The cargo and the transport system: secreted proteins and protein secretion in () Open Access

Abstract

() is an efficient cell factory for protein production that is exploited by the enzyme industry. Yields of over 100 g secreted protein l from industrial fermentations have been reported. In this review we discuss the spectrum of proteins secreted by and the studies carried out on its protein secretion system. The major enzymes secreted by under production conditions are those degrading plant polysaccharides, the most dominant ones being the major cellulases, as demonstrated by the 2D gel analysis of the secretome. According to genome analysis, has fewer genes encoding enzymes involved in plant biomass degradation compared with other fungi with sequenced genomes. We also discuss other secreted enzymes and proteins that have been studied, such as proteases, laccase, tyrosinase and hydrophobins. Investigation of the secretion pathway has included molecular characterization of the pathway components functioning at different stages of the secretion process as well as analysis of the stress responses caused by impaired folding or trafficking in the pathway or by expression of heterologous proteins. Studies on the transcriptional regulation of the secretory pathway have revealed similarities, but also interesting differences, with other organisms, such as a different induction mechanism of the unfolded protein response and the repression of genes encoding secreted proteins under secretion stress conditions.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.053132-0
2012-01-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/1/46.html?itemId=/content/journal/micro/10.1099/mic.0.053132-0&mimeType=html&fmt=ahah

References

  1. Aalto M. K., Ronne H., Keränen S. ( 1993). Yeast syntaxins Sso1p and Sso2p belong to a family of related membrane proteins that function in vesicular transport. EMBO J 12:4095–4104[PubMed]
    [Google Scholar]
  2. Al-Sheikh H., Watson A. J., Lacey G. A., Punt P. J., MacKenzie D. A., Jeenes D. J., Pakula T., Penttilä M., Alcocer M. J. C., Archer D. B. ( 2004). Endoplasmic reticulum stress leads to the selective transcriptional downregulation of the glucoamylase gene in Aspergillus niger . Mol Microbiol 53:1731–1742 [View Article][PubMed]
    [Google Scholar]
  3. Aro N., Pakula T., Penttilä M. ( 2005). Transcriptional regulation of plant cell wall degradation by filamentous fungi. FEMS Microbiol Rev 29:719–739 [View Article][PubMed]
    [Google Scholar]
  4. Arvas M., Pakula T., Lanthaler K., Saloheimo M., Valkonen M., Suortti T., Robson G., Penttilä M. ( 2006). Common features and interesting differences in transcriptional responses to secretion stress in the fungi Trichoderma reesei and Saccharomyces cerevisiae . BMC Genomics 7:32 [View Article][PubMed]
    [Google Scholar]
  5. Askolin S., Penttilä M., Wösten H. A., Nakari-Setälä T. ( 2005). The Trichoderma reesei hydrophobin genes hfb1 and hfb2 have diverse functions in fungal development. FEMS Microbiol Lett 253:281–288 [View Article][PubMed]
    [Google Scholar]
  6. Bernasconi R., Molinari M. ( 2011). ERAD and ERAD tuning: disposal of cargo and of ERAD regulators from the mammalian ER. Curr Opin Cell Biol 23:176–183 [View Article][PubMed]
    [Google Scholar]
  7. Cherry J. R., Fidantsef A. L. ( 2003). Directed evolution of industrial enzymes: an update. Curr Opin Biotechnol 14:438–443 [View Article][PubMed]
    [Google Scholar]
  8. Chundawat S. P. S., Lipton M. S., Purvine S. O., Uppugundla N., Gao D., Balan V., Dale B. E. ( 2011). Proteomics-based compositional analysis of complex cellulase–hemicellulase mixtures. J Proteome Res 10:4365–4372 [View Article][PubMed]
    [Google Scholar]
  9. Collén A., Saloheimo M., Bailey M., Penttilä M., Pakula T. M. ( 2005). Protein production and induction of the unfolded protein response in Trichoderma reesei strain Rut-C30 and its transformant expressing endoglucanase I with a hydrophobic tag. Biotechnol Bioeng 89:335–344 [View Article][PubMed]
    [Google Scholar]
  10. Conesa A., Punt P. J., van Luijk N., van den Hondel C. A. ( 2001). The secretion pathway in filamentous fungi: a biotechnological view. Fungal Genet Biol 33:155–171 [View Article][PubMed]
    [Google Scholar]
  11. Cox J. S., Walter P. ( 1996). A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87:391–404 [View Article][PubMed]
    [Google Scholar]
  12. Dienes D., Börjesson J., Hägglund P., Tjerneld F., Lidén G., Réczey K., Stålbrand H. ( 2007). Identification of a trypsin-like serine protease from Trichoderma reesei QM9414. Enzyme Microb Technol 40:1087–1094 [View Article]
    [Google Scholar]
  13. Divne C., Ståhlberg J., Teeri T. T., Jones T. A. ( 1998). High-resolution crystal structures reveal how a cellulose chain is bound in the 50 Å long tunnel of cellobiohydrolase I from Trichoderma reesei . J Mol Biol 275:309–325 [View Article][PubMed]
    [Google Scholar]
  14. Foreman P. K., Brown D., Dankmeyer L., Dean R., Diener S., Dunn-Coleman N. S., Goedegebuur F., Houfek T. D., England G. J. & other authors ( 2003). Transcriptional regulation of biomass-degrading enzymes in the filamentous fungus Trichoderma reesei . J Biol Chem 278:31988–31997 [View Article][PubMed]
    [Google Scholar]
  15. Fryksdale B. G., Jedrzejewski P. T., Wong D. L., Gaertner A. L., Miller B. S. ( 2002). Impact of deglycosylation methods on two-dimensional gel electrophoresis and matrix assisted laser desorption/ionization-time of flight-mass spectrometry for proteomic analysis. Electrophoresis 23:2184–2193 [View Article][PubMed]
    [Google Scholar]
  16. Ghosh A., Al-Rabiai S., Ghosh B. K., Trimiño-Vazquez H., Eveleigh D. E., Montenecourt B. S. ( 1982). Increased endoplasmic reticulum content of a mutant of Trichoderma reesei (RUT-C30) in relation to cellulase synthesis. Enzyme Microb Technol 4:110–113 [View Article]
    [Google Scholar]
  17. Harkki A., Uusitalo J., Bailey M., Penttilä M., Knowles J. K. C. ( 1989). A novel fungal expression system: secretion of active calf chymosin from the filamentous fungus Trichoderma reesei . Bio/Technology 7:596–603 [View Article]
    [Google Scholar]
  18. Harrison M. J., Nouwens A. S., Jardine D. R., Zachara N. E., Gooley A. A., Nevalainen H., Packer N. H. ( 1998). Modified glycosylation of cellobiohydrolase I from a high cellulase-producing mutant strain of Trichoderma reesei. Eur J Biochem 256:119–127 [View Article][PubMed]
    [Google Scholar]
  19. Harrison M. J., Wathugala I. M., Tenkanen M., Packer N. H., Nevalainen K. M. H. ( 2002). Glycosylation of acetylxylan esterase from Trichoderma reesei . Glycobiology 12:291–298 [View Article][PubMed]
    [Google Scholar]
  20. Hayakawa Y., Ishikawa E., Shoji J. Y., Nakano H., Kitamoto K. ( 2011). Septum-directed secretion in the filamentous fungus Aspergillus oryzae . Mol Microbiol 81:40–55 [View Article][PubMed]
    [Google Scholar]
  21. He B., Guo W. ( 2009). The exocyst complex in polarized exocytosis. Curr Opin Cell Biol 21:537–542 [View Article][PubMed]
    [Google Scholar]
  22. Herpoël-Gimbert I., Margeot A., Dolla A., Jan G., Mollé D., Lignon S., Mathis H., Sigoillot J.-C., Monot F., Asther M. ( 2008). Comparative secretome analyses of two Trichoderma reesei RUT-C30 and CL847 hypersecretory strains. Biotechnol Biofuels 1:18 [View Article][PubMed]
    [Google Scholar]
  23. Hetz C., Glimcher L. H. ( 2009). Fine-tuning of the unfolded protein response: Assembling the IRE1α interactome. Mol Cell 35:551–561 [View Article][PubMed]
    [Google Scholar]
  24. Hutagalung A. H., Novick P. J. ( 2011). Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91:119–149 [View Article][PubMed]
    [Google Scholar]
  25. Joutsjoki V. V., Kuittinen M., Torkkeli T. K., Suominen P. L. ( 1993). Secretion of the Hormoconis resinae glucoamylase P enzyme from Trichoderma reesei directed by the natural and the cbh1 gene secretion signal. FEMS Microbiol Lett 112:281–286 [View Article][PubMed]
    [Google Scholar]
  26. Kienle N., Kloepper T. H., Fasshauer D. ( 2009). Phylogeny of the SNARE vesicle fusion machinery yields insights into the conservation of the secretory pathway in fungi. BMC Evol Biol 9:19 [View Article][PubMed]
    [Google Scholar]
  27. Kisko K., Szilvay G., Vuorimaa E., Lemmetyinen H., Linder M., Torkkeli M., Serimaa R. ( 2007). Self-assembled films of hydrophobin protein HFBIII from Trichoderma reesei . J Appl Cryst 40:Suppl. 1S355–S360 [View Article]
    [Google Scholar]
  28. Kontkanen H., Westerholm-Parvinen A., Saloheimo M., Bailey M., Rättö M., Mattila I., Mohsina M., Kalkkinen N., Nakari-Setälä T., Buchert J. ( 2009). Novel Coprinopsis cinerea polyesterase that hydrolyzes cutin and suberin. Appl Environ Microbiol 75:2148–2157 [View Article][PubMed]
    [Google Scholar]
  29. Kubicek C. P., Baker S., Gamauf C., Kenerley C. M., Druzhinina I. S. ( 2008). Purifying selection and birth-and-death evolution in the class II hydrophobin gene families of the ascomycete Trichoderma/Hypocrea . BMC Evol Biol 8:4 [View Article][PubMed]
    [Google Scholar]
  30. Kubicek C. P., Mikus M., Schuster A., Schmoll M., Seiboth B. ( 2009). Metabolic engineering strategies for the improvement of cellulase production by Hypocrea jecorina . Biotechnol Biofuels 2:19 [View Article][PubMed]
    [Google Scholar]
  31. Levasseur A., Saloheimo M., Navarro D., Andberg M., Pontarotti P., Kruus K., Record E. ( 2010). Exploring laccase-like multicopper oxidase genes from the ascomycete Trichoderma reesei: a functional, phylogenetic and evolutionary study. BMC Biochem 11:32 [View Article][PubMed]
    [Google Scholar]
  32. Linder M. ( 2009). Hydrophobins: proteins that self assemble at interfaces. Curr Opin Colloid Interface Sci 14:356–363 [View Article]
    [Google Scholar]
  33. Linder M. B., Qiao M., Laumen F., Selber K., Hyytiä T., Nakari-Setälä T., Penttilä M. E. ( 2004). Efficient purification of recombinant proteins using hydrophobins as tags in surfactant-based two-phase systems. Biochemistry 43:11873–11882 [View Article][PubMed]
    [Google Scholar]
  34. Malhotra J. D., Kaufman R. J. ( 2007). The endoplasmic reticulum and the unfolded protein response. Semin Cell Dev Biol 18:716–731 [View Article][PubMed]
    [Google Scholar]
  35. Malsam J., Kreye S., Söllner T. H. ( 2008). Membrane fusion: SNAREs and regulation. Cell Mol Life Sci 65:2814–2832 [View Article][PubMed]
    [Google Scholar]
  36. Mäntylä A., Paloheimo M., Suominen P. ( 1998). Industrial mutants and recombinant strains of Trichoderma reesei . Trichoderma and Gliogladium vol. 2291–304 Harman G. E., Kubicek C. London: Taylor and Francis;
    [Google Scholar]
  37. Maras M., De Bruyn A., Schraml J., Herdewijn P., Claeyssens M., Fiers W., Contreras R. ( 1997). Structural characterization of N-linked oligosaccharides from cellobiohydrolase I secreted by the filamentous fungus Trichoderma reesei RUTC 30. Eur J Biochem 245:617–625 [View Article][PubMed]
    [Google Scholar]
  38. Margolles-Clark E., Hayes C. K., Harman G. E., Penttilä M. ( 1996). Improved production of Trichoderma harzianum endochitinase by expression in Trichoderma reesei . Appl Environ Microbiol 62:2145–2151[PubMed]
    [Google Scholar]
  39. Martinez D., Berka R. M., Henrissat B., Saloheimo M., Arvas M., Baker S. E., Chapman J., Chertkov O., Coutinho P. M. & other authors ( 2008). Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 26:553–560 [View Article][PubMed]
    [Google Scholar]
  40. Matsui Y., Toh-E A. ( 1992). Yeast RHO3 and RHO4 ras superfamily genes are necessary for bud growth, and their defect is suppressed by a high dose of bud formation genes CDC42 and BEM1. Mol Cell Biol 12:5690–5699[PubMed]
    [Google Scholar]
  41. Mattinen M. L., Lantto R., Selinheimo E., Kruus K., Buchert J. ( 2008). Oxidation of peptides and proteins by Trichoderma reesei and Agaricus bisporus tyrosinases. J Biotechnol 133:395–402 [View Article][PubMed]
    [Google Scholar]
  42. Montenecourt B., Eveleigh D. ( 1979). Selective screening methods for the isolation of high yielding cellulase mutants of Trichoderma reesei . Adv Chem Ser 181:289–301 [View Article]
    [Google Scholar]
  43. Nakańo A., Muramatsu M. ( 1989). A novel GTP-binding protein, Sar1p, is involved in transport from the endoplasmic reticulum to the Golgi apparatus. J Cell Biol 109:2677–2691 [View Article][PubMed]
    [Google Scholar]
  44. Nakari-Setälä T., Aro N., Kalkkinen N., Alatalo E., Penttilä M. ( 1996). Genetic and biochemical characterization of the Trichoderma reesei hydrophobin HFBI. Eur J Biochem 235:248–255 [View Article][PubMed]
    [Google Scholar]
  45. Nakari-Setälä T., Aro N., Ilmén M., Muñoz G., Kalkkinen N., Penttilä M. ( 1997). Differential expression of the vegetative and spore-bound hydrophobins of Trichoderma reesei – cloning and characterization of the hfb2 gene. Eur J Biochem 248:415–423 [View Article][PubMed]
    [Google Scholar]
  46. Nevalainen H., Penttilä M. ( 2004). Molecular biology of cellulolytic fungi. The Mycota II, Genetics and Biotechnology, 2nd edn.369–390 Kück U. Berlin, Heidelberg: Springer-Verlag;
    [Google Scholar]
  47. Nevalainen H., Te’o V., Penttilä M. ( 2004). Application of genetic engineering for strain improvement in filamentous fungi. Handbook of Fungal Biotechnology193–208 Arora D. K. New York, Basel: Marcel Dekker; [View Article]
    [Google Scholar]
  48. Nevalainen H., Te’o V., Penttilä M., Pakula T. 2005; Heterologous gene expression in filamentous fungi: a holistic view. Applied Mycology and Biotechnology, Genes and Genomics vol. 5211–237 Arora D. K., Berka R. Amsterdam, The Netherlands: Elsevier;
    [Google Scholar]
  49. Nykänen M. ( 2002). Protein secretion in Trichoderma reesei. Expression, secretion and maturation of cellobiohydrolase I, barley cysteine proteinase and calf chymosin in Rut-C30 .
    [Google Scholar]
  50. Nykänen M., Saarelainen R., Raudaskoski M., Nevalainen K., Mikkonen A. ( 1997). Expression and secretion of barley cysteine endopeptidase B and cellobiohydrolase I in Trichoderma reesei . Appl Environ Microbiol 63:4929–4937[PubMed]
    [Google Scholar]
  51. Nykänen M. J., Raudaskoski M., Nevalainen H., Mikkonen A. ( 2002). Maturation of barley cysteine endopeptidase expressed in Trichoderma reesei is distorted by incomplete processing. Can J Microbiol 48:138–150 [View Article][PubMed]
    [Google Scholar]
  52. Nyyssönen E., Penttilä M., Harkki A., Saloheimo A., Knowles J. K. C., Keränen S. ( 1993). Efficient production of antibody fragments by the filamentous fungus Trichoderma reesei . Biotechnology (N Y) 11:591–595 [View Article][PubMed]
    [Google Scholar]
  53. Pakula T. M., Uusitalo J., Saloheimo M., Salonen K., Aarts R. J., Penttilä M. ( 2000). Monitoring the kinetics of glycoprotein synthesis and secretion in the filamentous fungus Trichoderma reesei: cellobiohydrolase I (CBHI) as a model protein. Microbiology 146:223–232[PubMed]
    [Google Scholar]
  54. Pakula T. M., Laxell M., Huuskonen A., Uusitalo J., Saloheimo M., Penttilä M. ( 2003). The effects of drugs inhibiting protein secretion in the filamentous fungus Trichoderma reesei. Evidence for down-regulation of genes that encode secreted proteins in the stressed cells. J Biol Chem 278:45011–45020 [View Article][PubMed]
    [Google Scholar]
  55. Pakula T. M., Salonen K., Uusitalo J., Penttilä M. ( 2005). The effect of specific growth rate on protein synthesis and secretion in the filamentous fungus Trichoderma reesei . Microbiology 151:135–143 [View Article][PubMed]
    [Google Scholar]
  56. Paloheimo M., Mäntylä A., Kallio J., Suominen P. ( 2003). High-yield production of a bacterial xylanase in the filamentous fungus Trichoderma reesei requires a carrier polypeptide with an intact domain structure. Appl Environ Microbiol 69:7073–7082 [View Article][PubMed]
    [Google Scholar]
  57. Penttilä M., Lehtovaara P., Nevalainen H., Bhikhabhai R., Knowles J. ( 1986). Homology between cellulase genes of Trichoderma reesei: complete nucleotide sequence of the endoglucanase I gene. Gene 45:253–263 [View Article][PubMed]
    [Google Scholar]
  58. Penttilä M., Limón C., Nevalainen H. ( 2004). Molecular biology of Trichoderma and biotechnological applications. Handbook of Fungal Biotechnology413–427 Arora D. K. New York, Basel: Marcel Dekker; [View Article]
    [Google Scholar]
  59. Read N. D. ( 2011). Exocytosis and growth do not occur only at hyphal tips. Mol Microbiol 81:4–7 [View Article][PubMed]
    [Google Scholar]
  60. Rouvinen J., Bergfors T., Teeri T., Knowles J. K., Jones T. A. ( 1990). Three-dimensional structure of cellobiohydrolase II from Trichoderma reesei . Science 249:380–386 [View Article][PubMed]
    [Google Scholar]
  61. Sallese M., Giannotta M., Luini A. ( 2009). Coordination of the secretory compartments via inter-organelle signalling. Semin Cell Dev Biol 20:801–809 [View Article][PubMed]
    [Google Scholar]
  62. Saloheimo M., Lund M., Penttilä M. E. ( 1999). The protein disulphide isomerase gene of the fungus Trichoderma reesei is induced by endoplasmic reticulum stress and regulated by the carbon source. Mol Gen Genet 262:35–45 [View Article][PubMed]
    [Google Scholar]
  63. Saloheimo M., Valkonen M., Penttilä M. ( 2003). Activation mechanisms of the HAC1-mediated unfolded protein response in filamentous fungi. Mol Microbiol 47:1149–1161 [View Article][PubMed]
    [Google Scholar]
  64. Saloheimo M., Wang H., Valkonen M., Vasara T., Huuskonen A., Riikonen M., Pakula T., Ward M., Penttilä M. ( 2004). Characterization of secretory genes ypt1/yptA and nsf1/nsfA from two filamentous fungi: induction of secretory pathway genes of Trichoderma reesei under secretion stress conditions. Appl Environ Microbiol 70:459–467 [View Article][PubMed]
    [Google Scholar]
  65. Selinheimo E., Saloheimo M., Ahola E., Westerholm-Parvinen A., Kalkkinen N., Buchert J., Kruus K. ( 2006). Production and characterization of a secreted, C-terminally processed tyrosinase from the filamentous fungus Trichoderma reesei . FEBS J 273:4322–4335 [View Article][PubMed]
    [Google Scholar]
  66. Selinheimo E., Autio K., Kruus K., Buchert J. ( 2007). Elucidating the mechanism of laccase and tyrosinase in wheat bread making. J Agric Food Chem 55:6357–6365 [View Article][PubMed]
    [Google Scholar]
  67. Shoemaker S., Schweickart V., Ladner M., Gelfand D., Kwok S., Myambo K., Innis M. ( 1983). Molecular cloning of exo-cellobiohydrolase I derived from Trichoderma reesei strain L27. Nat Biotechnol 1:691–696 [View Article]
    [Google Scholar]
  68. Shoji J. Y., Arioka M., Kitamoto K. ( 2008). Dissecting cellular components of the secretory pathway in filamentous fungi: insights into their application for protein production. Biotechnol Lett 30:7–14 [View Article][PubMed]
    [Google Scholar]
  69. Sidrauski C., Cox J. S., Walter P. ( 1996). tRNA ligase is required for regulated mRNA splicing in the unfolded protein response. Cell 87:405–413 [View Article][PubMed]
    [Google Scholar]
  70. Søgaard M., Tani K., Ye R. R., Geromanos S., Tempst P., Kirchhausen T., Rothman J. E., Söllner T. ( 1994). A rab protein is required for the assembly of SNARE complexes in the docking of transport vesicles. Cell 78:937–948 [View Article][PubMed]
    [Google Scholar]
  71. Spang A. ( 2008). Membrane traffic in the secretory pathway: the life cycle of a transport vesicle. Cell Mol Life Sci 65:2781–2789 [View Article][PubMed]
    [Google Scholar]
  72. Stals I., Sandra K., Devreese B., Van Beeumen J., Claeyssens M. ( 2004). Factors influencing glycosylation of Trichoderma reesei cellulases. II: N-glycosylation of Cel7A core protein isolated from different strains. Glycobiology 14:725–737 [View Article][PubMed]
    [Google Scholar]
  73. Steiger M. G., Mach R. L., Mach-Aigner A. R. ( 2010). An accurate normalization strategy for RT-qPCR in Hypocrea jecorina (Trichoderma reesei). J Biotechnol 145:30–37 [View Article][PubMed]
    [Google Scholar]
  74. Teeri T. T., Lehtovaara P., Kauppinen S., Salovuori I., Knowles J. ( 1987). Homologous domains in Trichoderma reesei cellulolytic enzymes: gene sequence and expression of cellobiohydrolase II. Gene 51:43–52 [View Article][PubMed]
    [Google Scholar]
  75. Travers K. J., Patil C. K., Wodicka L., Lockhart D. J., Weissman J. S., Walter P. ( 2000). Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101:249–258 [View Article][PubMed]
    [Google Scholar]
  76. Valkonen M. ( 2003). Functional studies of the secretory pathway of filamentous fungi. The effect of unfolded protein response on protein production Espoo, Finland: VTT Publications 505;
    [Google Scholar]
  77. Valkonen M., Penttilä M., Saloheimo M. ( 2003a). Effects of inactivation and constitutive expression of the unfolded-protein response pathway on protein production in the yeast Saccharomyces cerevisiae . Appl Environ Microbiol 69:2065–2072 [View Article][PubMed]
    [Google Scholar]
  78. Valkonen M., Ward M., Wang H., Penttilä M., Saloheimo M. ( 2003b). Improvement of foreign-protein production in Aspergillus niger var. awamori by constitutive induction of the unfolded-protein response. Appl Environ Microbiol 69:6979–6986 [View Article][PubMed]
    [Google Scholar]
  79. Valkonen M., Penttilä M., Saloheimo M. ( 2004). The ire1 and ptc2 genes involved in the unfolded protein response pathway in the filamentous fungus Trichoderma reesei . Mol Genet Genomics 272:443–451 [View Article][PubMed]
    [Google Scholar]
  80. Valkonen M., Kalkman E. R., Saloheimo M., Penttilä M., Read N. D., Duncan R. R. ( 2007). Spatially segregated SNARE protein interactions in living fungal cells. J Biol Chem 282:22775–22785 [View Article][PubMed]
    [Google Scholar]
  81. Vasara T., Saloheimo M., Keränen S., Penttilä M. ( 2001a). Trichoderma reesei rho3 a homologue of yeast RH03 suppresses the growth defect of yeast sec15-1 mutation. Curr Genet 40:119–127 [View Article][PubMed]
    [Google Scholar]
  82. Vasara T., Salusjärvi L., Raudaskoski M., Keränen S., Penttilä M., Saloheimo M. ( 2001b). Interactions of the Trichoderma reesei rho3 with the secretory pathway in yeast and T. reesei . Mol Microbiol 42:1349–1361 [View Article][PubMed]
    [Google Scholar]
  83. Vasara T., Keränen S., Penttilä M., Saloheimo M. ( 2002). Characterisation of two 14-3-3 genes from Trichoderma reesei: interactions with yeast secretory pathway components. Biochim Biophys Acta 1590:27–40 [View Article][PubMed]
    [Google Scholar]
  84. Veldhuisen G., Saloheimo M., Fiers M. A., Punt P. J., Contreras R., Penttilä M., van den Hondel C. A. M. J. J. ( 1997). Isolation and analysis of functional homologues of the secretion-related SAR1 gene of Saccharomyces cerevisiae from Aspergillus niger and Trichoderma reesei . Mol Gen Genet 256:446–455 [View Article][PubMed]
    [Google Scholar]
  85. Vinzant T. B., Adney W. S., Decker S. R., Baker J. O., Kinter M. T., Sherman N. E., Fox J. W., Himmel M. E. ( 2001). Fingerprinting Trichoderma reesei hydrolases in a commercial cellulase preparation. Appl Biochem Biotechnol 91-93:99–108 [View Article][PubMed]
    [Google Scholar]
  86. Wilson D. W., Wilcox C. A., Flynn G. C., Chen E., Kuang W. J., Henzel W. J., Block M. R., Ullrich A., Rothman J. E. ( 1989). A fusion protein required for vesicle-mediated transport in both mammalian cells and yeast. Nature 339:355–359 [View Article][PubMed]
    [Google Scholar]
  87. Yoshida H., Matsui T., Yamamoto A., Okada T., Mori K. ( 2001). XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107:881–891 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.053132-0
Loading
/content/journal/micro/10.1099/mic.0.053132-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed