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Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Mini-Review Article

Challenges and Solutions in the Recombinant Expression of Membrane Proteins

Author(s): Caijuan Liu, Hanxue He, Jie Tian and Yunqi Ma*

Volume 30, Issue 10, 2023

Published on: 10 October, 2023

Page: [806 - 820] Pages: 15

DOI: 10.2174/0109298665264728230920070145

Price: $65

Abstract

Membrane proteins are important components of the proteome and play key roles in many biological processes, such as signal transduction, material transport, cell recognition, etc. Membrane proteins are involved in several fields, and more and more researchers want to understand them. However, the structural properties of membrane proteins make their recombinant expression yield low. This adversely affects the study of the structure and function of membrane proteins. Therefore, it is crucial to have a comprehensive and up-to-date understanding of membrane protein recombinant expression. Based on the current stage of research on membrane proteins, the article describes the current challenges faced by membrane protein recombinant expression and the solutions that can be applied to lay the foundation for a better study of membrane proteins in the future.

Keywords: Membrane proteins, recombinant expression, solubility, posttranslational modifications, GPCRs, neurodegenerative disease.

Graphical Abstract
[1]
Ryu, H.; Fuwad, A.; Yoon, S.; Jang, H.; Lee, J.; Kim, S.; Jeon, T.J. Biomimetic membranes with transmembrane proteins: state-of-the-art in transmembrane protein applications. Int. J. Mol. Sci., 2019, 20(6), 1437.
[http://dx.doi.org/10.3390/ijms20061437] [PMID: 30901910]
[2]
Fliegel, L. Structure and function of membrane proteins. Int. J. Mol. Sci., 2023, 24(9), 8350.
[http://dx.doi.org/10.3390/ijms24098350] [PMID: 37176058]
[3]
Le Bon, C.; Marconnet, A.; Masscheleyn, S.; Popot, J.L.; Zoonens, M. Folding and stabilizing membrane proteins in amphipol A8-35. Methods, 2018, 147, 95-105.
[http://dx.doi.org/10.1016/j.ymeth.2018.04.012] [PMID: 29678587]
[4]
Tosaka, T.; Kamiya, K. Function investigations and applications of membrane proteins on artificial lipid membranes. Int. J. Mol. Sci., 2023, 24(8), 7231.
[http://dx.doi.org/10.3390/ijms24087231] [PMID: 37108393]
[5]
Congreve, M.; de Graaf, C.; Swain, N.A.; Tate, C.G. Impact of GPCR structures on drug discovery. Cell, 2020, 181(1), 81-91.
[http://dx.doi.org/10.1016/j.cell.2020.03.003] [PMID: 32243800]
[6]
Davenport, A.P.; Scully, C.C.G.; de Graaf, C.; Brown, A.J.H.; Maguire, J.J. Advances in therapeutic peptides targeting G protein-coupled receptors. Nat. Rev. Drug Discov., 2020, 19(6), 389-413.
[http://dx.doi.org/10.1038/s41573-020-0062-z] [PMID: 32494050]
[7]
Lee, Y.; Warne, T.; Nehmé, R.; Pandey, S.; Dwivedi-Agnihotri, H.; Chaturvedi, M.; Edwards, P.C.; García-Nafría, J.; Leslie, A.G.W.; Shukla, A.K.; Tate, C.G. Molecular basis of β-arrestin coupling to formoterol-bound β1-adrenoceptor. Nature, 2020, 583(7818), 862-866.
[http://dx.doi.org/10.1038/s41586-020-2419-1] [PMID: 32555462]
[8]
Koivisto, A.P.; Belvisi, M.G.; Gaudet, R.; Szallasi, A. Advances in TRP channel drug discovery: From target validation to clinical studies. Nat. Rev. Drug Discov., 2022, 21(1), 41-59.
[http://dx.doi.org/10.1038/s41573-021-00268-4] [PMID: 34526696]
[9]
Rosenbaum, M.I.; Clemmensen, L.S.; Bredt, D.S.; Bettler, B.; Strømgaard, K. Targeting receptor complexes: A new dimension in drug discovery. Nat. Rev. Drug Discov., 2020, 19(12), 884-901.
[http://dx.doi.org/10.1038/s41573-020-0086-4] [PMID: 33177699]
[10]
Rahimov, F.; Kunkel, L.M. Cellular and molecular mechanisms underlying muscular dystrophy. J. Cell Biol., 2013, 201(4), 499-510.
[http://dx.doi.org/10.1083/jcb.201212142] [PMID: 23671309]
[11]
Santos, R.; Ursu, O.; Gaulton, A.; Bento, A.P.; Donadi, R.S.; Bologa, C.G.; Karlsson, A.; Al-Lazikani, B.; Hersey, A.; Oprea, T.I.; Overington, J.P. A comprehensive map of molecular drug targets. Nat. Rev. Drug Discov., 2017, 16(1), 19-34.
[http://dx.doi.org/10.1038/nrd.2016.230] [PMID: 27910877]
[12]
John, P. How many drug targets are there? Nat. Rev. Drug Discov., 2006, 5(12), 993-996.
[13]
Hutchings, C.J.; Colussi, P.; Clark, T.G. Ion channels as therapeutic antibody targets. MAbs, 2019, 11(2), 265-296.
[http://dx.doi.org/10.1080/19420862.2018.1548232] [PMID: 30526315]
[14]
Alballa, M.; Butler, G. Integrative approach for detecting membrane proteins. BMC Bioinformatics, 2020, 21(S19), 575.
[http://dx.doi.org/10.1186/s12859-020-03891-x] [PMID: 33349234]
[15]
Kwan, T.O.C.; Reis, R.; Siligardi, G.; Hussain, R.; Cheruvara, H.; Moraes, I. Selection of biophysical methods for characterisation of membrane proteins. Int. J. Mol. Sci., 2019, 20(10), 2605.
[http://dx.doi.org/10.3390/ijms20102605] [PMID: 31137900]
[16]
Waugh, D.S. Crystal structures of MBP fusion proteins. Protein Sci., 2016, 25(3), 559-571.
[http://dx.doi.org/10.1002/pro.2863] [PMID: 26682969]
[17]
Panavas, T.; Sanders, C.; Butt, T.R. SUMO fusion technology for enhanced protein production in prokaryotic and eukaryotic expression systems. Methods Mol. Biol., 2009, 497, 303-317.
[http://dx.doi.org/10.1007/978-1-59745-566-4_20]
[18]
Rosenbaum, D.M.; Cherezov, V.; Hanson, M.A.; Rasmussen, S.G.F.; Thian, F.S.; Kobilka, T.S.; Choi, H.J.; Yao, X.J.; Weis, W.I.; Stevens, R.C.; Kobilka, B.K. GPCR engineering yields high-resolution structural insights into β2-adrenergic receptor function. Science, 2007, 318(5854), 1266-1273.
[http://dx.doi.org/10.1126/science.1150609] [PMID: 17962519]
[19]
Liu, S.; Li, W. Protein fusion strategies for membrane protein stabilization and crystal structure determination. Crystals, 2022, 12(8), 1041.
[http://dx.doi.org/10.3390/cryst12081041]
[20]
Singer, S.J. The fluid mosaic model of the structure of cell membranes. Science, 1972, 175, 720-731.
[http://dx.doi.org/10.1126/science.175.4023.720] [PMID: 4333397]
[21]
Cantor, R.S. The influence of membrane lateral pressures on simple geometric models of protein conformational equilibria. Chem. Phys. Lipids, 1999, 101(1), 45-56.
[http://dx.doi.org/10.1016/S0009-3084(99)00054-7] [PMID: 10810924]
[22]
Palsdottir, H.; Hunte, C. Lipids in membrane protein structures. Biochim. Biophys. Acta Biomembr., 2004, 1666(1-2), 2-18.
[http://dx.doi.org/10.1016/j.bbamem.2004.06.012]
[23]
Lee, A.G. Biological membranes: The importance of molecular detail. Trends Biochem. Sci., 2011, 36(9), 493-500.
[http://dx.doi.org/10.1016/j.tibs.2011.06.007] [PMID: 21855348]
[24]
Sanders, C.R.; Mittendorf, K.F. Tolerance to changes in membrane lipid composition as a selected trait of membrane proteins. Biochemistry, 2011, 50(37), 7858-7867.
[http://dx.doi.org/10.1021/bi2011527] [PMID: 21848311]
[25]
Contreras, F.X.; Ernst, A.M.; Wieland, F.; Brügger, B. Specificity of intramembrane protein-lipid interactions. Cold Spring Harb. Perspect. Biol., 2011, 3(6)a004705
[http://dx.doi.org/10.1101/cshperspect.a004705] [PMID: 21536707]
[26]
Whitelegge, J.P. Integral membrane proteins and bilayer proteomics. Anal. Chem., 2013, 85(5), 2558-2568.
[http://dx.doi.org/10.1021/ac303064a] [PMID: 23301778]
[27]
Long, S.B.; Tao, X.; Campbell, E.B.; MacKinnon, R. Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature, 2007, 450(7168), 376-382.
[http://dx.doi.org/10.1038/nature06265] [PMID: 18004376]
[28]
James, E. Native mass spectrometry of membrane proteins. Anal. Chem., 2020, 93(1), 583-597.
[29]
Laganowsky, A.; Reading, E.; Allison, T.M.; Ulmschneider, M.B.; Degiacomi, M.T.; Baldwin, A.J.; Robinson, C.V. Membrane proteins bind lipids selectively to modulate their structure and function. Nature, 2014, 510(7503), 172-175.
[http://dx.doi.org/10.1038/nature13419] [PMID: 24899312]
[30]
Pliotas, C. MS8 Membranes and membrane interacting proteins; , 2016. Available from https://journals.iucr.org/a/issues/2016/a1/00/a54054/a54054.pdf
[31]
Martfeld, A.N.; Rajagopalan, V.; Greathouse, D.V.; Koeppe, R.E., II Dynamic regulation of lipid-protein interactions. Biochim. Biophys. Acta Biomembr., 2015, 1848(9), 1849-1859.
[http://dx.doi.org/10.1016/j.bbamem.2015.01.019]
[32]
Hsia, C.Y.; Richards, M.J.; Daniel, S. A review of traditional and emerging methods to characterize lipid–protein interactions in biological membranes. Anal. Methods, 2015, 7(17), 7076-7094.
[http://dx.doi.org/10.1039/C5AY00599J]
[33]
Kaipa, J.M.; Krasnoselska, G.; Owens, R.J.; van den Heuvel, J. Screening of membrane protein production by comparison of transient expression in insect and mammalian cells. Biomolecules, 2023, 13(5), 817.
[http://dx.doi.org/10.3390/biom13050817] [PMID: 37238687]
[34]
Ilgü, H.; Jeckelmann, J.M.; Gachet, M.S.; Boggavarapu, R.; Ucurum, Z.; Gertsch, J.; Fotiadis, D. Variation of the detergent-binding capacity and phospholipid content of membrane proteins when purified in different detergents. Biophys. J., 2014, 106(8), 1660-1670.
[http://dx.doi.org/10.1016/j.bpj.2014.02.024] [PMID: 24739165]
[35]
Sanders, C.R., II; Schwonek, J.P. Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid-state NMR. Biochemistry, 1992, 31(37), 8898-8905.
[http://dx.doi.org/10.1021/bi00152a029] [PMID: 1390677]
[36]
van Geest, M.; Lolkema, J.S. Membrane topology and insertion of membrane proteins: Search for topogenic signals. Microbiol. Mol. Biol. Rev., 2000, 64(1), 13-33.
[http://dx.doi.org/10.1128/MMBR.64.1.13-33.2000] [PMID: 10704472]
[37]
Reiche, J.; Huber, O. Post-translational modifications of tight junction transmembrane proteins and their direct effect on barrier function. Biochim. Biophys. Acta Biomembr., 2020, 1862(9)183330
[http://dx.doi.org/10.1016/j.bbamem.2020.183330] [PMID: 32376223]
[38]
Laage, R.; Langosch, D. Strategies for prokaryotic expression of eukaryotic membrane proteins. Traffic, 2001, 2(2), 99-104.
[http://dx.doi.org/10.1034/j.1600-0854.2001.020204.x] [PMID: 11247308]
[39]
Walski, T. Diversity and functions of protein glycosylation in insects. Insect Biochem. Mol. Biol., 2017, 83, 21-34.
[http://dx.doi.org/10.1016/j.ibmb.2017.02.005]
[40]
Cummins, P.M. Occludin: One protein, many forms. Mol. Cell. Biol., 2012, 32(2), 242-250.
[http://dx.doi.org/10.1128/MCB.06029-11] [PMID: 22083955]
[41]
Dörfel, M.J.; Huber, O. Modulation of tight junction structure and function by kinases and phosphatases targeting occludin. J. Biomed. Biotechnol., 2012, 2012, 1-14.
[http://dx.doi.org/10.1155/2012/807356] [PMID: 22315516]
[42]
Ikenouchi, K.S.A.J. Regulation of the epithelial barrier by post-translational modifications of tight junction membrane proteins. J. Biochem., 2017, 163(4), 265-272.
[43]
Stamatovic, S.M.; Johnson, A.M.; Keep, R.F.; Andjelkovic, A.V. Junctional proteins of the blood-brain barrier: New insights into function and dysfunction. Tissue Barriers, 2016, 4(1), e1154641-e1154641.
[http://dx.doi.org/10.1080/21688370.2016.1154641] [PMID: 27141427]
[44]
Van Itallie, C.M.; Anderson, J.M. Phosphorylation of tight junction transmembrane proteins: Many sites, much to do. Tissue Barriers, 2018, 6(1)e1382671
[http://dx.doi.org/10.1080/21688370.2017.1382671] [PMID: 29083946]
[45]
Dörfel, M.J.; Huber, O. A phosphorylation hotspot within the occludin C-terminal domain. Ann. N. Y. Acad. Sci., 2012, 1257(1), 38-44.
[http://dx.doi.org/10.1111/j.1749-6632.2012.06536.x] [PMID: 22671587]
[46]
Urner, L.H.; Junge, F.; Fiorentino, F.; El-Baba, T.J.; Shutin, D.; Nölte, G.; Haag, R.; Robinson, C.V. Rationalizing the optimization of detergents for membrane protein purification. Chemistry, 2023, 29(30)e202300159
[http://dx.doi.org/10.1002/chem.202300159] [PMID: 36897295]
[47]
Jensen, M.Ø.; Mouritsen, O.G. Lipids do influence protein function-the hydrophobic matching hypothesis revisited. Biochim. Biophys. Acta Biomembr., 2004, 1666(1-2), 205-226.
[http://dx.doi.org/10.1016/j.bbamem.2004.06.009] [PMID: 15519316]
[48]
Gromiha, M.M.; Ou, Y.Y. Bioinformatics approaches for functional annotation of membrane proteins. Brief. Bioinform., 2014, 15(2), 155-168.
[http://dx.doi.org/10.1093/bib/bbt015] [PMID: 23524979]
[49]
Reid, D.J.; Thibert, S.; Zhou, M. Dissecting the structural heterogeneity of proteins by native mass spectrometry. Protein Sci., 2023, 32(4)e4612
[http://dx.doi.org/10.1002/pro.4612] [PMID: 36851867]
[50]
Mateus, A.; Määttä, T.A.; Savitski, M.M. Thermal proteome profiling: Unbiased assessment of protein state through heat-induced stability changes. Proteome Sci., 2016, 15(1), 13.
[http://dx.doi.org/10.1186/s12953-017-0122-4] [PMID: 28652855]
[51]
Chavez, J.D.; Wippel, H.H.; Tang, X.; Keller, A.; Bruce, J.E. In-cell labeling and mass spectrometry for systems-level structural biology. Chem. Rev., 2022, 122(8), 7647-7689.
[http://dx.doi.org/10.1021/acs.chemrev.1c00223] [PMID: 34232610]
[52]
James, E.I.; Murphree, T.A.; Vorauer, C.; Engen, J.R.; Guttman, M. Advances in hydrogen/deuterium exchange mass spectrometry and the pursuit of challenging biological systems. Chem. Rev., 2022, 122(8), 7562-7623.
[http://dx.doi.org/10.1021/acs.chemrev.1c00279] [PMID: 34493042]
[53]
McKenzie-Coe, A.; Montes, N.S.; Jones, L.M. Hydroxyl radical protein footprinting: A mass spectrometry-based structural method for studying the higher order structure of proteins. Chem. Rev., 2022, 122(8), 7532-7561.
[http://dx.doi.org/10.1021/acs.chemrev.1c00432] [PMID: 34633178]
[54]
Petrotchenko, E.V.; Borchers, C.H. Protein chemistry combined with mass spectrometry for protein structure determination. Chem. Rev., 2022, 122(8), 7488-7499.
[http://dx.doi.org/10.1021/acs.chemrev.1c00302] [PMID: 34968047]
[55]
Piersimoni, L.; Kastritis, P.L.; Arlt, C.; Sinz, A. Cross-linking mass spectrometry for investigating protein conformations and protein–protein interactions-A method for all seasons. Chem. Rev., 2022, 122(8), 7500-7531.
[http://dx.doi.org/10.1021/acs.chemrev.1c00786] [PMID: 34797068]
[56]
Schopper, S.; Kahraman, A.; Leuenberger, P.; Feng, Y.; Piazza, I.; Müller, O.; Boersema, P.J.; Picotti, P. Measuring protein structural changes on a proteome-wide scale using limited proteolysis-coupled mass spectrometry. Nat. Protoc., 2017, 12(11), 2391-2410.
[http://dx.doi.org/10.1038/nprot.2017.100] [PMID: 29072706]
[57]
Wheat, A.; Yu, C.; Wang, X.; Burke, A.M.; Chemmama, I.E.; Kaake, R.M.; Baker, P.; Rychnovsky, S.D.; Yang, J.; Huang, L. Protein interaction landscapes revealed by advanced in vivo cross-linking–mass spectrometry. Proc. Natl. Acad. Sci., 2021, 118(32)e2023360118
[http://dx.doi.org/10.1073/pnas.2023360118] [PMID: 34349018]
[58]
Yao, D.; Zhang, K.; Wu, J. Available strategies for improved expression of recombinant proteins in Brevibacillus expression system: A review. Crit. Rev. Biotechnol., 2020, 40(7), 1044-1058.
[http://dx.doi.org/10.1080/07388551.2020.1805404] [PMID: 32781847]
[59]
Satomura, T.; Emoto, S.; Kurosawa, N.; Ohshima, T.; Sakuraba, H.; Suye, S. Characterization of dye-linked d-amino acid dehydrogenase from Sulfurisphaera tokodaii expressed using an archaeal recombinant protein expression system. J. Biosci. Bioeng., 2020, 130(3), 247-252.
[http://dx.doi.org/10.1016/j.jbiosc.2020.04.008] [PMID: 32451245]
[60]
Hadiji-Abbes, N.; Borchani-Chabchoub, I.; Triki, H.; Ellouz, R.; Gargouri, A.; Mokdad-Gargouri, R. Expression of HBsAg and preS2-S protein in different yeast based system: A comparative analysis. Protein Expr. Purif., 2009, 66(2), 131-137.
[http://dx.doi.org/10.1016/j.pep.2009.03.006] [PMID: 19303931]
[61]
Bannach, C.; Buck, D.R.; Bobby, G.; Graves, L.P.; Li, S.; Chambers, A.C.; Gan, E.; Arinto-Garcia, R.; Possee, R.D.; King, L.A. Optimizing recombinant baculovirus vector design for protein production in insect cells. Processes, 2021, 9(12), 2118.
[http://dx.doi.org/10.3390/pr9122118]
[62]
Escandell, J.; Moura, F.; Carvalho, S.B.; Silva, R.J.S.; Correia, R.; Roldão, A.; Gomes-Alves, P.; Alves, P.M. Towards a scalable bioprocess for rAAV production using a HeLa stable cell line. Biotechnol. Bioeng., 2023, 120(9), 2578-2587.
[http://dx.doi.org/10.1002/bit.28394] [PMID: 37027346]
[63]
Wang, C.H.; Naik, N.G.; Liao, L.L.; Wei, S.C.; Chao, Y.C. Global screening of antiviral genes that suppress baculovirus transgene expression in mammalian cells. Mol. Ther. Methods Clin. Dev., 2017, 6, 194-206.
[http://dx.doi.org/10.1016/j.omtm.2017.07.002] [PMID: 28831401]
[64]
Rosano, G.L.; Ceccarelli, E.A. Recombinant protein expression in Escherichia coli: Advances and challenges. Front. Microbiol., 2014, 5, 172.
[http://dx.doi.org/10.3389/fmicb.2014.00172] [PMID: 24860555]
[65]
Schlegel, S. Bacterial-based membrane protein production. Biochimica et Biophysica Acta (BBA). Mol. Cell Res., 2014, 1843(8), 1739-1749.
[66]
Zakład Biochemii, W.B.I.O.; Zakład Inżynierii Tkankowej, C.M.I.L.; Zakład Biochemii, W.B.I.O. Zakład Biochemii. Prokariotyczne systemy ekspresyjne., 2013, 119.
[67]
Baneyx, F.; Mujacic, M. Recombinant protein folding and misfolding in Escherichia coli. Nat. Biotechnol., 2004, 22(11), 1399-1408.
[http://dx.doi.org/10.1038/nbt1029] [PMID: 15529165]
[68]
Abarghooi Kahaki, F.; Monzavi, S.; Bamehr, H.; Bandani, E.; Payandeh, Z.; Jahangiri, A.; Khalili, S. Expression and purification of membrane proteins in different hosts. Int. J. Pept. Res. Ther., 2020, 26(4), 2077-2087.
[http://dx.doi.org/10.1007/s10989-019-10009-2]
[69]
Kesidis, A.; Depping, P.; Lodé, A.; Vaitsopoulou, A.; Bill, R.M.; Goddard, A.D.; Rothnie, A.J. Expression of eukaryotic membrane proteins in eukaryotic and prokaryotic hosts. Methods, 2020, 180, 3-18.
[http://dx.doi.org/10.1016/j.ymeth.2020.06.006] [PMID: 32534131]
[70]
Rebba, C. ntegral membrane protein expression in Saccharomyces cerevisiae. Methods Mol. Biol., 2016, 1432, 163-186.
[71]
Wang, X.; van Westen, G.J.P.; Heitman, L.H.; IJzerman, A.P. G protein-coupled receptors expressed and studied in yeast. The adenosine receptor as a prime example. Biochem. Pharmacol., 2021, 187114370
[http://dx.doi.org/10.1016/j.bcp.2020.114370] [PMID: 33338473]
[72]
Furukawa, H.; Simorowski, N.; Michalski, K. Chapter One - Effective production of oligomeric membrane proteins by EarlyBac-insect cell system. In: Methods in Enzymology; Minor, D.L.; Colecraft, D.L., Eds.; Academic Press, 2021; pp. 3-19.
[73]
Joshi, P.R.H.; Venereo-Sanchez, A.; Chahal, P.S.; Kamen, A.A. Advancements in molecular design and bioprocessing of recombinant adeno‐associated virus gene delivery vectors using the insect‐cell baculovirus expression platform. Biotechnol. J., 2021, 16(4)2000021
[http://dx.doi.org/10.1002/biot.202000021] [PMID: 33277815]
[74]
Zhu, J. Mammalian cell protein expression for biopharmaceutical production. Biotechnol. Adv., 2012, 30(5), 1158-1170.
[http://dx.doi.org/10.1016/j.biotechadv.2011.08.022] [PMID: 21968146]
[75]
Guo, X.; Wang, C.; Wang, T.Y. Chromatin-modifying elements for recombinant protein production in mammalian cell systems. Crit. Rev. Biotechnol., 2020, 40(7), 1035-1043.
[http://dx.doi.org/10.1080/07388551.2020.1805401] [PMID: 32777953]
[76]
Mancia, F.; Patel, S.D.; Rajala, M.W.; Scherer, P.E.; Nemes, A.; Schieren, I.; Hendrickson, W.A.; Shapiro, L. Optimization of protein production in mammalian cells with a coexpressed fluorescent marker. Structure, 2004, 12(8), 1355-1360.
[http://dx.doi.org/10.1016/j.str.2004.06.012] [PMID: 15296729]
[77]
El-Baky, N.A. EL-Fakharany, E.M.; Sabry, S.A.; El-Helow, E.R.; Redwan, E.M.; Sabry, A. A de novo optimized cell-free system for the expression of soluble and active human tumor necrosis factor-alpha. Biology, 2022, 11(2), 157.
[http://dx.doi.org/10.3390/biology11020157] [PMID: 35205024]
[78]
Endo, Y. Development of a cell-free protein synthesis system for practical use. Proc. Jpn. Acad., Ser. B, Phys. Biol. Sci., 2021, 97(5), 261-276.
[http://dx.doi.org/10.2183/pjab.97.015] [PMID: 33980755]
[79]
Focke, P.J.; Hein, C.; Hoffmann, B.; Matulef, K.; Bernhard, F.; Dötsch, V.; Valiyaveetil, F.I. Combining in vitro folding with cell free protein synthesis for membrane protein expression. Biochemistry, 2016, 55(30), 4212-4219.
[http://dx.doi.org/10.1021/acs.biochem.6b00488] [PMID: 27384110]
[80]
Kosobokova, E.N.; Skrypnik, K.A.; Kosorukov, V.S. Overview of fusion tags for recombinant proteins. Biochemistry, 2016, 81(3), 187-200.
[http://dx.doi.org/10.1134/S0006297916030019] [PMID: 27262188]
[81]
Nallamsetty, S.; Waugh, D.S. A generic protocol for the expression and purification of recombinant proteins in Escherichia coli using a combinatorial His6-maltose binding protein fusion tag. Nat. Protoc., 2007, 2(2), 383-391.
[http://dx.doi.org/10.1038/nprot.2007.50] [PMID: 17406599]
[82]
Butt, T.R.; Suzanne, C.E.J.P. Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID- 19. The COVID-19 resource centre is hosted on Elsevier Connect, the company’s public news and information website; , 2005. Available from https://ir.ymlib.yonsei.ac.kr/bitstream/22282913/179464/1/T202002283.pdf
[83]
Balchin, D.; Hayer-Hartl, M.; Hartl, F.U. In vivo aspects of protein folding and quality control. Science, 2016, 353(6294)aac4354
[http://dx.doi.org/10.1126/science.aac4354] [PMID: 27365453]
[84]
Klaus Richter, M.H.A.J. 2010.
[85]
Taguchi, H.; Koike-Takeshita, A. In vivo client proteins of the chaperonin GroEL-GroES provide insight into the role of chaperones in protein evolution. Front. Mol. Biosci., 2023, 101091677
[http://dx.doi.org/10.3389/fmolb.2023.1091677] [PMID: 36845542]
[86]
Sadaf, A.; Kim, S.; Bae, H.E.; Wang, H.; Nygaard, A.; Uegaki, Y.; Du, Y.; Munk, C.F.; Katsube, S.; Sung Lee, H.; Bae, J.; Choi, C.W.; Choi, H.J.; Byrne, B.; Gellman, S.H.; Guan, L.; Loland, C.J.; Kobilka, B.K. Im, W.; Chae, P.S. Conformationally flexible core-bearing detergents with a hydrophobic or hydrophilic pendant: Effect of pendant polarity on detergent conformation and membrane protein stability. Acta Biomater., 2021, 128, 393-407.
[http://dx.doi.org/10.1016/j.actbio.2021.04.043] [PMID: 33933694]
[87]
Birch, J.; Axford, D.; Foadi, J.; Meyer, A.; Eckhardt, A.; Thielmann, Y.; Moraes, I. The fine art of integral membrane protein crystallisation. Methods, 2018, 147, 150-162.
[http://dx.doi.org/10.1016/j.ymeth.2018.05.014] [PMID: 29778646]
[88]
Drew, D.; Lerch, M.; Kunji, E.; Slotboom, D.J.; de Gier, J.W. Optimization of membrane protein overexpression and purification using GFP fusions. Nat. Methods, 2006, 3(4), 303-313.
[http://dx.doi.org/10.1038/nmeth0406-303] [PMID: 16554836]
[89]
Kawate, T.; Gouaux, E. Fluorescence-detection size-exclusion chromatography for precrystallization screening of integral membrane proteins. Structure, 2006, 14(4), 673-681.
[http://dx.doi.org/10.1016/j.str.2006.01.013] [PMID: 16615909]
[90]
Stetsenko, A.; Guskov, A. An overview of the top ten detergents used for membrane protein crystallization. Crystals, 2017, 7(7), 197.
[http://dx.doi.org/10.3390/cryst7070197]
[91]
Thoma, J.; Burmann, B.M. Fake it ‘Till you make it—the pursuit of suitable membrane mimetics for membrane protein biophysics. Int. J. Mol. Sci., 2020, 22(1), 50.
[http://dx.doi.org/10.3390/ijms22010050] [PMID: 33374526]
[92]
Prince, C.C.; Jia, Z. Detergent quantification in membrane protein samples and its application to crystallization experiments. Amino Acids, 2013, 45(6), 1293-1302.
[http://dx.doi.org/10.1007/s00726-013-1600-3] [PMID: 24105076]
[93]
Chen, W.; Cai, Y.; Fu, Q.; Chen, B.; Guo, J.; Chou, J.J. Unidirectional presentation of membrane proteins in nanoparticle‐supported liposomes. Angew. Chem. Int. Ed., 2019, 58(29), 9866-9870.
[http://dx.doi.org/10.1002/anie.201903093] [PMID: 30990942]
[94]
Schneiter, R.; Toulmay, A. The role of lipids in the biogenesis of integral membrane proteins. Appl. Microbiol. Biotechnol., 2007, 73(6), 1224-1232.
[http://dx.doi.org/10.1007/s00253-006-0707-9] [PMID: 17111137]
[95]
So, K.K.; Le, N.M.T.; Nguyen, N.L.; Kim, D.H. Improving expression and assembly of difficult-to-express heterologous proteins in Saccharomyces cerevisiae by culturing at a sub-physiological temperature. Microb. Cell Fact., 2023, 22(1), 55.
[http://dx.doi.org/10.1186/s12934-023-02065-7] [PMID: 36959657]
[96]
Kang, M-K.
[97]
Avery, A. Effect of osmolytes on proteins. Biophysical J.,, 2010, 98(3, sup 1), 447A.
[http://dx.doi.org/10.1016/j.bpj.2009.12.2429]
[98]
Wagner, S.; Bader, M.L.; Drew, D.; de Gier, J.W. Rationalizing membrane protein overexpression. Trends Biotechnol., 2006, 24(8), 364-371.
[http://dx.doi.org/10.1016/j.tibtech.2006.06.008] [PMID: 16820235]
[99]
Tate, C.G. Overexpression of mammalian integral membrane proteins for structural studies. FEBS Lett., 2001, 504(3), 94-98.
[http://dx.doi.org/10.1016/S0014-5793(01)02711-9] [PMID: 11532439]
[100]
Miroux, B.; Walker, J.E. 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., 1996, 260(3), 289-298.
[http://dx.doi.org/10.1006/jmbi.1996.0399] [PMID: 8757792]
[101]
Edmund, R.S. Eukaryotic membrane protein overproduction in Lactococcus lactis. Curr. Opin. Biotechnol., 2005, 16(5), 546-551.
[102]
von Heijne, G. Membrane-protein topology. Nat. Rev. Mol. Cell Biol., 2006, 7(12), 909-918.
[http://dx.doi.org/10.1038/nrm2063] [PMID: 17139331]
[103]
Redden, H.; Morse, N.; Alper, H.S. The synthetic biology toolbox for tuning gene expression in yeast. FEMS Yeast Res., 2014, 15(1), 1-10.
[http://dx.doi.org/10.1111/1567-1364.12188]
[104]
Mishra, A.; Siwach, P.; Misra, P.; Jayaram, B.; Bansal, M.; Olson, W.K.; Thayer, K.M.; Beveridge, D.L. Toward a universal structural and energetic model for prokaryotic promoters. Biophys. J., 2018, 115(7), 1180-1189.
[http://dx.doi.org/10.1016/j.bpj.2018.08.002] [PMID: 30172386]
[105]
Browning, D.F.; Busby, S.J.W. Local and global regulation of transcription initiation in bacteria. Nat. Rev. Microbiol., 2016, 14(10), 638-650.
[http://dx.doi.org/10.1038/nrmicro.2016.103] [PMID: 27498839]
[106]
Kanhere, A.; Bansal, M. Structural properties of promoters: Similarities and differences between prokaryotes and eukaryotes. Nucleic Acids Res., 2005, 33(10), 3165-3175.
[http://dx.doi.org/10.1093/nar/gki627] [PMID: 15939933]
[107]
Wilkinson, G.W.G.; Akrigg, A. Constitutive and enhanced expression from the CMV major IE promoter in a defective adenovirus vector. Nucleic Acids Res., 1992, 20(9), 2233-2239.
[http://dx.doi.org/10.1093/nar/20.9.2233] [PMID: 1317548]
[108]
Davey, J.A.; Wilson, C.J. Engineered signal-coupled inducible promoters: Measuring the apparent RNA-polymerase resource budget. Nucleic Acids Res., 2020, 48(17), 9995-10012.
[http://dx.doi.org/10.1093/nar/gkaa734] [PMID: 32890400]
[109]
Iyer, S.; Karig, D.K.; Norred, S.E.; Simpson, M.L.; Doktycz, M.J. Multi-input regulation and logic with T7 promoters in cells and cell-free systems. PLoS One, 2013, 8(10)e78442
[http://dx.doi.org/10.1371/journal.pone.0078442] [PMID: 24194933]
[110]
Shinoda, T.; Shinya, N.; Ito, K.; Ishizuka-Katsura, Y.; Ohsawa, N.; Terada, T.; Hirata, K.; Kawano, Y.; Yamamoto, M.; Tomita, T.; Ishibashi, Y.; Hirabayashi, Y.; Kimura-Someya, T.; Shirouzu, M.; Yokoyama, S. Cell-free methods to produce structurally intact mammalian membrane proteins. Sci. Rep., 2016, 6(1), 30442.
[http://dx.doi.org/10.1038/srep30442] [PMID: 27465719]
[111]
Wuu, J.J.; Swartz, J.R. High yield cell-free production of integral membrane proteins without refolding or detergents. Biochim. Biophys. Acta Biomembr., 2008, 1778(5), 1237-1250.
[http://dx.doi.org/10.1016/j.bbamem.2008.01.023] [PMID: 18295592]
[112]
Harrison, P.J.; Vecerkova, T.; Clare, D.K.; Quigley, A. A review of the approaches used to solve sub-100 kDa membrane proteins by cryo-electron microscopy. J. Struct. Biol., 2023, 215(2)107959
[http://dx.doi.org/10.1016/j.jsb.2023.107959] [PMID: 37004781]
[113]
Denisov, I.G.; Sligar, S.G. Nanodiscs for structural and functional studies of membrane proteins. Nat. Struct. Mol. Biol., 2016, 23(6), 481-486.
[http://dx.doi.org/10.1038/nsmb.3195] [PMID: 27273631]
[114]
Jessica, S. ScienceDirect. Clin. Microbiol. Newsl., 2015, 37(4), 33.
[http://dx.doi.org/10.1016/j.clinmicnews.2015.01.008]

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