van de Vondervoort J Visser PJ Schaap 2000 Characterization of the kexin-like maturase of Aspergillus niger Appl Environ Microbiol 66 363 336 10.1128/AEM.66.1.363-368.2000 1:CAS:528:DC%2BD3cXktlSrsQ%3D%3D
8. FJ Jin J Maruyama PR Juvvadi M Arioka K Kitamoto 2004 Development of a novel quadruple auxotrophic host transformation system by argB gene disruption using adeA gene and exploiting adenine auxotrophy in Aspergillus oryzae FEMS Microbiol Lett 239 79 85 10.1016/j.femsle.2004.08.025 1:CAS:528: DC%2BD2cXnvV2ltLo%3D (Pubitemid 39296719)
9. FJ Jin T Watanabe PR Juvvadi J Maruyama M Arioka K Kitamoto 2007 Double disruption of the proteinase genes, tppA and pepE, increases the production level of human lysozyme by Aspergillus oryzae Appl Microbiol Biotechnol 76 1059 1068 10.1007/s00253-007-1088-4 1:CAS:528:DC%2BD2sXhtVCns7%2FF (Pubitemid 47415619)
10. T Kasuya H Nakajima K Kitamoto 1999 Cloning and characterization of the bipA gene encoding ER chaperone BiP from Aspergillus oryzae J Biosci Bioeng 88 472 478 10.1016/S1389-1723(00)87661-6 1:CAS:528:DC%2BD3cXks1aqsA%3D%3D (Pubitemid 30000557)
11. S Kimura J Maruyama M Takeuchi K Kitamoto 2008 Monitoring global gene expression of proteases and improvement of human lysozyme production in nptB gene disruptant of Aspergillus oryzae Biosci Biotechnol Biochem 72 499 502 10.1271/bbb.70582 1:CAS:528:DC%2BD1cXjsVWrsrw%3D (Pubitemid 351353688)
12. S Kimura J Maruyama T Kikuma M Arioka K Kitamoto 2011 Autophagy delivers misfolded secretory proteins accumulated in endoplasmic reticulum to vacuoles in the filamentous fungus Aspergillus oryzae Biochem Biophys Res Commun 406 464 470 10.1016/j.bbrc.2011.02.075 1:CAS:528:DC%2BC3MXjsFKmtLc%3D
13. K Kitamoto 2002 Molecular biology of the Koji molds Adv Appl Microbiol 51 129 153 10.1016/S0065-2164(02)51004-2 1:CAS:528:DC%2BD38XotFOgu7k%3D (Pubitemid 34987559)
14. BR Lee O Yamada K Kitamoto K Takahashi 1996 Cloning, characterization and overexpression of a gene (pdiA) encoding protein disulfide isomerase of Aspergillus oryzae J Ferment Bioeng 82 538 543 10.1016/S0922-338X(97)81248-2 1:CAS:528:DyaK2sXisVCrtg%3D%3D (Pubitemid 27044261)
15. Y Mabashi T Kikuma J Maruyama M Arioka K Kitamoto 2006 Development of a versatile expression plasmid construction system for Aspergillus oryzae and its application to visualization of mitochondria Biosci Biotechnol Biochem 70 1882 1889 10.1271/bbb.60052 1:CAS:528:DC%2BD28Xpsl2htrc%3D (Pubitemid 44285421)
16. M Machida K Asai M Sano T Tanaka T Kumagai G Terai K Kusumoto T Arima O Akita Y Kashiwagi K Abe K Gomi H Horiuchi K Kitamoto T Kobayashi M Takeuchi DW Denning JE Galagan WC Nierman J Yu DB Archer JW Bennett D Bhatnagar TE Cleveland ND Fedorova O Gotoh H Horikawa A Hosoyama M Ichinomiya R Igarashi K Iwashita PR Juvvadi M Kato Y Kato T Kin A Kokubun H Maeda N Maeyama J Maruyama H Nagasaki T Nakajima K Oda K Okada I Paulsen K Sakamoto T Sawano M Takahashi K Takase Y Terabayashi JR Wortman O Yamada Y Yamagata H Anazawa Y Hata Y Koide T Komori Y Koyama T Minetoki S Suharnan A Tanaka K Isono S Kuhara N Ogasawara H Kikuchi 2005 Genome sequencing and analysis of Aspergillus oryzae Nature 438 1157 1161 10.1038/nature04300 (Pubitemid 41831685)
17. J Maruyama K Kitamoto 2008 Multiple gene disruptions by marker recycling with highly efficient gene-targeting background (DeltaligD) in Aspergillus oryzae Biotechnol Lett 30 1811 1817 10.1007/s10529-008-9763-9 1:CAS:528:DC%2BD1cXhtVWnsr%2FP
18. T Minetoki Y Nunokawa K Gomi K Kitamoto C Kumagai G Tamura 1996 Deletion analysis of promoter elements of the Aspergillus oryzae agdA gene encoding alpha-glucosidase Curr Genet 30 432 438 10.1007/s002940050153 1:CAS:528:DyaK28XnsVajtr8%3D (Pubitemid 26402482)
19. HJ Mulder I Nikolaev SM Madrid 2006 HACA, the transcriptional activator of the unfolded protein response (UPR) in Aspergillus niger, binds to partly palindromic UPR elements of the consensus sequence 5′-CAN(G/A)NTGT/GCCT- 3′ Fungal Genet Biol 43 560 572 10.1016/j.fgb.2006.02.005 1:CAS:528:DC%2BD28XmslGqsbw%3D
20. K Nakajima T Asakura J Maruyama Y Morita H Oike A Shimizu-Ibuka T Misaka H Sorimachi S Arai K Kitamoto K Abe 2006 Extracellular production of neoculin, a sweet-tasting heterodimeric protein with taste-modifying activity, by Aspergillus oryzae Appl Environ Microbiol 72 3716 3723 10.1128/AEM.72.5.3716- 3723.2006 1:CAS:528:DC%2BD28XkvFWjt7k%3D (Pubitemid 43728030)
21. T Nemoto J Maruyama K Kitamoto 2009 Improvement of heterologous protein production in Aspergillus oryzae by RNA interference of α-amylase genes Biosci Biotech Biochem 73 2370 2373 10.1271/bbb.90177 1:CAS:528: DC%2BC3cXis1Oisw%3D%3D
22. T Nemoto T Watanabe Y Mizogami J Maruyama K Kitamoto 2009 Isolation of Aspergillus oryzae mutants for heterologous protein production from a double proteinase gene disruptant Appl Microbiol Biotechnol 82 1105 1114 10.1007/s00253-008-1851-1 1:CAS:528:DC%2BD1MXjvFeisrY%3D
23. C Ngiam DJ Jeenes PJ Punt CA van den Hondel DB Archer 2000 Characterization of a foldase, protein disulfide isomerase A, in the protein secretory pathway of Aspergillus niger Appl Environ Microbiol 66 775 782 10.1128/AEM.66.2.775-782.2000 1:CAS:528:DC%2BD3cXhtFeqsL0%3D (Pubitemid 30082773)
24. VB Pedersen KA Christensen B Foltmann 1979 Investigations on the activation of bovine prochymosin Eur J Biochem 94 573 580 10.1111/j.1432-1033. 1979.tb12927.x 1:STN:280:DyaE1M7kvVCisg%3D%3D (Pubitemid 9236105)
25. PJ Punt IA van Gemeren J Drint-Kuijvenhoven JG Hessing GM van Muijlwijk-Harteveld A Beijersbergen CT Verrips CA van den Hondel 1998 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 50 447 454 10.1007/s002530051319 1:CAS:528:DyaK1cXnsVKlur4%3D (Pubitemid 28509222)
26. PJ Punt A Drint-Kuijvenhoven BC Lokman JA Spencer D Jeenes DA Archer CA van den Hondel 2003 The role of the Aspergillus niger furin-type protease gene in processing of fungal proproteins and fusion proteins. Evidence for alternative processing of recombinant (fusion-) proteins J Biotechnol 106 23 32 10.1016/j.jbiotec.2003.09.005 1:CAS:528:DC%2BD3sXptVGrt78%3D (Pubitemid 37421370)
27. D Ron P Walter 2007 Signal integration in the endoplasmic reticulum unfolded protein response Nat Rev Mol Cell Biol 8 519 529 10.1038/nrm2199 1:CAS:528:DC%2BD2sXmvVaktLY%3D (Pubitemid 46985379)
28. AH Sims ME Gent K Lanthaler NS Dunn-Coleman SG Oliver GD Robson 2005 Transcriptome analysis of recombinant protein secretion by Aspergillus nidulans and the unfolded-protein response in vivo Appl Environ Microbiol 71 2737 2747 10.1128/AEM.71.5.2737-2747.2005 1:CAS:528:DC%2BD2MXktFKlsrk%3D (Pubitemid 40647021)
29. K Tsuchiya T Nagashima Y Yamamoto K Gomi K Kitamoto C Kumagai G Tamura 1994 High level secretion of calf chymosin using a glucoamylase-prochymosin fusion gene in Aspergillus oryzae Biosci Biotechnol Biochem 58 895 899 10.1271/bbb.58.895 1:CAS:528:DyaK2cXksFGqtbk%3D (Pubitemid 2108811)
30. M Valkonen M Ward H Wang M Penttilä M Saloheimo 2003 Improvement of foreign-protein production in Aspergillus niger var. awamori by constitutive induction of the unfolded-protein response Appl Environ Microbiol 69 6979 6986 10.1128/AEM.69.12.6979-6986.2003 1:CAS:528:DC%2BD3sXpvFCmur4%3D (Pubitemid 38585342)
31. IA van Gemeren PJ Punt A Drint-Kuyvenhoven MP Broekhuijsen A van't Hoog A Beijersbergen CT Verrips CA van den Hondel 1997 The ER chaperone encoding bipA gene of black Aspergilli is induced by heat shock and unfolded proteins Gene 198 43 52 10.1016/S0378-1119(97)00290-4 (Pubitemid 27453724)
32. H Wang M Ward 2000 Molecular characterization of a PDI-related gene prpA in Aspergillus niger var. awamori Curr Genet 37 57 64 10.1007/s002940050009 1:CAS:528:DC%2BD3cXitFaqtg%3D%3D (Pubitemid 30160679)
33. H Wang J Entwistle E Morlon DB Archer JF Peberdy M Ward DJ Jeenes 2003 Isolation and characterisation of a calnexin homologue, clxA, from Aspergillus niger Mol Genet Genomics 268 684 691 1:CAS:528:DC%2BD3sXhtFSmsbY%3D (Pubitemid 36286512)
34. T Watanabe I Matsuo J Maruyama K Kitamoto Y Ito 2007 Identification and characterization of an intracellular lectin, calnexin, from Aspergillus oryzae using N-glycan-conjugated beads Biosci Biotechnol Biochem 71 2688 2696 10.1271/bbb.70289 1:CAS:528:DC%2BD2sXhsVWrs77I (Pubitemid 350164252)
35. O Yamada BR Lee K Gomi Y Iimura 1999 Cloning and functional analysis of the Aspergillus oryzae conidiation regulator gene brlA by its disruption and misscheduled expression J Biosci Bioeng 87 424 429 10.1016/S1389-1723(99)80089-9 1:CAS:528:DyaK1MXkvFajsbs%3D (Pubitemid 29239002)
36. J Yoon S Kimura J Maruyama K Kitamoto 2009 Construction of quintuple protease gene disruptant for heterologous protein production in Aspergillus oryzae Appl Microbiol Biotechnol 82 691 701 10.1007/s00253-008-1815-5 1:CAS:528:DC%2BD1MXisVWktb0%3D
37. J Yoon T Aishan J Maruyama K Kitamoto 2010 Enhanced production and secretion of heterologous proteins by the filamentous fungus Aspergillus oryzae via disruption of vacuolar protein sorting receptor gene Aovps10 Appl Environ Microbiol 76 5718 5727 10.1128/AEM.03087-09 1:CAS:528:DC%2BC3cXht1Wms7nL
38. J Yoon J Maruyama K Kitamoto 2011 Disruption of ten protease genes in the filamentous fungus Aspergillus oryzae highly improves production of heterologous proteins Appl Microbiol Biotechnol 89 747 759 10.1007/s00253-010- 2937-0 1:CAS:528:DC%2BC3MXnsVWktg%3D%3D