Saccharomyces cerevisiae as a superior host for overproduction of prokaryotic integral membrane proteins

Current Research in Structural Biology - Tập 3 - Trang 51-71 - 2021
Sarah Spruce Preisler1, Anders Drabaek Wiuf2, Marc Friis1, Lasse Kjaergaard1, Molly Hurd3, Eva Ramos Becares2, Casper Normann Nurup1, Frederik Bühring Bjoerkskov1, Zsófia Szathmáry1, Pontus Emanuel Gourdon2, Kirstine Calloe3, Dan A. Klaerke3, Kamil Gotfryd2, Per Amstrup Pedersen1
1Department of Biology, University of Copenhagen, Universitetsparken 13, DK-2100, Copenhagen, OE, Denmark
2Membrane Protein Structural Biology Group, Department of Biomedical Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Maersk Tower 7-9, DK 2200, Copenhagen N, Denmark
3University of Copenhagen, Department of Veterinary and Animal Sciences, Dyrlaegevej 100, Frederiksberg, DK, 1870, Denmark

Tài liệu tham khảo

Baker, 2017, Charged residues next to transmembrane regions revisited: "Positive-inside rule" is complemented by the "negative inside depletion/outside enrichment rule, BMC Biol., 15, 66, 10.1186/s12915-017-0404-4 Bannwarth, 2003, The expression of outer membrane proteins for crystallization, Biochim. Biophys. Acta, 1610, 37, 10.1016/S0005-2736(02)00711-3 Bill, 2014, Playing catch-up with Escherichia coli: using yeast to increase success rates in recombinant protein production experiments, Front. Microbiol., 5, 85, 10.3389/fmicb.2014.00085 Bill, 2011, Overcoming barriers to membrane protein structure determination, Nat. Biotechnol., 29, 335, 10.1038/nbt.1833 Bjorkskov, 2017, Purification and functional comparison of nine human Aquaporins produced in Saccharomyces cerevisiae for the purpose of biophysical characterization, Sci. Rep., 7, 16899, 10.1038/s41598-017-17095-6 Bohnsack, 2010, The evolution of protein targeting and translocation systems, Biochim. Biophys. Acta, 1803, 1115, 10.1016/j.bbamcr.2010.06.005 Bomholt, 2013, Recombinant production of human Aquaporin-1 to an exceptional high membrane density in Saccharomyces cerevisiae, PloS One, 8, 10.1371/journal.pone.0056431 Burley, 2019, RCSB Protein Data Bank: biological macromolecular structures enabling research and education in fundamental biology, biomedicine, biotechnology and energy, Nucleic Acids Res., 47, D464, 10.1093/nar/gky1004 Callahan, 2018, Molecular dynamics of ion conduction through the selectivity filter of the NaVAb sodium channel, J. Phys. Chem. B, 122, 10126, 10.1021/acs.jpcb.8b09678 Cesareni, 1987, Plasmid vectors carrying the replication origin of filamentous single-stranded phages, 135 Conde, 2004, A search for hyperglycosylation signals in yeast glycoproteins, J. Biol. Chem., 279, 43789, 10.1074/jbc.M406678200 Cournia, 2015, Membrane protein structure, function, and dynamics: a perspective from experiments and theory, J. Membr. Biol., 248, 611, 10.1007/s00232-015-9802-0 Cross, 2009, Delivering proteins for export from the cytosol, Nat. Rev. Mol. Cell Biol., 10, 255, 10.1038/nrm2657 Cymer, 2015, Mechanisms of integral membrane protein insertion and folding, J. Mol. Biol., 427, 999, 10.1016/j.jmb.2014.09.014 de Kroon, 2013, Checks and balances in membrane phospholipid class and acyl chain homeostasis, the yeast perspective, Prog. Lipid Res., 52, 374, 10.1016/j.plipres.2013.04.006 Dilworth, 2018, Microbial expression systems for membrane proteins, Methods, 147, 3, 10.1016/j.ymeth.2018.04.009 Dowhan W, 2008, Functional roles of lipids in membranes Drew, 2001, Green fluorescent protein as an indicator to monitor membrane protein overexpression in Escherichia coli, FEBS (Fed. Eur. Biochem. Soc.) Lett., 507, 220, 10.1016/S0014-5793(01)02980-5 Fantini, 2013, How cholesterol interacts with membrane proteins: an exploration of cholesterol-binding sites including CRAC, CARC, and tilted domains, Front. Physiol., 4 Freigassner, 2009, Tuning microbial hosts for membrane protein production, Microb. Cell Factories, 8, 69, 10.1186/1475-2859-8-69 Geertsma, 2008, Quality control of overexpressed membrane proteins, Proc. Natl. Acad. Sci. U. S. A., 105, 5722, 10.1073/pnas.0802190105 Gietz, 2007, Frozen competent yeast cells that can be transformed with high efficiency using the LiAc/SS carrier DNA/PEG method, Nat. Protoc., 2, 1, 10.1038/nprot.2007.17 Gileadi, 2017, Recombinant protein expression in E. coli : a historical perspective, Methods Mol. Biol., 1586, 3, 10.1007/978-1-4939-6887-9_1 Gong, 2019, Understanding membrane protein drug targets in computational perspective, Curr. Drug Targets, 20, 551, 10.2174/1389450120666181204164721 Gotfryd, 2018, Human adipose glycerol flux is regulated by a pH gate in AQP10, Nat. Commun., 9, 4749, 10.1038/s41467-018-07176-z Grouleff, 2015, The influence of cholesterol on membrane protein structure, function, and dynamics studied by molecular dynamics simulations, Biochim. Biophys. Acta, 1848, 1783, 10.1016/j.bbamem.2015.03.029 Hsieh, 2010, Bridging the gap: a GFP-based strategy for overexpression and purification of membrane proteins with intra and extracellular C-termini, Protein Sci., 19, 868, 10.1002/pro.365 Jain, 2014, Biosynthesis of archaeal membrane ether lipids, Front. Microbiol., 5, 641, 10.3389/fmicb.2014.00641 Kanonenberg, 2019, Shaping the lipid composition of bacterial membranes for membrane protein production, Microb. Cell Factories, 18, 131, 10.1186/s12934-019-1182-1 Kiefer, 2003, In vitro folding of alpha-helical membrane proteins, Biochim. Biophys. Acta, 1610, 57, 10.1016/S0005-2736(02)00717-4 Klose, 2012, Flexibility of a eukaryotic lipidome-insights from yeast lipidomics, PloS One, 7, 10.1371/journal.pone.0035063 Krogh, 2001, Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes, J. Mol. Biol., 305, 567, 10.1006/jmbi.2000.4315 Kwon, 2015, Comparative genomics and experimental evolution of Escherichia coli BL21(DE3) strains reveal the landscape of toxicity escape from membrane protein overproduction, Sci. Rep., 5, 16076, 10.1038/srep16076 Laemmli, 1970, Cleavage of structural proteins during assembly of head of bacteriophage-T4, Nature, 227, 680, 10.1038/227680a0 LeMasurier, 2001, KcsA: it’s a potassium channel, J. Gen. Physiol., 118, 303, 10.1085/jgp.118.3.303 Lin, 2010, Selective electrodiffusion of zinc ions in a Zrt-, Irt-like protein, ZIPB, J. Biol. Chem., 285, 39013, 10.1074/jbc.M110.180620 Lyons, 2016, Expression strategies for structural studies of eukaryotic membrane proteins, Curr. Opin. Struct. Biol., 38, 137, 10.1016/j.sbi.2016.06.011 Ma, 2015, A versatile strategy for production of membrane proteins with diverse topologies: application to investigation of bacterial homologues of human divalent metal ion and nucleoside transporters, PloS One, 10, 10.1371/journal.pone.0143010 Martens, 2016, Lipids modulate the conformational dynamics of a secondary multidrug transporter, Nat. Struct. Mol. Biol., 23, 744, 10.1038/nsmb.3262 Mesters, 2007, Protein glycosylation, sweet to crystal growth?, Cryst. Growth Des., 7, 2251, 10.1021/cg7006843 Miroux, 1996, Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels, J. Mol. Biol., 260, 289, 10.1006/jmbi.1996.0399 Mohanty, 2004, Membrane protein expression and production: effects of polyhistidine tag length and position, Protein Expr. Purif., 33, 311, 10.1016/j.pep.2003.10.010 Molbaek, 2015, High yield purification of full-length functional hERG K+ channels produced in Saccharomyces cerevisiae, Microb. Cell Factories, 14, 15, 10.1186/s12934-015-0193-9 Neubert, 2016, Mapping the O-mannose glycoproteome in Saccharomyces cerevisiae, Mol. Cell. Proteomics, 15, 1323, 10.1074/mcp.M115.057505 Pandey, 2016, Current strategies for protein production and purification enabling membrane protein structural biology, Biochem. Cell. Biol., 94, 507, 10.1139/bcb-2015-0143 Pechmann, 2013, The ribosome as a hub for protein quality control, Mol. Cell, 49, 411, 10.1016/j.molcel.2013.01.020 Pedersen, 1996, Expression in high yield of pig alpha 1 beta 1 Na,K-ATPase and inactive mutants D369N and D807N in Saccharomyces cerevisiae, J. Biol. Chem., 271, 2514, 10.1074/jbc.271.5.2514 Punta, 2009, Structural genomics target selection for the New York consortium on membrane protein structure, J. Struct. Funct. Genom., 10, 255, 10.1007/s10969-009-9071-1 Quick, 2002, Employing Escherichia coli to functionally express, purify, and characterize a human transporter, Proc. Natl. Acad. Sci. U.S.A., 99, 8597, 10.1073/pnas.132266599 Rahman, 2007, Topology-informed strategies for the overexpression and purification of membrane proteins, Mol. Membr. Biol., 24, 407, 10.1080/09687860701243998 Rath, 2009, Detergent binding explains anomalous SDS-PAGE migration of membrane proteins, Proc. Natl. Acad. Sci. U. S. A., 106, 1760, 10.1073/pnas.0813167106 Renne, 2018, The role of phospholipid molecular species in determining the physical properties of yeast membranes, FEBS Lett., 592, 1330, 10.1002/1873-3468.12944 Routledge, 2016, The synthesis of recombinant membrane proteins in yeast for structural studies, Methods, 95, 26, 10.1016/j.ymeth.2015.09.027 Scharff-Poulsen, 2013, Saccharomyces cerevisiae-based platform for rapid production and evaluation of eukaryotic nutrient transporters and transceptors for biochemical studies and crystallography, PloS One, 8, 10.1371/journal.pone.0076851 Schlegel, 2014, Bacterial-based membrane protein production, Biochim. Biophys. Acta, 1843, 1739, 10.1016/j.bbamcr.2013.10.023 Seppala, 2010, Control of membrane protein topology by a single C-terminal residue, Science, 328, 1698, 10.1126/science.1188950 Shaya, 2011, Voltage-gated sodium channel (NaV) protein dissection creates a set of functional pore-only proteins, Proc. Natl. Acad. Sci. U. S. A., 108, 12313, 10.1073/pnas.1106811108 Some, 2019, Characterization of proteins by size-exclusion chromatography coupled to multi-angle light scattering (SEC-MALS), JoVE, 148 Stephenson, 2005, Sec-dependent protein translocation across biological membranes: evolutionary conservation of an essential protein transport pathway (review), Mol. Membr. Biol., 22, 17, 10.1080/09687860500063308 Studier, 1991, Use of bacteriophage-T7 lysozyme to improve an inducible T7 expression system, J. Mol. Biol., 219, 37, 10.1016/0022-2836(91)90855-Z Studier, 1986, Use of bacteriophage-T7 rna-polymerase to direct selective high-level expression of cloned genes, J. Mol. Biol., 189, 113, 10.1016/0022-2836(86)90385-2 UniProt, 2019, UniProt: a worldwide hub of protein knowledge, Nucleic Acids Res., 47, D506, 10.1093/nar/gky1049 Wang, 2019, Structure of the human ClC-1 chloride channel, PLoS Biol., 17, 10.1371/journal.pbio.3000218 White, 1999, Membrane protein folding and stability: physical principles, Annu. Rev. Biophys. Biomol. Struct., 28, 319, 10.1146/annurev.biophys.28.1.319 Widmann, 2000, Comparison of folding rates of homologous prokaryotic and eukaryotic proteins, J. Biol. Chem., 275, 18619, 10.1074/jbc.C000156200 Yin, 2016, Drugging membrane protein interactions, Annu. Rev. Biomed. Eng., 18, 51, 10.1146/annurev-bioeng-092115-025322