Overexpression of cell-wall GPI-anchored proteins restores cell growth of N-glycosylation-defective och1 mutants in Schizosaccharomyces pombe.
GPI-anchored protein
Genetic screening
Glyco-engineering
Glycoprotein
Schizosaccharomyces pombe
Journal
Applied microbiology and biotechnology
ISSN: 1432-0614
Titre abrégé: Appl Microbiol Biotechnol
Pays: Germany
ID NLM: 8406612
Informations de publication
Date de publication:
Dec 2021
Dec 2021
Historique:
received:
15
07
2021
accepted:
14
10
2021
revised:
08
10
2021
pubmed:
6
11
2021
medline:
17
11
2021
entrez:
5
11
2021
Statut:
ppublish
Résumé
The glycoproteins of yeast contain a large outer chain on N-linked oligosaccharides; therefore, yeast is not suitable for producing therapeutic glycoproteins for human use. Using a deletion mutant strain of α1,6-mannosyltransferase (och1Δ), we previously produced humanized N-glycans in fission yeast; however, the Schizosaccharomyces pombe och1Δ cells displayed a growth delay even during vegetative growth, resulting in reduced productivity of heterologous proteins. To overcome this problem, here we performed a genome-wide screen for genes that would suppress the growth defect of temperature-sensitive och1Δ cells. Using a genomic library coupled with screening of 18,000 transformants, we identified two genes (pwp1
Identifiants
pubmed: 34738170
doi: 10.1007/s00253-021-11649-5
pii: 10.1007/s00253-021-11649-5
doi:
Substances chimiques
GPI-Linked Proteins
0
Schizosaccharomyces pombe Proteins
0
Mannosyltransferases
EC 2.4.1.-
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
8771-8781Subventions
Organisme : jsps kakenhi
ID : JP17H03966
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Alfa C, Fantes P, Hyams J, Mcleod M, Warbrick E (1993) Experiments with fission yeast: a laboratory manual. Cold Spring Harbor Laboratory Press, New York
Ballou CE, Ballou L, Ball G (1994) Schizosaccharomyces pombe glycosylation mutant with altered cell surface properties. Proc Natl Acad Sci U S A 91:9327–9331
doi: 10.1073/pnas.91.20.9327
Bates S, Hughes HB, Munro CA, Thomas WPH, MacCallum DM, Bertram G, Atrih A, Ferguson MAJ, Brown AJP, Odds FC, Gow NAR (2006) Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans. J Biol Chem 281:90–98
doi: 10.1074/jbc.M510360200
Bush DA, Horisberger M, Horman I, Wursch P (1974) The wall structure of Schizosaccharomyces pombe. J Gen Microbiol 81:199–206
pubmed: 4822119
Choi B-K, Bobrowicz P, 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 U S A 100:5022–5027
doi: 10.1073/pnas.0931263100
De Groot PW, Hellingwerf KJ, Klis FM (2003) Genome-wide identification of fungal GPI proteins. Yeast 20(9):781–796
doi: 10.1002/yea.1007
De Groot PW, De Boer AD, Cunningham J, Dekker HL, De Jong L, Hellingwerf KJ, De Koster C, Klis FM (2004) Proteomic analysis of Candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukaryot Cell 4:955–965
doi: 10.1128/EC.3.4.955-965.2004
De Groot PW, Yin QY, Weig M, Sosinska GJ, Klis FM, De Koster CG (2007) Mass spectrometric identification of covalently bound cell wall proteins from the fission yeast Schizosaccharomyces pombe. Yeast 24(4):267–278
doi: 10.1002/yea.1443
Dichtl K, Samantaray S, Aimanianda V, Zhu Z, Prévost MC, Latgé JP, Ebel F, Wagener J (2015) Aspergillus fumigatus devoid of cell wall β-1,3-glucan is viable, massively sheds galactomannan and is killed by septum formation inhibitors. Mol Microbiol 95(3):458–471
doi: 10.1111/mmi.12877
Giga-Hama Y, Tohda H, Takegawa K, Kumagai H (2007) Schizosaccharomyces pombe minimum genome factory. Biotechnol Appl Biochem 46:147–155
doi: 10.1042/BA20060106
Hamilton SR, Bobrowicz P, Bobrowicz B, Davidson RC, Li H, Mitchell T, Nett JH, Rausch S, Stadheim TA, Wischnewski H, Wildt S, Gerngross TU (2003) Production of complex human glycoprotein in yeast. Science 301:1244–1246
doi: 10.1126/science.1088166
Hamilton SR, Davidson RC, Sethuraman N, Nett JH, Jiang Y, Rios S, Bobrowicz P, Stadheim TA, Li H, Choi B-K, Hopkins D, Wischnewski H, Roser J, Mitchell T, Strawbridge RR, Hooped J, Wildt S, Gerngross TU (2006) Humanization of yeast to produce complex terminally sialylated glycoproeins. Science 313:1441–1443
doi: 10.1126/science.1130256
Hartsuiker E, Bähler J, Kohli J (1998) The role of topoisomerase II in meiotic chromosome condensation and segregation in Schizosaccharomyces pombe. Mol Biol Cell 10:2739–2750
doi: 10.1091/mbc.9.10.2739
Idiris A, Tohda H, Kumagai H, Takegawa K (2010) Engineering of protein secretion in yeast: strategies and impact on protein production. Appl Microbiol Biotechnol 86(2):403–417
Imai Y, Yamamoto M (1994) The fission yeast mating pheromone P-factor: its molecular structure, gene structure, and ability to induce gene expression and G1 arrest in the mating partner. Genes Dev 8(3):328–338
Kapteyn JC, Montijn R, Dijkgraaf G, Ende H, Klis F (1995) Mannoproteins in cell walls of Candida albicans. J Bacteriol 177:3788–3792
doi: 10.1128/jb.177.13.3788-3792.1995
Kapteyn JC, Montijn RC, Vink E, De la Cruz J, Llobell A, Douwes JE, Shimoi H, Lipke PN, Klis FM (1996) Retention of Saccharomyces cerevisiae cell wall proteins through a phosphodiester-linked beta-1,3-/beta-1,6-glucan heteropolymer. Glycobiology 6:337–345
doi: 10.1093/glycob/6.3.337
Kim MK, Kim EJ, Kim J-Y, Park J-S, Oh D-B, Shimma Y-I, Chiba Y, Jigami Y, Rhee SK, Kang HA (2006) Functional characterization of the Hansenula polymorpha HOC1, OCH1, and OCR1 genes as members of the yeast OCH1 mannosyltransferase family involved in protein glycosylation. J Biol Chem 281:6261–6271
doi: 10.1074/jbc.M508507200
Kominami K, Seth-Smith H, Toda T (1998) Apc10 and Ste9/Srw1, two regulators of the APC-cyclosome, as well as the CDK inhibitor Rum1 are required for G1 cell-cycle arrest in fission yeast. EMBO J 17(18):5388–5399
doi: 10.1093/emboj/17.18.5388
Kruppa M, Goins T, Cutler JE, Lowman D, Williams D, Chauhan N, Menon V, Singh P, Li D, Calderone R (2003) The role of the Candida albicans histidine kinase [CHK1] gene in the regulation of cell wall mannan and glucan biosynthesis. FEMS Yeast Res 3:289–299
pubmed: 12689636
Kuroda K, Kobayashi K, Tsumura H, Komeda T, Chiba Y, Jigami Y (2006) Production of Man
doi: 10.1111/j.1567-1364.2006.00116.x
Lu CF, Kurjan J, Lipke PN (1994) A pathway for cell wall anchorage of Saccharomyces cerevisiae alpha-agglutinin. Mol Cell Biol 14:4825–4833
pubmed: 8007981
pmcid: 358855
Lu CF, Montijn RC, Brown JL, Klis F, Kurjan J, Bussey H, Lipke PN (1995) Glycosyl phosphatidylinositol-dependent cross-linking of alpha-agglutinin and beta 1,6-glucan in the Saccharomyces cerevisiae cell wall. J Cell Biol 128:333–340
doi: 10.1083/jcb.128.3.333
Maundrell K (1993) Thiamine-repressible expression vectors pREP and pRIP for fission yeast. Gene 123:127–130
doi: 10.1016/0378-1119(93)90551-D
Moreno S, Klar A, Nurse P (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194:795–823
doi: 10.1016/0076-6879(91)94059-L
Morita T, Takegawa K (2004) A simple and efficient procedure for transformation of Schizosaccharomyces pombe. Yeast 21:613–617
doi: 10.1002/yea.1104
Nakamura T, Nakamura-Kubo M, Hirata A, Shimoda C (2001) The Schizosaccharomyces pombe spo3
doi: 10.1091/mbc.12.12.3955
Nakayama K, Nagasu T, Shinma Y, Kuromitsu J, Jigami Y (1992) OCH1 encodes a novel membrane bound mannosyltransferase: outer chain elongation of asparagines-linked oligosaccharides. EMBO J 11:2511–2519
doi: 10.1002/j.1460-2075.1992.tb05316.x
Ohashi T, Takegawa K (2010) N- and O-linked oligosaccharides completely lack galactose residues in the gms1och1Δ mutant of Schizosaccharomyces pombe. Appl Microbiol Biotechnol 86(1):263–272
doi: 10.1007/s00253-009-2297-9
Ohashi T, Ikeda Y, Tanaka N, Nakakita S, Natsuka S, Giga-Hama Y, Takegawa K (2009) The och1Δ mutant of Schizosaccharomyces pombe produces galactosylated core structures of N-linked oligosaccharides. Biosci Biotechnol Biochem 73:407–414
doi: 10.1271/bbb.80712
Ohashi T, Nakakita S, Sumiyoshi W, Takegawa K (2010) Production of heterologous glycoproteins by a glycosylation-defective alg3och1Δ mutant of Schizosaccharomyces pombe. J Biotechnol 150(3):348–356
doi: 10.1016/j.jbiotec.2010.09.942
Ohashi T, Nakakita S, Sumiyoshi W, Yamada N, Ikeda Y, Tanaka N, Takegawa K (2011) Structural analysis of α1,3-linked galactose-containing oligosaccharides in Schizosaccharomyces pombe mutants harboring single and multiple α-galactosyltransferase genes disruptions. Glycobiology 21:340–351
doi: 10.1093/glycob/cwq167
Okazaki K, Okazaki N, Kume K, Jinno S, Tanaka K, Okayama H (1990) High-frequency transformation method and library transducing vectors for cloning mammalian cDNAs by trans-complementation of Schizosaccharomyces pombe. Nucleic Acids Res 18:6485–6489
doi: 10.1093/nar/18.22.6485
Orlean P (2012) Architecture and biosynthesis of the Saccharomyces cerevisiae cell wall. Genetics 192(3):775–818
doi: 10.1534/genetics.112.144485
Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Schneider C, Rasband W, Eliceiri K (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
doi: 10.1038/nmeth.2089
Song Y, Choi MH, Park J-N, Kim MW, Kim EJ, Kang HA, Kim J-Y (2007) Engineering of the yeast Yarrowia lipolytica for the production of glycoproeins lacking the outer chain mannose residues of N-glycans. Appl Environ Microbiol 73:4446–4454
doi: 10.1128/AEM.02058-06
Takegawa K, Tohda H, Sasaki M, Idris A, Ohashi T, Mukaiyama H, Giga-Hama Y, Kumagai H (2009) Production of heterologous proteins using the fission-yeast (Schizosaccharomyces pombe) expression system. Biotechnol Appl Biochem 53:227–235
doi: 10.1042/BA20090048
Tanaka N, Takegawa K (2001) Functional characterization of Gms1p/UDP-galactose transporter in Schizosaccharomyces pombe. Yeast 18:745–757
doi: 10.1002/yea.725
Walker LA, Lee KK, Munro CA, Gow NA (2015) Caspofungin treatment of Aspergillus fumigatus results in ChsG-dependent upregulation of chitin synthesis and the formation of chitin-rich microcolonies. Antimicrob Agents Chemother 59(10):5932–5941
doi: 10.1128/AAC.00862-15
Wang Y, Maeda Y, Liu YS, Takada Y, Ninomiya A, Hirata T, Fujita M, Murakami Y, Kinoshita T (2020) Cross-talks of glycosylphosphatidylinositol biosynthesis with glycosphingolipid biosynthesis and ER-associated degradation. Nat Commun 11(1):860
doi: 10.1038/s41467-020-14678-2
Yoko-o T, Tsukahara K, Watanabe T, Hata-Sugi N, Yoshimitsu K, Nagasu T, Jigami Y (2001) Schizosaccharomyces pombe och1
doi: 10.1016/S0014-5793(01)02082-8