Predicted N-terminal N-linked glycosylation sites may underlie membrane protein expression patterns in Saccharomyces cerevisiae.
G-protein coupled receptors
N-linked glycosylation
Saccharomyces cerevisiae
expression
membrane proteins
post-translational modifications
Journal
Yeast (Chichester, England)
ISSN: 1097-0061
Titre abrégé: Yeast
Pays: England
ID NLM: 8607637
Informations de publication
Date de publication:
09 2021
09 2021
Historique:
revised:
15
06
2021
received:
27
01
2021
accepted:
17
06
2021
pubmed:
29
6
2021
medline:
28
1
2022
entrez:
28
6
2021
Statut:
ppublish
Résumé
N-linked glycosylation is one type of posttranslational modification that proteins undergo during expression. The following describes the effects of N-linked glycosylation on high-level membrane protein expression in yeast with an emphasis on Saccharomyces cerevisiae. N-linked glycosylation is highlighted here as an important consideration when preparing membrane protein gene constructs for expression in S. cerevisiae, which continues to be used as a workhorse in both research and industrial applications. Non-native N-linked glycosylation commonly occurs during the heterologous expression of mammalian proteins in many yeast species which can have important immunological consequences when used in the production of biotherapeutic proteins or peptides. Further, non-native N-linked glycosylation can lead to improper protein folding and premature degradation, which can impede high-level expression yields and hinder downstream analysis. Multiple strategies are presented in this article, which suggest different methods that can be implemented to circumvent the unwanted consequences of N-linked glycosylation during the expression process. These considerations may have long-term benefits for high-level protein production in S. cerevisiae across a broad spectrum of expression targets with special emphasis placed on G-protein coupled receptors, one of the largest families of membrane proteins.
Substances chimiques
Membrane Proteins
0
Saccharomyces cerevisiae Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
497-506Informations de copyright
© 2021 John Wiley & Sons, Ltd.
Références
Ahmad, M., Hirz, M., Pichler, H., & Schwab, H. (2014). Protein expression in Pichia pastoris: Recent achievements and perspectives for heterologous protein production. Applied Microbiology and Biotechnology, 98, 5301-5317. https://doi.org/10.1007/s00253-014-5732-5
Aicart-Ramos, C., Rodriguez-Crespo, I., & Valero, R. A. (2011). Protein palmitoylation and subcellular trafficking. Biochim. Biophys. Acta.-Biomembranes, 1808, 2981-2994. https://doi.org/10.1016/j.bbamem.2011.07.009
Allen, A. C., Feehally, J., & Harper, S. J. (2008). Galactosylation of N- and O-linked carbohydrate moieties of IgA1 and IgG in IgA nephropathy. Clinical and Experimental Immunology, 100, 470-474. https://doi.org/10.1111/j.1365-2249.1995.tb03724.x
An, H. J., Hedrick, J. L., Lebrilla, C. B., & Peavy, T. R. (2003). Determination of N-glycosylation sites and site heterogeneity in glycoproteins. Analytical Chemistry, 75(20), 5628-5637. https://doi.org/10.1021/ac034414x
Arnold, K., Artimo, P., Baratin, D., Csardi, G., De Castro, E., Duvaud, S., Flegel, V., Fortier, A., Gasteiger, E., Grosdidier, A., Hernandez, C., Ioannidis, V., , Jonnalagedda, M., Kuznetsov, D., Liechti, R., Moretti, S., Mostaguir, K., Redaschi, N., Rossier, G., … Stockinger, H. (2012). ExPASy: SIB bioinformatics resource portal. Nucleic Acids Research, 40(W1), W597-W603. https://doi.org/10.1093/nar/gks400
Audagnotto, M., & Dal Peraro, M. (2017). Protein post-translational modifications: In silico prediction tools and molecular modeling. Comp. Structural Biotechnol. J., 15, 307-319. https://doi.org/10.1016/j.csbj.2017.03.004
Benyair, R., Lederkremer, G. Z., & Ron, E. (2011). Protein quality control, retention, and degradation at the endoplasmic reticulum. International Review of Cell and Molecular Biology, 292, 197-280. https://doi.org/10.1016/B978-0-12-386033-0.00005-0
Bertheleme, N., Byrne, B., Dowell, S., & Singh, S. (2015). Heterologous expression of G-protein-coupled receptors in yeast. Methods in Enzymology, 556, 141-164. https://doi.org/10.1016/bs.mie.2014.11.046
Bian, X., Huang, F., Müller, R., Stewart, F. A., Xia, L., & Zhang, Y. (2012). Direct cloning, genetic engineering, and heterologous expression of the syringolin biosynthetic gene cluster in E. coli through red/ET recombineering. ChemBioChem, 13, 1946-1952. https://doi.org/10.1002/cbic.201200310
Butcher, A. J., Kong, K. C., & Tobin, A. B. (2011). Examining site-specific GPCR phosphorylation. Methods in Molecular Biology, 746, 237-249. https://doi.org/10.1007/978-1-61779-126-0_12
Butz, J. A., Niebauer, R. T., & Robinson, A. S. (2003). Co-expression of molecular chaperones does not improve the heterologous expression of mammalian G-protein coupled receptor expression in yeast. Biotechnology and Bioengineering, 84, 292-304. https://doi.org/10.1002/bit.10771
Cain, J. A., Solis, N., & Cordwell, S. J. (2014). Beyond gene expression: The impact of protein post-translational modifications in bacteria. Journal of Proteomics, 97, 265-286. https://doi.org/10.1016/j.jprot.2013.08.012
Cereghino, G. P. L., Cereghino, J. L., Ilgen, C., & Cregg, J. M. (2002). Production of recombinant proteins in fermenter cultures of the yeast Pichia pastoris. Current Opinion in Biotechnology, 13, 329-332. https://doi.org/10.1016/S0958-1669(02)00330-0
Chiba, Y., & Jigami, Y. (2007). Production of humanized glycoproteins in bacteria and yeasts. Current Opinion in Chemical Biology, 11(6), 670-676. https://doi.org/10.1016/j.cbpa.2007.08.037
Ciruela, F., Gomez-Soler, M., Guidolin, D., Borroto-Escuela, D. O., Agnati, L. F., Fuxe, K., & Fernandez-Duenas, V. (2011). Adenosine receptor containing oligomers: Their role in the control of dopamine and glutamate neurotransmission in the brain. Biochim. Biophys. Acta-Biomembranes., 1808, 1245-1255. https://doi.org/10.1016/j.bbamem.2011.02.007
Clark, L., Dikiy, I., Rosenbaum, D. M., & Gardner, K. H. (2018). On the use of Pichia pastoris for isotopic labeling of human GPCRs for NMR studies. Journal of Biomolecular NMR, 71, 203-211. https://doi.org/10.1007/s10858-018-0204-3
Clements, J. M., Catlin, G. H., Price, M. J., & Edwards, R. M. (1991). Secretion of human epidermal growth factor from Saccharomyces cerevisiae using synthetic leader sequences. Gene, 106, 267-271. https://doi.org/10.1016/0378-1119(91)90209-T
Conde, R., Cueva, R., Pablo, G., Polaina, J., & Larriba, G. (2004). A search for hyperglycosylation signals in yeast glycoproteins. The Journal of Biological Chemistry https://doi.org/10.1074/jbc. M406678200, 279, 43789, 43798
Cooper, C. A., Gasteiger, E., & Packer, N. H. (2001). GlycoMod-A software tool for determining glycosylation compositions from mass spectrometric data. PROTEOMICS: Inter. Ed., 1(2), 340-349.
Costa, A. R., Rodrigues, M. E., Henriques, M., Oliveira, R., & Azeredo, J. (2014). Glycosylation: Impact, control and improvement during therapeutic protein production. Critical Reviews in Biotechnology, 34, 281-299. https://doi.org/10.3109/07388551.2013.793649
Dalbey, R. E., & von Heijne, G. (Eds.). (2002). Protein targeting, transport & translocation. USA: Academic Press.
Delic, M., Valli, M., Graf, A. B., Pfeffer, M., Mattanovich, D., & Gasser, B. (2013). The secretory pathway: Exploring yeast diversity. FEMS Microbiology Reviews, 37, 872-914. https://doi.org/10.1111/1574-6976.12020
Fan, Y., Emami, S., Munro, R., Ladizhansky, V., & Brown, L. S. (2015). Isotope labeling of eukaryotic membrane proteins in yeast for solid-state NMR. Methods in Enzymology, 565, 193-212. https://doi.org/10.1016/bs.mie.2015.05.010
Feilmeier, B. J., Iseminger, G., Schroeder, D., Webber, H., & Phillips, G. J. (2000). Green fluorescent protein functions as a reporter for protein localization in Escherichia coli. Journal of Bacteriology, 182, 4068-4076. https://doi.org/10.1128/JB.182.14.4068-4076.2000
Feyder, S., De Craene, J. O., Bär, S., Bertazzi, D. L., & Friant, S. (2015). Membrane trafficking in the yeast Saccharomyces cerevisiae model. Inter. J. Molec. Sci., 16, 1509-1525. https://doi.org/10.3390/ijms16011509
Freedman, R. B. (1989). Post-translational modification and folding of secreted proteins. Biochemical Society Transactions, 17, 331-335. https://doi.org/10.1042/bst0170331
Gallo-Ebert, C., McCourt, P. C., Donigan, M., Villasmil, M. L., Chen, W., Pandya, D., Franco, J., Romano, D., Chadwick, S. G., Gygax, S. E., & Nickels, J. T. (2012). Arv1 lipid transporter function is conserved between pathogenic and nonpathogenic fungi. Fungal Genetics and Biology, 49, 101-113. https://doi.org/10.1016/j.fgb.2011.11.006
Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R. D., & Bairoch, A. (2003). ExPASy: The proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Research, 31, 3784-3788. https://doi.org/10.1093/nar/gkg563
Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M. R., Appel, R. D., & Bairoch, A. (2005). Protein identification and analysis tools on the ExPASy server. In The Proteomics Protocols Handbook (pp. 571-607). NY: Humana Press. https://doi.org/10.1385/1-59259-890-0:571
Ge, F., Zhu, L., Aang, A., Song, P., Li, W., Tao, Y., & Du, G. (2018). Recent advances in enhanced enzyme activity, thermostability and secretion by N-glycosylation regulation in yeast. Biotechnology Letters, 40(5), 847-854. https://doi.org/10.1007/s10529-018-2526-3
Goddard, A. D., & Watts, A. (2012). Regulation of G protein-coupled receptors by palmitoylation and cholesterol. BMC Biology, 10, 27-29. https://doi.org/10.1186/1741-7007-10-27
Grangeasse, C., Stülke, J., & Mijakovic, I. (2015). Regulatory potential of post-translational modifications in bacteria. Frontiers in Microbiology, 6, 1-2. https://doi.org/10.3389/fmicb.2015.00500
Gupta, S. K., & Shukla, P. (2018). Glycosylation control technologies for recombinant therapeutic proteins. App. Microbiol. Biotechnol., 102, 10457-10468. https://doi.org/10.1007/s00253-018-9430-6
Haines, N., & Irvine, K. D. (2003). Glycosylation regulates Notch signalling. Nat. Rev. Molec. Cell Biol., 4, 786-797. https://doi.org/10.1038/nrm1228
Hanson, M. R., & Köhler, R. H. (2001). GFP imaging: Methodology and application to investigate cellular compartmentation in plants. Journal of Experimental Botany, 52, 529-539. https://doi.org/10.1093/jexbot/52.356.529
Hauser, A. S., Attwood, M. M., Rask-Andersen, M., Schiöth, H. B., & Gloriam, D. E. (2017). Trends in GPCR drug discovery: New agents, targets and indications. Nat. Rev. Drug Disc., 16, 829-842. https://doi.org/10.1038/nrd.2017.178
Håvarstein, L. S., Diep, D. B., & Nes, I. F. (1995). A family of bacteriocin ABC transporters carry out proteolytic processing of their substrates concomitant with export. Molecular Microbiology, 16, 229-240. https://doi.org/10.1111/j.1365-2958.1995.tb02295.x
Hilger, D., Masureel, M., & Kobilka, B. K. (2018). Structure and dynamics of GPCR signaling complexes. Nature Structural & Molecular Biology, 25, 4-12. https://doi.org/10.1038/s41594-017-0011-7
Horn, F., Bettler, E., Oliveira, L., Campagne, F., Cohen, F. E., & Vriend, G. (2003). GPCRDB information system for G protein-coupled receptors. Nucleic Acids Research, 31, 294-297. https://doi.org/10.1093/nar/gkg103
Hu, W., Liu, X., Li, Y., Liu, D., Kuang, Z., Qian, C., & Yao, D. (2017). Rational design for the stability improvement of Armillariella tabescens β-mannanase MAN47 based on N-glycosylation modification. Enzyme and Microbial Technology, 97, 82-89. https://doi.org/10.1016/j.enzmictec.2016.11.005
Irani, Z. A., Kerkhoven, E. J., Shojaosadati, S. A., & Nielsen, J. (2016). Genome-scale metabolic model of Pichia pastoris with native and humanized glycosylation of recombinant proteins. Biotechnology and Bioengineering, 113(5), 961-969. https://doi.org/10.1002/bit.25863
Jacobs, P. P., Geysens, S., Vervecken, W., Contreras, R., & Callewaert, N. (2009). Engineering complex-type N-glycosylation in Pichia pastoris using GlycoSwitch technology. Nature Protocols, 4, 58-70. https://doi.org/10.1038/nprot.2008.213
Jamshad, M., Charlton, J., Lin, Y. P., Routledge, S. J., Bawa, Z., Knowles, T. J., Overduin, M., Dekker, N., Dafforn, T. R., Bill, R. M., Poyner, D. R., & Wheatley, M. (2015). G-protein coupled receptor solubilization and purification for biophysical analysis and functional studies, in the total absence of detergent. Bioscience Reports, 35, e00188-e00198. https://doi.org/10.1042/BSR20140171
Janda, C. Y., Li, J., Oubridge, C., Hernández, H., Robinson, C. V., & Nagai, K. (2010). Recognition of a signal peptide by the signal recognition particle. Nature, 465, 507-510. https://doi.org/10.1038/nature08870
Jigami, Y. (2008). Yeast glycobiology and its application. Biosci., Biotechnol., Biochem., 72(3), 637-648.
Kang, H. A., Sohn, J.-H., Choi, E.-S., Chung, B. H., Yu, M.-H., & Rhee, S.-K. (1998). Glycosylation of human α1-antitrypsin in Saccharomyces cerevisiae and methylotrophic yeasts. Yeast, 14(4), 371-381. https://doi.org/10.1002/(SICI)1097-0061(19980315)14:4<371::AID-YEA231>3.0.CO;2-1
Karbalaei, M., Rezaee, S.A. & Farsiani, H. (2021). Pichia pastoris: A highly successful expression system for optimal synthesis of heterologous proteins. Journal of Cellular Physiology, https;//doi.org/https://doi.org/10.1002/jcp.29583, 235, 5867, 5881
Kelkar, D. A., & Chattopadhyay, A. (2007). The gramicidin ion channel: A model membrane protein. Biochim. Biophys. Acta-Biomembranes., 1768, 2011-2025. https://doi.org/10.1016/j.bbamem.2007.05.011
Kersten, R. D., Ziemert, N., Gonzalez, D. J., Duggan, B. M., Nizet, V., Dorrestein, P. C., & Moore, B. S. (2013). Glycogenomics as a mass spectrometry-guided genome-mining method for microbial glycosylated molecules. Proceedings of the National Academy of Sciences, 110(47), E4407-E4416.
Khan, A. H., & Noordin, R. (2019). Strategies for humanizing glycosylation pathways and producing recombinant glycoproteins in microbial expression systems. Biotechnology Progress, 35, e2752. https://doi.org/10.1002/btpr.2752
Kim, H. J., & Kim, H.-J. (2017). Yeast as an expression system for producing virus-like particles: What factors do we need to consider? Letters in Applied Microbiology, 64, 111-123. https://doi.org/10.1111/lam.12695
Kim, Y. H., Kwak, M. S., Park, J. B., Lee, S.-A., Choi, J. E., Cho, H.-S., & Shin, J.-S. (2016). N-linked glycosylation plays a crucial role in the secretion of HMGB1. Journal of Cell Science, 129, 29-38. https://doi.org/10.1242/jcs.176412
Kruszewska, J. S., Butterweck, A. H., Kurza, W., Migdalski, A., & Kubicek, C. P. (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. Applied and Environmental Microbiology, 65(6), 2382-2387. https://doi.org/10.1128/AEM.65.6.2382-2387.1999
Laurent, J. M., Young, J. H., Kachroo, A. H., & Marcotte, E. M. (2016). Efforts to make and apply humanized yeast. Briefings in Functional Genomics, 15, 155-163. https://doi.org/10.1093/bfgp/elv041
Lee, H. S., Qi, Y., & Im, W. (2015). Effects of N-glycosylation on protein conformation and dynamics: Protein data bank analysis and molecular dynamics simulation study. Scientific Reports, 5, 8926-8932. https://doi.org/10.1038/srep08926
Letts, J. A., & Sazanov, L. A. (2017). Clarifying the supercomplex: The higher-order organization of the mitochondrial electron transport chain. Nature Structural & Molecular Biology, 24, 800-808. https://doi.org/10.1038/nsmb.3460
Liang, Y., Eng, W. S., Colquhoun, D. R., Dinglasan, R. R., Graham, D. R., & Mahal, L. K. (2014). Complex N-linked glycans serve as a determinant for exosome/microvesicle cargo recruitment. The Journal of Biological Chemistry, 289, 32526-32537. https://doi.org/10.1074/jbc.M114.606269
Macauley-Patrick, S., Fazenda, M. L., McNeil, B., & Harvey, L. M. (2005). Heterologous protein production using the Pichia pastoris expression system. Yeast, 22, 249-270. https://doi.org/10.1002/yea.1208
Miao, Y., & McCammon, J. A. (2016). G-protein coupled receptors: Advances in simulation and drug discovery. Current Opinion in Structural Biology, 41, 83-89. https://doi.org/10.1016/j.sbi.2016.06.008
Miller, K. D., Weaver-Feldhaus, J., Gray, S. A., Siegel, R. W., & Feldhaus, M. J. (2005). Production, purification, and characterization of human scFv antibodies expressed in Saccharomyces cerevisiae, Pichia pastoris, and Escherichia coli. Protein Expression and Purification, 42, 255-267. https://doi.org/10.1016/j.pep.2005.04.015
Min, C., Zheng, M., Zhang, X., Guo, S., Kwon, K. J., Shin, C. Y., Kim, H. S., Cheon, S. H., & Kim, K. M. (2015). N-linked glycosylation on the N-terminus of the dopamine D2 and D3 receptors determines receptor association with specific microdomains in the plasma membrane. Biochim. Biophys. Acta - Molecular Cell Research., 1853, 41-51. https://doi.org/10.1016/j.bbamcr.2014.09.024
Monaco, G., Rovere, R. L., Karamanou, S., Welkenhuyzen, K., Ivanova, H., Vandermarliere, E., Martile, M. D., Bufalo, D. D., Smedt, H. D., Parys, J. B., Economou, A., & Bultynck, G. (2018). A double point mutation at residues Ile14 and Val15 of Bcl-2 uncovers a role for the BH4 domain in both protein stability and function. FEBS., 285, 127-145. https://doi.org/10.1111/febs.14324
Montesino, R., García, R., Quintero, O., & Cremata, J. A. (1998). Variation in N-linked oligosaccharide structures on heterologous proteins secreted by the methylotrophic yeast Pichia pastoris. Protein Expression and Purification, 14, 197-207. https://doi.org/10.1006/prep.1998.0933
Morawski, B., Lin, Z., Cirino, P., Joo, H., Bandara, G., & Arnold, F. H. (2000). Functional expression of horseradish peroxidase in Saccharomyces cerevisiae and Pichia pastoris. Protein Engineering, Design & Selection, 13, 377-384. https://doi.org/10.1093/protein/13.5.377
Mus-Veteau, I. (Ed.) (2014). Membrane proteins production for structural analysis. In Membrane Proteins Production for Structural Analysis (1st ed., pp. 1-44). NY: Springer. https://doi.org/10.1007/978-1-4939-0662-8
Nakamura, S., Takasaki, H., Kobayashi, K., & Kato, A. (1993). Hyperglycosylation of hen egg white lysozyme in yeast. The Journal of Biological Chemistry, 268(17), 12706-12712. https://doi.org/10.1016/S0021-9258(18)31445-5
Naumenko, V. S., & Ponimaskin, E. (2018). Palmitoylation as a functional regulator of neurotransmitter receptors. Neural Plasticity., 2018, 1-18. https://doi.org/10.1155/2018/5701348
Ng, D. T., Brown, J. D., & Walter, P. (1996). Signal sequences specify the targeting route to the endoplasmic reticulum membrane. The Journal of Cell Biology, 134(2), 269-278. https://doi.org/10.1083/jcb.134.2.269
Ngo, T., Ilatovskiy, A. V., Stewart, A. G., Coleman, J. L. J., McRobb, F. M., Riek, R. P., Graham, R. M., Abagyan, R., Kufareva, I., & Smith, N. J. (2017). Orphan receptor ligand discovery by pickpocketing pharmacological neighbors. Nature Chemical Biology, 13, 235-242. https://doi.org/10.1038/nchembio.2266
Nissley, D. A., Sharma, A. K., Ahmed, N., Friedrich, U. A., Kramer, G., Bukau, B., & O'Brien, E. P. (2016). Accurate prediction of cellular co-translational folding indicates proteins can switch from post- to co-translational folding. Nature Communications, 7, 10341-10353. https://doi.org/10.1038/ncomms10341
O'Malley, M. A., Mancini, J. D., Young, C. L., McCusker, E. C., Raden, D., & Robinson, A. S. (2009). Progress toward heterologous expression of active G-protein-coupled receptors in Saccharomyces cerevisiae: Linking cellular stress response with translocation and trafficking. Protein Science, 18, 2356-2370. https://doi.org/10.1002/pro.246
O'Malley, M. A., Robinson, A. S., Niebauer, R. T., & Wedekind, A. (2006). Optimization of the human adenosine A2a receptor yields in Saccharomyces cerevisiae. Biotechnology Progress, 22, 1249-1255. https://doi.org/10.1021/bp050431r
Ons, S., Lavore, A., Sterkel, M., Wulff, J. P., Sierra, I., Martínez-Barnetche, J., Rodriguez, M. H., & Rivera-Pomar, R. (2016). Identification of G protein coupled receptors for opsines and neurohormones in Rhodnius prolixus. Genomic and Transcriptomic Analysis. Insect Biochemistry and Molecular Biology, 69, 34-50. https://doi.org/10.1016/j.ibmb.2015.05.003
Oueslati, A., Fournier, M., & Lashuel, H. A. (2010). Role of post-translational modifications in modulating the structure, function and toxicity of α-synuclein. Implications for Parkinson's Disease Pathogenesis and Theries. Progress in Brain Research, 183, 115-145. https://doi.org/10.1016/S0079-6123(10)83007-9
Pines, O., & Inouye, M. (1999). Expression and secretion of proteins in E. coli. Appl. Biochem. Biotechnol.-Part B Molecular Biotechnology, 12, 25-34. https://doi.org/10.1385/MB:12:1:25
Razaghi, A., Owens, L., & Heimann, K. (2016). Review of the recombinant human interferon gamma as an immunotherapeutic: Impacts of production platforms and glycosylation. Journal of Biotechnology, 240, 48-60. https://doi.org/10.1016/j.jbiotec.2016.10.022
Rosenbaum, D. M., Rasmussen, S. G. F., & Kobilka, B. K. (2009). The structure and function of G-protein-coupled receptors. Nature, 459, 356-363. https://doi.org/10.1038/nature08144
Roth, J., Zuber, C., Park, S., Jang, I., Lee, Y., Kysela, K. G., Fourn, V., Santimaria, R., Guhl, B., & Cho, J. W. (2010). Protein N-glycosylation, protein folding, and protein quality control. Molecules and Cells, 30, 497-506. https://doi.org/10.1007/s10059-010-0159-z
Routledge, S. J., Mikaliunaite, L., Patel, A., Clare, M., Cartwright, S. P., Bawa, Z., Wilks, M. D. B., Low, F., Hardy, D., Rothnie, A. J., & Bill, R. M. (2016). The synthesis of recombinant membrane proteins in yeast for structural studies. Methods, 95, 26-37. https://doi.org/10.1016/j.ymeth.2015.09.027
Saida, F., Uzan, M., Odaert, B., & Bontems, F. (2006). Expression of Highly Toxic Genes in E. coli: Special Strategies and Genetic Tools. Curr. Protein Pept. Sci. 7, 47-56. https://doi.org/10.2174/138920306775474095
Scheller, C., Krebs, F., Wiesner, R., Wätzig, H., & Oltmann-Norden, I. (2021). A comparative study of CE-SDS, SDS-PAGE and simple western-Precision, repeatability and apparent molecular mass shifts by glycosylation. Electrophoresis, 0, 1-11. https://doi.org/10.1002/elps.202100068
Schonenbach, N. S., Hussain, S., & O'Malley, M. A. (2015). Structure and function of G protein-coupled receptor oligomers: Implications for drug discovery. Wiley Interdisciplinary Reviews. Nanomedicine and Nanobiotechnology, 7, 408-427. https://doi.org/10.1002/wnan.1319
Sebban-Kreuzer, C., Deprez-Beauclair, P., Berton, A., & Crenon, I. (2006). High-level expression of nonglycosylated human pancreatic lipase-related protein 2 in Pichia pastoris. Protein Expression and Purification, 49(2), 284-291. https://doi.org/10.1016/j.pep.2006.06.001
Simon, E. J., & Linstedt, A. D. (2018). Site-specific glycosylation of Ebola virus glycoprotein by human polypeptide GalNAc-transferase 1 induces cell adhesion defects. The Journal of Biological Chemistry, 293, 19866-19873. https://doi.org/10.1074/jbc.RA118.005375
Snider, N. T., & Omary, M. B. (2014). Post-translational modifications of intermediate filament proteins: Mechanisms and functions. Nature Reviews. Molecular Cell Biology, 15, 163-177. https://doi.org/10.1038/nrm3753
Solá, R. J., & Griebenow, K. (2010). Glycosylation of Therapeutic Proteins. BioDrugs, 24, 9-21. https://doi.org/10.2165/11530550-000000000-00000
Soto, A. G., Smith, T. H., Chen, B., Bhattacharya, S., Cordova, I. C., Kenakin, T., Vaidehi, N., Trejo, J. A., & Lefkowitz, R. J. (2015). N-linked glycosylation of protease-activated receptor-1 at extracellular loop 2 regulates G-protein signaling bias. Proceedings of the National Academy of Sciences, 112, E3600-E3608. https://doi.org/10.1073/pnas.1508838112
Stanley, P., Taniguchi, N., & Aebi, M. (2017). N-glycans. Essentials of Glycobiology (Chap. 9, 3rd ed., pp. 1-13). Cold Spring Harbor, NY: Cold Spring Harbor Laboratories. https://doi.org/10.1101/glycobiology.3e.009
Sugiki, T., Ichikawa, O., Miyazawa-Onami, M., Shimada, I., & Takahashi, H. (2012). Isotopic labeling of heterologous proteins in the yeast Pichia pastoris and Kluyveromyces lactis. In Methods in Molecular Biology (Vol. 831, pp. 19-36). NY: Humana Press. https://doi.org/10.1007/978-1-61779-480-3_2
Tokmakov, A. A., Kurotani, A., Takagi, T., Toyama, M., Shirouzu, M., Fukami, Y., & Yokoyama, S. (2012). Multiple post-translational modifications affect heterologous protein synthesis. The Journal of Biological Chemistry, 287, 27106-27116. https://doi.org/10.1074/jbc.M112.366351
Traynelis, S. F., Wollmuth, L. P., McBain, C. J., Menniti, F. S., Vance, K. M., Ogden, K. K., Hansen, K. B., Yuan, H., Myers, S. J., & Dingledine, R. (2010). Glutamate receptor ion channels: Structure, regulation, and function. Pharmacological Reviews, 62, 405-496. https://doi.org/10.1124/pr.109.002451
Varki, A., Cummings, R. D., Esko, J. D., Freeze, H. H., Stanley, P., Bertozzi, C. R., Hart, G. W., & Etzler, M. E. (Eds.) (2009). Essentials of Glycobiology (2nd ed.). Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.
Voolstra, O., & Huber, A. (2014). Post-Translational Modifications of TRP Channels. Cell, 3(2), 258-287. https://doi.org/10.3390/cells3020258
Wang, T., Chu, L., Li, W., Lawson, K., Apostol, I., & Eris, T. (2017). Application of a quantitative LC-MS multiattribute method for monitoring site-specific glycan heterogeneity on a monoclonal antibody containing two N-linked glycosylation sites. Analytical Chemistry, 89, 3562-3567. https://doi.org/10.1021/acs.analchem.6b04856
Wang, T.-Y., Huang, C.-J., Chen, H.-L., Ho, P.-C., Ke, H.-M., Cho, H.-Y., Ruan, S.-K., Hung, K.-Y., Wang, I.-L., Cai, Y.-W., Sung, H.-M., Li, W.-H., & Shih, M.-C. (2013). Systematic screening of glycosylation- and trafficking-associated gene knockouts in Saccharomyces cerevisiae identifies mutants with improved heterologous exocellulase activity and host secretion. BMC Biotechnology, 13, 71. https://doi.org/10.1186/1472-6750-13-71
Wedekind, A., O'Malley, M. A., Niebauer, R. T., & Robinson, A. S. (2006). Optimization of the human adenosine A2a receptor yields in Saccharomyces cerevisiae. Biotechnology Progress, 22, 1249-1255. https://doi.org/10.1021/bp050431r
West, C. M., Malzl, D., Hykollari, A., & Wilson, I. B. H. (2021). Glycomics, glycoproteomics, and glycogenomics: An inter-taxa evolutionary perspective. Molecular & Cellular Proteomics https://doi.org/10.1074/mcp. R120.002263, 20, 100024
Wickner, S., Maurizi, M. R., & Gottesman, S. (1999). Posttranslational quality control: Folding, refolding, and degrading proteins. Science, 286, 1888-1893. https://doi.org/10.1126/science.286.5446.1888
Wildt, S., & Gerngross, T. U. (2005). The humanization of N-glycosylation pathways in yeast. Nature Reviews. Microbiology, 3, 119-128. https://doi.org/10.1038/nrmicro1087
Wloga, D., & Gaertig, J. (2010). Post-translational modifications of microtubules. Journal of Cell Science, 123, 3447-3455. https://doi.org/10.1242/jcs.063727
Yoo, J., Mashalidis, E. H., Kuk, A. C., Yamamoto, K., Kaeser, B., Ichikawa, S., & Lee, S.-Y. (2018). GlcNAc-1-P-transferase-tunicamycin complex structure reveals basis for inhibition of N-glycosylation. Nature Structural & Molecular Biology, 25(3), 217-224. https://doi.org/10.1038/s41594-018-0031-y
Young, C. L., & Robinson, A. S. (2014). Protein folding and secretion: Mechanistic insights advancing recombinant protein production in S. cerevisiae. Curr. Opin. Biotechnol, 30, 168-177. https://doi.org/10.1016/j.copbio.2014.06.018
Zuckerman, D. M., Hicks, S. W., Charron, G., Hang, H. C., & Machamer, C. E. (2011). Differential regulation of two palmitoylation sites in the cytoplasmic tail of the beta1-adrenergic receptor. The Journal of Biological Chemistry, 286, 19014-19023. https://doi.org/10.1074/jbc.M110.189977