Dissecting cellular components of the secretory pathway in filamentous fungi: Insights into their application for protein production

Biotechnology Letters

Volumn 30, Issue 1, 2008, Pages 7-14

  Shoji, Jun Ya ^a   Arioka, Manabu ^a   Kitamoto, Katsuhiko ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Aspergillus; Protein production; SNARE; Vesicular trafficking

Indexed keywords

BIODIVERSITY; CELLS; GENE EXPRESSION; MOLECULAR BIOLOGY; PROTEINS;

ASPERGILLUS; FILAMENTOUS FUNGI; GENETIC MODIFICATIONS; PROTEIN PRODUCTION; VESICULAR TRAFFICKING;

FUNGI;

FUNGAL PROTEIN;

BIOLOGICAL MODEL; CELL FRACTIONATION; FUNGUS; GENE EXPRESSION PROFILING; METABOLISM; METHODOLOGY; PHYSIOLOGY; REVIEW; SECRETION; SIGNAL TRANSDUCTION; ULTRASTRUCTURE;

FUNGAL PROTEINS; FUNGI; GENE EXPRESSION PROFILING; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS;

ASPERGILLUS; FUNGI;

EID: 36649015551     PISSN: 01415492     EISSN: 15736776     Source Type: Journal    
DOI: 10.1007/s10529-007-9516-1     Document Type: Review

References (53)

1. Aalto MK, 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 12:4095-1104
2. Ashford AE (1998) Dynamic pleiomorphic vacuole systems: are they endosomes and transport compartments in fungal hyphae? Adv Bot Res 28:119-159
3. Becherer KA, Rieder SE, Emr SD, Jones EW (1996) Novel syntaxin homologue, Pep12p, required for the sorting of lumenal hydrolases to the lysosome-like vacuole in yeast. Mol Biol Cell 7:579-594
4. Cole L, Davies D, Hyde GJ, Ashford AE (2000) Brefeldin A affects growth, endoplasmic reticulum, Golgi bodies, tubular vacuole system, and secretory pathway in Pisolithus tinctorius. Fungal Genet Biol 29:95-106
5. Conesa A, Punt PJ, van Luijk N, van den Hondel CA (2001) The secretion pathway in filamentous fungi: a biotechnological view. Fungal Genet Biol 33:155-171
6. Coughlan CM, Walker JL, Cochran JC, Wittrup KD, Brodsky JL (2004) Degradation of mutated bovine pancreatic trypsin inhibitor in the yeast vacuole suggests post-endoplasmic reticulum protein quality control. J Biol Chem 279:15289-15297
7. Damveld R, ten Haaft P, Hartog M, Minneboo I, Dekker P, Wenzel T, Sagt C (2007) Engineering of a novel protein secretion pathway in Aspergillus niger. Paper presented at 3rd Conference on Physiology of Yeasts and Filamentous Fungi, Marina Congress Centre, Helsinki, Finland, 13-16 June 2007
8. David D, Sundarababu S, Gerst JE (1998) Involvement of long chain fatty acid elongation in the trafficking of secretory vesicles in yeast. J Cell Biol 143:1167-1182
9. Geißenhöner A, Sievers N, Brock M, Fischer R (2001) Aspergillus nidulans DigA, a potential homolog of Saccharomyces cerevisiae Pep3 (Vps18), is required for nuclear migration, mitochondrial morphology and polarized growth. Mol Genet Genomics 266:672-685
10. Gordon CL, Khalaj V, Ram AF, Archer DB, Brookman JL, Trinci AP, Jeenes DJ, Doonan JH, Wells B, Punt PJ, van den Hondel CA, Robson GD (2000) Glucoamylase::green fluorescent protein fusions to monitor protein secretion in Aspergillus niger. Microbiology 146:415-426
11. Gouka RJ, Punt PJ, van den Hondel CA (1997) Efficient production of secreted proteins by Aspergillus: progress, limitations and prospects. Appl Microbiol Biotechnol 47:1-11
12. Gupta GD, Heath IB (2002) Predicting the distribution, conservation, and functions of SNAREs and related proteins in fungi. Fungal Genet Biol 36:1-21
13. Gupta GD, Free SJ, Levina NN, Keränen S, Heath IB (2003) Two divergent plasma membrane syntaxin-like SNAREs, nsyn1 and nsyn2, contribute to hyphal tip growth and other developmental processes in Neurospora crassa. Fungal Genet Biol 40:271-286
14. Hampton RY (2002) ER-associated degradation in protein quality control and cellular regulation. Curr Opin Cell Biol 14:476-482
15. Harris SD (2001) Septum formation in Aspergillus nidulans. Curr Opin Microbiol 4:736-739
16. Harsay E, Bretscher A (1995) Parallel secretory pathways to the cell surface in yeast. J Cell Biol 131:297-310
17. Higuchi Y, Nakahama T, Shoji JY, Arioka M, Kitamoto K (2006) Visualization of the endocytic pathway in the filamentous fungus Aspergillus oryzae using an EGFP-fused plasma membrane protein. Biochem Biophys Res Commun 340:784-791
18. Holkeri H, Makarow M (1998) Different degradation pathways for heterologous glycoproteins in yeast. FEBS Lett 429:162-166
19. Hong E, Davidson AR, Kaiser CA (1996) A pathway for targeting soluble misfolded proteins to the yeast vacuole. J Cell Biol 135:623-633
20. Klionsky DJ, Herman PK, Emr SD (1990) The fungal vacuole: composition, function, and biogenesis. Microbiol Rev 54:266-292
21. Kruse KB, Brodsky JL, McCracken AA (2006) Characterization of an ERAD gene as VPS30/ATG6 reveals two alternative and functionally distinct protein quality control pathways: one for soluble Z variant of human alpha-1 proteinase inhibitor (A1PiZ) and another for aggregates of A1PiZ. Mol Biol Cell 17:203-212
22. Kuratsu M, Taura A, Shoji JY, Kikuchi S, Arioka M, Kitamoto K (2007) Systematic analysis of SNARE localization in the filamentous fungus Aspergillus oryzae. Fungal Genet Biol, doi:10.1016/j.fgb.2007.04.012
23. Lewis MJ, Nichols BJ, Prescianotto-Baschong C, Riezman H, Pelham HR (2000) Specific retrieval of the exocytic SNARE Snc1p from early yeast endosomes. Mol Biol Cell 11:23-38
24. Lombraña M, Moralejo FJ, Pinto R, Martín JF (2004) Modulation of Aspergillus awamori thaumatin secretion by modification of bipA gene expression. Appl Environ Microbiol 70:5145-5152
25. Machida M, Asai K, Sano M, Tanaka T, Kumagai T, Terai G, Kusumoto K, Arima T, Akita O, Kashiwagi Y, Abe K, Gomi K, Horiuchi H, Kitamoto K, Kobayashi T, Takeuchi M, Denning DW, Galagan JE, Nierman WC, Yu J, Archer DB, Bennett JW, Bhatnagar D, Cleveland TE, Fedorova ND, Gotoh O, Horikawa H, Hosoyama A, Ichinomiya M, Igarashi R, Iwashita K, Juvvadi PR, Kato M, Kato Y, Kin T, Kokubun A, Maeda H, Maeyama N, Maruyama J, Nagasaki H, Nakajima T, Oda K, Okada K, Paulsen I, Sakamoto K, Sawano T, Takahashi M, Takase K, Terabayashi Y, Wortman JR, Yamada O, Yamagata Y, Anazawa H, Hata Y, Koide Y, Komori T, Koyama Y, Minetoki T, Suharnan S, Tanaka A, Isono K, Kuhara S, Ogasawara N, Kikuchi H (2005) Genome sequencing and analysis of Aspergillus oryzae. Nature 438:1157-1161
26. Maruyama JI, Kikuchi S, Kitamoto K (2006) Differential distribution of the endoplasmic reticulum network as visualized by the BipA-EGFP fusion protein in hyphal compartments across the septum of the filamentous fungus, Aspergillus oryzae. Fungal Genet Biol 43:642-654
27. Masai K, Maruyama J, Nakajima H, Kitamoto K (2003) In vivo visualization of the distribution of a secretory protein in Aspergillus oryzae hyphae using the RntA-EGFP fusion protein. Biosci Biotechnol Biochem 67:455-459
28. Masai K, Maruyama JI, Sakamoto K, Nakajima H, Akita O, Kitamoto K (2006) Square-plate culture method allows detection of differential gene expression and screening of novel, region-specific genes in Aspergillus oryzae. Appl Microbiol Biotechnol 71:881-891
29. Moralejo FJ, Watson AJ, Jeenes DJ, Archer DB, Martín JF (2001) A defined level of protein disulfide isomerase expression is required for optimal secretion of thaumatin by Aspegillus awamori. Mol Genet Genomics 266:246-253
30. Ohneda M, Arioka M, Nakajima H, Kitamoto K (2002) Visualization of vacuoles in Aspergillus oryzae by expression of CPY-EGFP. Fungal Genet Biol 37:29-38
31. Ohneda M, Arioka M, Kitamoto K (2005) Isolation and characterization of Aspergillus oryzae vacuolar protein sorting mutants. Appl Environ Microbiol 71:4856-4861
32. Palmer GE, Cashmore A, Sturtevant J (2003) Candida albicans VPS11 is required for vacuole biogenesis and germ tube formation. Eukaryot Cell 2:411-421
33. 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, van den Berg 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, van den Hombergh JP, van den Hondel CA, van der Heijden RT, van der Kaaij RM, Klis FM, Kools HJ, Kubicek CP, van Kuyk PA, Lauber J, Lu X, van der Maarel 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, van de Vondervoort PJ, Wedler H, Wösten HA, Zeng AP, van Ooyen AJ, Visser J, Stam H (2007) Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol 25:221-231
34. Peñalva MA (2005) Tracing the endocytic pathway of Aspergillus nidulans with FM4-64. Fungal Genet Biol 42:963-975
35. Punt PJ, Seiboth B, Weenink XO, van Zeijl C, Lenders M, Konetschny C, Ram AF, Montijn R, Kubicek CP, van den Hondel CA (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. Mol Microbiol 41:513-525
36. Punt PJ, van Biezen N, Conesa A, Albers A, Mangnus J, van den Hondel CA (2002) Filamentous fungi as cell factories for heterologous protein production. Trends Biotechnol 20:200-206
37. Raymond CK, Howald-Stevenson I, Vater CA, Stevens TH (1992) Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol Biol Cell 3:1389-1402
38. Roberg KJ, Rowley N, Kaiser CA (1997) Physiological regulation of membrane protein sorting late in the secretory pathway of Saccharomyces cerevisiae. J Cell Biol 137:1469-1482
39. Rothman JE, Warren G (1994) Implications of the SNARE hypothesis for intracellular membrane topology and dynamics. Curr Biol 4:220-233
40. Saloheimo M, Lund M, Penttilä ME (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
41. Shoji JY, Arioka M, Kitamoto K (2006) Vacuolar membrane dynamics in the filamentous fungus Aspergillus oryzae. Eukaryot Cell 5:411-421
42. Steinberg G (2007) On the move: endosomes in fungal growth and pathogenicity. Nat Rev Microbiol 5:309-316
43. Tatsumi A, Kikuma T, Arioka M, Kitamoto K (2006) Aovps24, a homologue of VPS24, is required for vacuolar formation which could maintain proper growth and development in the filamentous fungus Aspergillus oryzae. Biochem Biophys Res Commun 347:970-978
44. te Biesebeke R, Record E, van Biezen N, Heerikhuisen M, Franken A, Punt PJ, van den Hondel CA (2005) Branching mutants of Aspergillus oryzae with improved amylase and protease production on solid substrates. Appl Microbiol Biotechnol 69:44-50
45. Ungermann C, Wickner W (1998) Vam7p, a vacuolar SNAP-25 homolog, is required for SNARE complex integrity and vacuole docking and fusion. EMBO J 17:3269-3276
46. Valkonen M, Kalkman ER, Saloheimo M, Penttila M, Read ND, Duncan RR (2007) Spatially segregated snare protein interactions in living fungal cells. J Biol Chem (in press)
47. 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. Appl Environ Microbiol 69:6979-6986
48. van den Hombergh JPTW, van de Vondervoort PJ, Fraissinet-Tachet L, Visser J (1997) Aspergillus as a host for heterologous protein production: the problem of proteases. Trends Biotechnol 15:256-263
49. Veses V, Casanova M, Murgui A, Domínguez A, Gow NA, Martínez JP (2005) ABG1, a novel and essential Candida albicans gene encoding a vacuolar protein involved in cytokinesis and hyphal branching. Eukaryot Cell 4:1088-1101
50. Wada Y, Nakamura N, Ohsumi Y, Hirata A (1997) Vam3p, a new member of syntaxin related protein, is required for vacuolar assembly in the yeast Saccharomyces cerevisiae. J Cell Sci 110:1299-1306
51. Walworth NC, Brennwald P, Kabcenell AK, Garrett M, Novick P (1992) Hydrolysis of GTP by Sec4 protein plays an important role in vesicular transport and is stimulated by a GTPase-activating protein in Saccharomyces cerevisiae. Mol Cell Biol 12:2017-2028
52. Wedlich-Söldner R, Bölker M, Kahmann R, Steinberg G (2000) A putative endosomal t-SNARE links exo- and endocytosis in the phytopathogenic fungus Ustilago maydis. EMBO J 19:1974-1986
53. Wösten HA, Moukha SM, Sietsma JH, Wessels JG (1991) Localization of growth and secretion of proteins in Aspergillus niger. J Gen Microbiol 137:2017-2023