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  • Print publication year: 2007
  • Online publication date: October 2013

9 - Protein secretion and associated stresses in Aspergillus: a genomic perspective

from III - Protein folding and secretion

Summary

Introduction

Aspergillus spp. are filamentous fungi of which several have been studied in relation to the secretion of proteins. This chapter will only discuss those species for which there is currently genome sequence information even though the secretion of proteins is probably an important aspect of the lifestyles of the more than 180 known species of Aspergillus. Therefore, the emphasis is with a common saprophyte and human pathogen (Aspergillus fumigatus), a sexual species and one that has been developed as a convenient laboratory species for basic studies (Aspergillus nidulans), and two species that are widely exploited commercially for their secreted enzymes (Aspergillus niger and Aspergillus oryzae). The genome sequence data have been recently acquired and made available to the scientific community so it is particularly timely that the annotated sequences serve as a framework for this chapter on protein secretion. That will also avoid a substantial amount of repetition because there are several excellent reviews on protein secretion by Aspergillus that are primarily pre-genomic in their outlook (Conesa et al., 2001; Punt et al., 2002; MacKenzie et al., 2004) even though extensive use of gene sequences and expression data has been made in the reviewed literature. More recent reviews have been able to take a more genomic view from the outset (Archer & Dyer, 2004; Archer & Turner, 2005) but, even then, the full annotated genome sequences were not available.

References
Al-Sheikh, H. M., Watson, A. J., Lacey, G. A., Punt, P., 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. Molecular Microbiology, 53, 1731–42.
Archer, D. B. (2000). Filamentous fungi as microbial cell factories for food use. Current Opinion in Biotechnology, 11, 478–83.
Archer, D. B. & Dyer, P. S. (2004). From genomics to post-genomics in Aspergillus niger. Current Opinion in Microbiology, 7, 499–504.
Archer, D. B. & Turner, G. (2005). Genomics of protein secretion and hyphal growth in Aspergillus. In The Mycota XIII, Fungal Genomics, ed. Brown, A. J.. Berlin: Springer-Verlag.
Beffa, T., Staib, F., Fischer, J. L., Lyon, P. F., Gumowski, P., Marfenina, O. E., Dunoyer-Geindre, S., Georgen, F., Roch-Susuki, R., Gallaz, L. & Latge, J.-P. (1998). Mycological control and surveillance of biological waste and compost. Medical Mycology, 36 (suppl. I), 137–45.
Biesebeke, R. T., Levin, A., Sagt, C., Bartels, J., Goosen, T., Ram, A., Hondel, C. A. M. J. J. & Punt, P. (2005). Identification of growth phenotype-related genes in Aspergillus oryzae by heterologous macroarray and suppression subtractive hybridization. Molecular Genetics and Genomics, 272, 33–42.
Conesa, A., Punt, P. J., Luijk, N. & Hondel, C. A. M. J. J. (2001). The secretion pathway in filamentous fungi: a biotechnological view. Fungal Genetics and Biology, 33, 155–71.
Vries, R. P., Jansen, J., Aguilar, G., Parenicova, L., Joosten, V., Wulfert, F., Benen, J. A. E. & Visser, J. (2002). Expression profiling of pectinolytic genes from Aspergillus niger. FEBS Letters, 530, 41–7.
Vries, R. P., Burgers, K., Vondervoort, P. J. I., Frisvad, J. C., Samson, R. A. & Visser, J. (2004). A new black Aspergillus species, A. vadensis, is a promising host for homologous and heterologous protein production. Applied and Environmental Microbiology, 70, 3954–9.
Vries, R. P., Grieken, C., Kuyk, P. A. & Wosten, H. A. B. (2005a). The value of genome sequences in the rapid identification of novel genes encoding specific plant cell wall degrading enzymes. Current Genomics, 6, 157–87.
Vries, R. P., Frisvad, J. C., Vondervoort, P. J. I., Burgers, K., Kuijpers, A. F., Samson, R. A. & Visser, J. (2005b). Aspergillus vadensis, a new species of the group of black Aspergilli. Antonie van Leeuwenhoek International Journal of General and Molecular Microbiology, 87, 195–203.
Diener, S. E., Dunn-Coleman, N., Foreman, P., Houfek, T. D., Teunissen, P. J., Solingen, P., Dankmeyer, L., Mitchell, T. K., Ward, M. & Dean, R. A. (2004). Characterization of the protein processing and secretion pathways in a comprehensive set of expressed sequence tags from Trichoderma reseei. FEMS Microbiology Letters, 230, 275–82.
Ellgaard, L. & Helenius, A. (2003). Quality control in the endoplasmic reticulum. Nature Reviews in Molecular Cell Biology, 4, 181–91.
Galagan, J. E., Calvo, S. E., Cuomo, C.et al. (2005). Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature, 438, 1105–15.
Heerikhuisen, M., van den Hondel, C. & Punt, P. (2004). Aspergillus sojae. In Production of Recombinant Proteins: Novel Microbial and Eukaryotic Expression Systems, ed. Gellissen, G.. The Netherlands: Wiley, pp. 191–214.
Kaufman, R. J. (2004). Regulation of mRNA translation by protein folding in the endoplasmic reticulum. Trends in Biochemical Sciences, 29, 152–8.
Kaufman, R. J., Scheuner, D., Schröder, M., Shen, X., Lee, K., Liu, C. Y. & Arnold, S. M. (2002). The unfolded protein response in nutrient sensing and differentiation. Nature Reviews in Molecular Cell Biology, 3, 411–21.
Kitamoto, K. (2002). Molecular biology of the Koji moulds. Advances in Applied Microbiology, 51, 129–53.
Latge, J.-P., (1999). Aspergillus fumigatus and aspergillosis. Clinical Microbiology Reviews, 12, 310–50.
Lombraña, M., Moralejo, F. J., Pinto, R. & Martin, J. F. (2004). Modulation of thaumatin secretion by Aspergillus awamori by modification of bipA gene expression. Applied and Environmental Microbiology, 70, 5145–52.
Machida, M. (2002). Progress of Aspergillus oryzae genomics. Advances in Applied Microbiology, 51, 81–106.
Machida, M., Asai, K., Sano, M., et al. (2005). Genome sequencing and analysis of Aspergillus oryzae. Nature, 438, 1157–61.
MacKenzie, D. A., Jeenes, D. J. & Archer, D. B. (2004). Filamentous fungi as expression systems for heterologous proteins. In The Mycota II, Ch.15, ed. Kück, U.. Springer, pp. 289–315.
Martinez, I. M. & Chrispeels, M. J. (2003). Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell, 15, 561–76.
Montiel, D., Dickinson, M. J., Lee, H. A., Dyer, P. S., Jeenes, D. J., Roberts, I. N., James, S., Fuller, S. J., Matsushima, K. & Archer, D. B. (2003). Genetic differentiation of the Aspergillus Section Flavi complex using AFLP fingerprints. Mycological Research 107, 1427–34.
Moralejo, F. J., Watson, A. J., Jeenes, D. J., Archer, D. B. & Martín, J. F. (2001). A defined level of protein disulfide isomerase expression is required for optimal secretion of thaumatin by Aspergillus awamori. Molecular Genetics and Genomics, 266, 246–53.
Mulder, H. J., Saloheimo, M., Penttilä, M. & Madrid, S. (2004). The transcription factor HACA mediates the unfolded protein response in Aspergillus niger, and up-regulates its own transcription. Molecular Genetics and Genomics, 271, 130–40.
Ngiam, C., Jeenes, D. J., Punt, P. J., Hondel, C. A. & Archer, D. B. (2000). Characterization of a foldase, protein disulfide isomerase A, in the protein secretory pathway of Aspergillus niger. Applied and Environmental Microbiology, 66, 775–82.
Nierman, W., Pain, A., Anderson, M. J., et al. (2005). Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature, 438, 1151–6.
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. Journal of Biological Chemistry, 278, 45011–20.
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, 135–43.
Patil, C. & Walter, P. (2001). Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Current Opinion in Cell Biology, 13, 349–56.
Patil, C., Li, H. & Walter, P. (2004). Gcn4p and novel upstream activating sequences regulate targets of the unfolded protein response. Plos Biology, 2, 1208–23.
Pritchard, B. L., Yu, J., Nierman, W., Dean, R. A., Bhatnagar, D., Cleveland, T. E. & Payne, G. A. (2005). Aspergillus flavus genome sequence: status and release of sequence data. Proceedings of Plant and Animal Genomes XIII Conference, San Diego, USA, P037.
Punt, P. J., Seiboth, B., Weenink, X. O., Zeijl, C., Lenders, M., Konetschny, C., Ram, A. F. J., Montijn, R., Kubicek, C. P. & Hondel, C. A. M. J. J. (2001). Identification and characterization of a family of secretion-related small GTPase-encoding genes from the filamentous fungus Aspergillus niger: a putative SEC4 homologue is not essential for growth. Molecular Microbiology, 41, 513–25.
Punt, P. J., Biezen, N., Conesa, A., Albers, A., Mangnus, J. & Hondel, C. A. M. J. J. (2002). Filamentous fungi as cell factories for heterologous protein production. Trends in Biotechnology, 20, 200–6.
Robson, G. E., Huang., J., Wortman, J. & Archer, D. B. (2005). A preliminary analysis of the process of protein secretion, and the diversity of putative secreted hydrolases encoded in Aspergillus fumigatus: insights from the genome. Medical Mycology Supplement 1, 43, S41–S47.
Rüegsegger, U., Leber, J. H. & Walter, P. (2001). Block of HAC1 mRNA translation by long-range base pairing is released by cytoplasmic splicing upon induction of the unfolded protein response. Cell, 107, 103–14.
Rutkowski, D. T. & Kaufman, R. J. (2004). A trip to the ER: coping with stress. Trends in Cell Biology, 14, 20–8.
Sakaguchi, K., Takagi, M., Horiuchi, H. & Gomi, K. (1992). Fungal enzymes used in oriental food and beverage industries. In Applied Molecular Genetics of Filamentous Fungi, eds. Kinghorn, J. R. & Turner, G.. London: Blackie, pp. 54–99.
Saloheimo, M., Valkonen, M. & Penttilä, M. (2003). Activation mechanisms of the HACI-mediated unfolded protein response in filamentous fungi. Molecular Microbiology, 47, 1149–61.
Schröder, M., Clark, R. & Kaufman, R. J. (2003). IRE1- and HAC1-independent transcriptional regulation in the unfolded protein response of yeast. Molecular Microbiology, 49, 591–606.
Schröder, M. & Kaufman, R. J. (2005). ER stress and the unfolded protein response. Mutation Research, 569, 29–63.
Sims, A. H., Gent, M. E., Robson, G. D., Dunn-Coleman, N. S. & Oliver, S. G. (2004). Combining transcriptome data with genomic and cDNA sequence alignments to make confident functional assignments for Aspergillus nidulans genes. Mycological Research, 108, 853–7.
Sims, A. H., Gent, M. E., Lanthaler, K., Dunn-Coleman, N. S., Oliver, S. G. & Robson, G. D. (2005). Transcriptome analysis of recombinant protein secretion by Aspergillus nidulans and the unfolded protein response in vivo. Applied and Environmental Microbiology, 71, 2737–47.
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, 249–58.
Valkonen, M., Ward, M., Wang, H., Penttilä, M. & Saloheimo, M. (2003). Improvement of foreign protein production in Aspergillus niger var. awamori by constitutive induction of the unfolded protein response. Applied and Environmental Microbiology, 69, 6979–86.
Wymelenberg, A., Sabat, G., Martinez, D., Rajangam, A. S., Teeri, T. T., Gaskell, J., Kersten, P. J. & Cullen, D. (2005). The Phanerochaete chrysosporium secretome: database predictions and initial mass spectrometry peptide identifications in cellulose-grown medium. Journal of Biotechnology, 118, 17–34.
Vashist, S. & Ng, D. T. W. (2004). Misfolded proteins are sorted by a sequential checkpoint mechanism of ER quality control. Journal of Cell Biology, 165, 41–52.
Wiebe, M. G., Karandikar, A., Robson, G. D., Trinci, A. P. J., Candia, J. L. F., Trappe, S., Wallis, G., Rinas, U., Derkx, P. M. F., Madrid, S., Sisniega, H., Faus, I., Montijn, R., Hondel, C. A. M. J. J. & Punt, P. J. (2001). Production of tissue plasminogen activator (t-PA) in Aspergillus niger. Biotechnology and Bioengineering, 76, 164–74.
Zhang, K. & Kaufman, R. J. (2004). Signaling the unfolded protein response from the endoplasmic reticulum. Journal of Biological Chemistry, 279, 25935–8.