Alterations in protein secretion caused by metabolic engineering of glycosylation pathways in fungi

Acta Biochimica Polonica

Volumn 55, Issue 3, 2008, Pages 447-456

  Kruszewska, Joanna S ^a   Perlińska Lenart, Urszula ^a   Górka Nieć, Wioletta ^a   Orłowski, Jacek ^a   Zembek, Patrycja ^a   Palamarczyk, Grazyna ^a  

^a INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

Author keywords

Glycosylation; Protein secretion; Trichoderma

Indexed keywords

FUNGI; HYPOCREA JECORINA; TRICHODERMA;

EID: 56049116987     PISSN: 0001527X     EISSN: 1734154X     Source Type: Journal    
DOI: 10.18388/abp.2008_3050     Document Type: Review

References (82)

1. Adair WLJ, Cafmeyer N (1987) Characterization of the Saccharomyces cerevisiae cis-prenyltransferase required for dolichyl phosphate biosynthesis. Arch Biochem Biophys 259: 589-596.
2. Agaphonov MO, Packeiser AN, Chechenova MB, Choi E, Ter-Avanesyan MD (2001) Mutation of the homologue of GDP-mannose pyrophosphorylase alters cell wall structure, protein glycosylation and secretion in Hansenula polymorpha. Yeast 18: 391-402.
3. Agaphonov MO, Sokolov S, Romanova NV, Sohn J, Kim SY, Kalebina TS, Choi ES, Ter-Avanesyan MD (2005) Mutation of the protein-O-mannosyltransferase enhances secretion of the human urokinase-type plasminogen activator in Hansenula polymorpha. Yeast 22: 1037-1047.
4. Al-Sheikh H, Watson AJ, Lacey GA, Punt PJ, MacKenzie DA, Jeenes DJ, Pakula T, Penttila M, Alcocer MJ, Archer DB (2004) Endoplasmic reticulum stress leads to the selective transcriptional downregulation of the glucoamylase gene in Aspergillus niger. Mol Microbiol 53: 1731-1742.
5. Ashida H, Maeda Y, Kinoshita T (2006) DPM1, the catalytic subunit of dolichol-phosphate mannose synthase, is tethered to and stabilized on the endoplasmic reticulum membrane by DPM3. J Biol Chem 281: 896-904.
6. Beauvais A, Maubon D, Park S, Morelle W, Tanguy M, Huerre M, Perlin DS, Latge JP (2005) Two alpha(1-3) glucan synthases with different functions in Aspergillus fumigatus. Appl Environ Microbiol 71: 1531-1538.
7. Belgareh-Touze N, Corral-Debrinski M, Launhardt H, Galan JM, Munder T, Le Panse S, Haguenauer-Tsapis R (2003) Yeast functional analysis: identification of two essential genes involved in ER to Golgi trafficking Traffic 4: 607-617.
8. Chavan M, Suzuki T, Rekowicz M, Lennarz W (2003) Genetic, biochemical, and morphological evidence for the involvement of N-glycosylation in biosynthesis of the cell wall β1,6-glucan of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 100: 15381-15386.
9. Choi BK, Davidson RC, Hamilton SR, Kung DH, Li H, Miele RG, Nett JH, Wildt S, Gerngross TU (2003) Use of combinatorial genetic libraries to humanize N-linked glycosylation in the yeast Pichia pastoris. Proc Natl Acad Sci USA 100: 5022-5027.
10. Colussi PA, Taron CH, Mack JC, Orlean P (1997) Human and Saccharomyces cerevisiae dolichol phosphate mannose synthases represent two classes of the enzyme, but both function in Schizosaccharomyces pombe. Proc Natl Acad Sci USA 94: 7873-7878.
11. Conesa A, Punt PJ, van Luijk N, van den Hondel CAMJJ (2001) The secretion pathway in filamentous fungi: A biotechnological view. Fungal Gen Biol 33: 155-171.
12. Daleo GR, Hopp HE, Romero PA, Lezica R (1977) Biosynthesis of dolichol phosphate by subcellular fractions from liver. FEBS Lett 81: 411-414.
13. Davydenko SG, Juselius JK, Munder T, Bogengruber E, Jantti J, Keranen S (2004) Screening for novel essential genes of Saccharomyces cerevisiae involved in protein secretion. Yeast 21: 463-471.
14. De Bruyn A, Maras M, Schraml J, Herdewijn P, Contreras R (1997) NMR evidence for a novel asparagine-linked oligosaccharide on cellobiohydrolase I from Trichoderma reesei RUTC 30. FEBS Lett 405: 111-113.
15. Durand H, Clanet M, Tiraby G (1988) Genetic improvement of Trichoderma reesei for large scale cellulase production. Enzyme Microbiol Technol 10: 341-345.
16. Ecker M, Mrsa V, Hagen I, Deutzmann R, Strahl S, Tanner W (2003) O-mannosylation precedes and potentially controls the N-glycosylation of a yeast cell wall glycoprotein. EMBO reports 4: 628-632.
17. Ellgaard L, Helenius A (2003) Quality control in the endoplasmic reticulum. Mol Cell Biol 4: 181-191.
18. Fagerstam LG, Pettersson LG, Engström JA (1984) The primary structure of a β-1,4-glucan cellobiohydrolase from the fungus Trichoderma reesei QM9414. FEBS Lett 167: 309-315.
19. Gamauf C, Marchetti M, Kallio J, Puranen T, Vehmaanperä J, Allmaier G, Kubicek CP, Seiboth B (2007) Characterization of the bga1-encoded glucoside hydrolase family 35 β-galactosidase of Hypocrea jecorina with galacto-β-D-galactanase activity. FEBS J 274: 1691-1700.
20. Garcia R, Cremata JA, Quintero O, Montesino R, Benkestock K, Stahlberg J (2001) Characterization of protein glycoforms with N-linked neutral and phosphorylated oligosaccharides: studies on the glycosylation of endoglucanase 1 (Cel7B) from Trichoderma reesei. Biotechnol Appl Biochem 33: 141-152.
21. Gentzsch M, Tanner W (1996) The PMT gene family: protein O-glycosylation in Saccharomyces cerevisiae is vital. EMBO J 15: 5752-5759.
22. Gentzsch M, Tanner W (1997) Protein-O-glycosylation in yeast: protein-specific mannosyltransferases. Glycobiology 7: 481-486.
23. Girrbach V, Strahl S (2003) Members of the evolutionarily conserved PMT family of protein O-mannosyltransferases form distinct protein complexes among themselves. J Biol Chem 278: 12554-12562.
24. Goto M (2007) Protein O-glycosylation in fungi. Diverse structure and multiple functions. Biosci Biotechnol Biochem 71: 1415-1427.
25. Goto M, Tsukamoto M, Kwon I, Ekino K, Furukawa K (1999) Functional analysis of O-linked oligosaccharides in threonine/serine-rich region of Aspergillus glucoamylase by expression in mannosyltransferase disruptants of yeast. Eur J Biochem 260: 596-602.
26. Górka-Nieć W, Bańkowska R, Palamarczyk G, Kruszewska JS (2007) Protein glycosylation in pmt mutants of Saccharomyces cerevisiae. Influence of heterologously expressed cellobiohydrolase II of Trichoderma reesei and elevated levels of GDP-mannose and cis-prenyltransferase activity. Biochim Biophys Acta 1770: 774-780.
27. Górka-Nieć W, Pniewski M, Kania A, Perlińska-Lenart U, Palamarczyk G, Kruszewska JS (2008) Disruption of Trichoderma reesei gene encoding protein O-mannosyltransferase I results in a decrease of the enzyme activity and alteration of cell wall composition. Acta Biochim Polon 55: 251-259.
28. Guillemette T, van Peij NNME, Goosen T, Lanthaler K, Robson GD, van den Hondel CAMJJ, Stam H, Archer DB (2007) Genomic analysis of the secretion stress response in the enzyme-producing cell factory Aspergillus niger. BMC Genomics 8: 158.
29. Harrison MJ, Nouwens AS, Jardine DR, Zachara NE, Gooley AA, Nevalainen H, Packer NH (1998) Modified glycosylation of cellobiohydrolase I from a high cellulase-producing mutant strain of Trichoderma reesei. Eur J Biochem 256: 119-127.
30. Harrison MJ, Wathugala IM, Tenkanen M, Packer NH, Nevalainen KMH (2002) Glycosylation of acetylxylan esterase from Trichoderma reesei. Glycobiology 12: 291-298.
31. Harty C, Strahl S, Romisch K (2001) O-mannosylation protects mutant alpha-factor precursor from endoplasmic reticulum-associated degradation. Mol Biol Cell 12: 1093-1101.
32. Helenius A, Aebi M (2001) Intracellular functions of N-linked glycans. Science 291: 2364-2369.
33. Hollister J, Grabenhorst E, Nimtz M, Conradt H, Jarvis DL (2002) Engineering the protein N-glycosylation pathway in insect cells for production of biantennary, complex N-glycans. Biochemistry 41: 15093-15104.
34. Hu JP, Lanthier P, White TC, McHugh SG, Yaguchi M, Thibault P (2001) Characterization of cellobiohydrolase I (Cel7A) glycoforms from extracts of Trichoderma reesei using capillary isoelectric focusing and electrospray mass spectrometry. J Chromatogr B Biomed Sci Appl 752: 349-68.
35. Hui JP, White TC, Thibault P (2002) Identification of glycan structure and glycosylation sites in cellobiohydrolase II and endoglucanases I and II from Trichoderma reesei. Glycobiology 12: 837-849.
36. Jenkins N, Marphy L, Thyler R (2008) Post-translational modifications of recombinant proteins: Significance for biopharmaceuticals. Mol Biotechnol 39: 113-118.
37. Jeoh T, Michener W, Himmel ME, Decker SR, Adney WS (2008) Implications of cellobiohydrolase glycosylation for use in biomass conversion. Biotechnol Biofuels 1: 10.
38. Klarskov K, Piens K, Sto̊hlberg J, Hoi PB, van Beeumen J, Claeyssens M (1997) Cellobiohydrolase I from Trichoderma reesei: identification of an active-site nucleophile and additional information on sequence including glycosylation pattern of the core protein. Carbohyd Res 304: 143-153.
39. Klis MF, Boorsma A, De Groot PWJ (2006) Cell wall construction in Saccharomyces cerevisiae. Yeast 23: 185-202.
40. Ko K, Ahn MH, Song M, Choo YK, Kim HS, Ko K, Joung H (2008) Glyco-engineering of biotherapeutic proteins in plants. Moll Cells 25: 494-503.
41. Kollar R, Reinhold BB, Petrakova E, Yeh HJC, Ashwell G, Drgonova J, Kapteyn JC, Klis FM, Cabib E (1997) Architecture of the yeast cell wall. J Biol Chem 272: 17762-17775.
42. Kruszewska J, Messner R, Kubicek CP, Palamarczyk G (1989) O-glycosylation of proteins by membrane fraction of Trichoderma reesei QM9414. J Gen Microbiol 135: 301-307.
43. Kruszewska J, Palamarczyk G, Kubicek CP (1990) Stimulation of exoprotein secretion by choline and Tween 80 in Trichoderma reesei QM 9414 correlates with increased activity of dolichol phosphate mannose synthase. J Gen Microbiol 136: 1293-1298.
44. Kruszewska J, Butterweck AH, Kurza̧tkowski W, Migdalski A, Kubicek CP, Palamarczyk G (1999) Overexpression of the Saccharomyces cerevisiae mannosylphosphodolichol synthase - encoding gene in Trichoderma reesei results in an increased level of protein secretion and abnormal cell ultrastructure. Appl Environm Microbiol 65: 2382-2387.
45. Kruszewska JS, Saloheimo M, Migdalski A, Orlean P, Penttilä M, Palamarczyk G (2000) Dolichol phosphate mannose synthase from the filamentous fungus Trichoderma reesei belongs to the human and Schizosaccharomyces pombe class of the enzyme. Glycobiology 10: 983-991.
46. Kubicek CP, Panda T, Schreferl-Kunar G, Messner R, Gruber F (1987) O-linked - but not N-linked - glycosylation is necessary for secretion of endoglucanase I and II by Trichoderma reesei. Can J Microbiol 33: 698-703.
47. Lennarz WJ (2007) Studies on oligosaccharyl transferase in yeast. Acta Biochim Polon 54: 673-677.
48. Maeda Y, Tomita S, Watanabe R, Ohishi K, Kinoshita T (1998) DPM2 regulates biosynthesis of dolichol phosphate-mannose in mammalian cells: correct subcellular localization and stabilization of DPM1, and binding of dolichol phosphate. EMBO J 17: 4920-4929.
49. Maeda Y, Tanaka S, Hino J, Kangawa K, Kinoshita T (2000) Human dolichol-phosphate-mannose synthase consists of three subunits: DPM1, DPM2, and DPM3. EMBO J 19: 2475-2482.
50. Maras M, de Bruyn A, Schraml J, Hersewijn P, Claeyssens M, Fiers W, Contreras R (1997) Structural characterization of N-linked oligosaccharides from cellobiohydrolase I secreted by filamentous fungus Trichoderma reesei RUTC 30. Eur J Biochem 245: 617-625.
51. Muller Ch, McIntyre M, Hansen K, Nielsen J (2002) Metabolic engineering of the morphology of Aspergillus oryzae by altering chitin synthesis. Appl Environ Microbiol 68: 1827-1836.
52. Nakatsukasa K, Okada S, Umebayashi K, Fukuda R, Nishikawa S, Endo T (2004) Roles of O-mannosylation of aberrant proteins in reduction of the load for endoplasmic reticulum chaperones in yeast. J Biol Chem 279: 49762-49772.
53. Oka T, Hamaguchi T, Sameshima Y, Goto M, Furukawa K (2004) Molecular characterization of protein O-mannosylation and its involvement in cell-wall synthesis in Aspergillus nidulans. Microbiology 150: 1973-1982.
54. Oka T, Sameshima Y, Koga T, Kim H, Goto M, Furukawa K (2005) Protein O-mannosyltransferase A of Aspergillus awamori is involved in O-mannosylation of glucoamylase I. Microbiol 151: 3657-3667.
55. Pakula TM, Laxell M, Huuskonen A, Uusitalo J, Saloheimo M, Penttila M (2003) The effects of drugs inhibiting protein secretion in the filamentous fungus Trichoderma reesei. Evidence for downregulation of genes that encode secreted proteins in the stressed cells. J Biol Chem 278: 45011-45020.
56. Pakula TM, Uusitalo J, Saloheimo M, Salonen K, Aarts RJ, Penttila 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.
57. Palamarczyk G, Maras M, Contreras R, Kruszewska J (1998) Protein secretion and glycosylation in Trichoderma. In Trichoderma and Glocladium. Kubicek CP, Harman GE, eds, vol 1, pp 121-138. Taylor and Francis Ltd, London, UK.
58. Parodi AJ (2000) Protein glucosylation and its role in protein folding. Annu Rev Biochem 69: 69-93.
59. Penttila ME, Andre L, Lehtovaara P, Bailey M, Teeri TT, Knowles JKC (1988) Efficient secretion of two fungal cellobiohydrolases by Saccharomyces cerevisiae. Gene 63: 103-112.
60. Perlińska-Lenart U, Kurza̧tkowski W, Janas P, Kopińska A, Palamarczyk G, Kruszewska JS (2005) Protein production and secretion in an Aspergillus nidulans mutant impaired in glycosylation. Acta Biochim Polon 52: 195-205.
61. Perlińska-Lenart U, Bańkowska R, Palamarczyk G, Kruszewska JS (2006a) Overexpression of the Saccharomyces cerevisiae RER2 gene in Trichoderma reesei affects dolichol dependent enzymes and protein glycosylation. Fungal Genet Biol 43: 422-429.
62. Perlińska-Lenart U, Orłowski J, Laudy AE, Zdebska E, Palamarczyk G, Kruszewska JS (2006b) Glycoprotein hypersecretion alters the cell wall in Trichoderma reesei strains expressing the Saccharomyces cerevisiae dolichylphosphate mannose synthase gene. Appl Environ Microbiol 72: 7778-7784.
63. Proszynski TJ, Simons K, Bagnat M (2004) O-Glycosylation as a sorting determinant for cell surface delivery in yeast. Mol Biol Cell 15: 1533-1543.
64. Qin Y, Wei X, Liu X, Wang T, Qu Y (2008) Purification and characterization of recombinant endoglucanase of Trichoderma reesei expressed in Saccharomyces cerevisiae with higher glycosylation and stability. Protein Expr Purif 58: 162-167.
65. Sanders S, Gentzsch M, Tanner W, Herskowitz I (1999) Oglycosylation of Axl1/Bud10p by Pmt4p is required for its stability, localization and function in daughter cells. J Cell Biol 145: 1177-1188.
66. Sato M, Sato K, Nishikawa S, Hirata A, Kato J, Nakano A (1999) The yeast RER2 gene, identified by endoplasmic reticulum protein localization mutations, encodes cis-prenyltansferase, a key enzyme in dolichol synthesis. Mol Cell Biol 19: 471-483.
67. Sato M, Fujisaki S, Sato K, Nishimura Y, Nakano A (2001) Yeast Saccharomyces cerevisiae has two cis-prenyltransferases with different properties and localizations. Implication for their distinct physiological roles in dolichol synthesis. Genes Cells 6: 495-506.
68. Savel'ev AN, Eneyskaya EV, Isaeva-Ivanova LS, Shabalin KA, Golubev AM, Neustroev KN (1997) The carbohydrate moiety of α-galactosidase from Trichoderma reesei. Glycoconjugate J 14: 897-905
69. Schmidt M, Strenk ME, Boyer MP, Fritsch BJ (2005) Importance of cell wall mannoproteins for septum formation in Saccharomyces cerevisiae. Yeast 22: 715-723.
70. Seidl V, Huemer B, Seiboth B, Kubicek CP (2005) A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases. FEBS J 272: 5923-5939.
71. Shahinian S, Dijkgraaf GJ, Sdicu AM, Thomas DY, Jakob CA, Aebi M, Bussey H (1998) Involvement of protein N-glycosyl chain glucosylation and processing in the biosynthesis of cell wall β-1,6-glucan of Saccharomyces cerevisiae. Genetics 149: 843-856.
72. Shenk B, Rush JS, Waechter ChJ, Aeby M (2001) An alternative cis-isoprenyltransferase activity in yeast that produces polyisoprenols with chain lengths similar to mammalian dolichols. Glycobiology 11: 89-98.
73. Shoemaker S, Schweickart V, Ladner M, Gelfand D, Kwok K, Myambo K, Innis M (1983) Molecular cloning of exo-cellobiohydrolase I derived from Trichoderma reesei strain L27. Bio/Technology 1: 691-699.
74. Shridas P, Rush JS, Waechter ChJ (2003) Identification and characterization of a cDNA encoding a long-chain cis-isoprenyltransferase involved in dolichyl monophosphate biosynthesis in the ER of brain cells. Biochem Biophys Res Comm 312: 1349-1356.
75. Spiriti J, Bogani F, van der Vaart A, Ghirlanda G (2008) Modulation of protein stability by O-glycosylation in a designed Gc-MAF analog. Biophys Chem 134: 157-167.
76. 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: 725-735.
77. Szkopińska A, Karst F, Palamarczyk G (1996) Products of S. cerevisiae cis-prenyltransferase activity in vitro. Biochimie 78: 111-116.
78. Uccelletti D, Staneva D, Rufini S, Rufini S, Vencov P, Palleschi C (2005) Enhanced secretion of heterologous proteins in Kluyveromyces lactis by overexpression of the GDP-mannose pyrophosphorylase, KlPsa1p. FEMS Yeast Res 5: 735-746.
79. Wildt S, Gerngross TU (2005) The humanization of N-glycosylation pathways in yeast. Nature Rev Microbiol 3: 119-128.
80. Williamson G, Belshaw NJ, Williamson MP (1992) O-glycosylation in Aspergillus glucoamylase. Conformation and role in binding. Biochem J 282: 423-428.
81. Yan A, Lennarz WJ (2005) Unraveling the mechanism of protein N-glycosylation. J Biol Chem 280: 3121-3124.
82. Zakrzewska A, Palamarczyk G, Krotkiewski H, Zdebska E, Saloheimo M, Penttilä M, Kruszewska JS (2003) Overexpression of the gene encoding GTP-mannose-1-phosphate guanyltransferase, mpg1, increases cellular GDP-mannose levels and protein mannosylation in Trichoderma reesei. Appl Environ Microbiol 69: 4383-4389.