Login Register Cart 0
Generic placeholder image

Current Proteomics

Editor-in-Chief

ISSN (Print): 1570-1646
ISSN (Online): 1875-6247

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Mini-Review Article

The Study of Different Signal Peptides in Improvement of Recombinant Proteins Solubility in E. coli: A Mini-Review Article

In Press, (this is not the final "Version of Record"). Available online 06 August, 2024
Author(s): Seyyed Soheil Rahmatabadi, Soudabeh Askari, Fatemeh Khademi and Bijan Soleymani*
Published on: 06 August, 2024

DOI: 10.2174/0115701646305738240730113619

Price: $95

Abstract

In E. coli, the production of proteins as inclusion bodies (IBs) caused a decrease in the solubility and activity of these products. Diverse approaches and methods have been used by investigators to overcome this problem. The secretion of recombinant proteins into the periplasmic space by means of suitable signal peptides is a way to resolve these limitations for the production of recombinant proteins in a native form. Secretory production of recombinant proteins in bacterial hosts has many advantages and thus, it is a topic of interest. However, it is hard to achieve due to the difficulty of the process and the need for the choice of appropriate signal peptide for each host and protein. Based on the literature, different signal peptides have experimentally been applied to enhance the solubility of various recombinant proteins. It has been shown that the secretion efficiency of a given protein differs dramatically based on the type of the signal peptide that is attached to the protein. Therefore, the choice and alteration of signal peptides are the two crucial approaches for the improvement of a recombinant protein secretion that have been discussed in this review. Also, different factors affecting the expression and solubility of recombinant proteins have been discussed.

[1]
Yin, J.; Li, G.; Ren, X.; Herrler, G. Select what you need: A comparative evaluation of the advantages and limitations of frequently used expression systems for foreign genes. J. Biotechnol., 2007, 127(3), 335-347.
[http://dx.doi.org/10.1016/j.jbiotec.2006.07.012] [PMID: 16959350]
[2]
Mergulhão, F.J.M.; Summers, D.K.; Monteiro, G.A. Recombinant protein secretion in Escherichia coli. Biotechnol. Adv., 2005, 23(3), 177-202.
[http://dx.doi.org/10.1016/j.biotechadv.2004.11.003] [PMID: 15763404]
[3]
Zhang, W.; Lu, J.; Zhang, S.; Liu, L.; Pang, X.; Lv, J. Development an effective system to expression recombinant protein in E. coli via comparison and optimization of signal peptides: Expression of Pseudomonas fluorescens BJ-10 thermostable lipase as case study. Microb. Cell Fact., 2018, 17(1), 50.
[http://dx.doi.org/10.1186/s12934-018-0894-y] [PMID: 29592803]
[4]
Shokri, A.; Sandén, A.; Larsson, G. Cell and process design for targeting of recombinant protein into the culture medium of Escherichia coli. Appl. Microbiol. Biotechnol., 2003, 60(6), 654-664.
[http://dx.doi.org/10.1007/s00253-002-1156-8] [PMID: 12664143]
[5]
Hoffmann, F.; Heuvel, J.; Zidek, N.; Rinas, U. Minimizing inclusion body formation during recombinant protein production in Escherichia coli at bench and pilot plant scale. Enzyme Microb. Technol., 2004, 34(3-4), 235-241.
[http://dx.doi.org/10.1016/j.enzmictec.2003.10.011]
[6]
Boock, J.T.; Waraho-Zhmayev, D.; Mizrachi, D.; DeLisa, M.P. Beyond the cytoplasm of Escherichia coli: Localizing recombinant proteins where you want them. Insoluble Proteins; SpringerLink: Berlin, Heidelberg, 2015, pp. 79-97.
[7]
Natale, P.; Brüser, T.; Driessen, A.J. Sec-and Tat-mediated protein secretion across the bacterial cytoplasmic membrane-distinct translocases and mechanisms. Biochimica et Biophysica Acta (BBA)-. Biomembranes, 2008, 1778(9), 1735-1756.
[http://dx.doi.org/10.1016/j.bbamem.2007.07.015] [PMID: 17935691]
[8]
Negahdaripour, M.; Nezafat, N.; Hajighahramani, N.; Soheil Rahmatabadi, S.; Hossein Morowvat, M.; Ghasemi, Y. In silico study of different signal peptides for secretory production of interleukin-11 in Escherichia coli. Curr. Proteomics, 2017, 14(2), 112-121.
[http://dx.doi.org/10.2174/1570164614666170106110848]
[9]
Pohl, S.; Harwood, C.R. Heterologous protein secretion by bacillus species from the cradle to the grave. Adv. Appl. Microbiol., 2010, 73, 1-25.
[http://dx.doi.org/10.1016/S0065-2164(10)73001-X] [PMID: 20800757]
[10]
Li, W.; Zhou, X.; Lu, P. Bottlenecks in the expression and secretion of heterologous proteins in Bacillus subtilis. Res. Microbiol., 2004, 155(8), 605-610.
[http://dx.doi.org/10.1016/j.resmic.2004.05.002] [PMID: 15380546]
[11]
Tsirigotaki, A.; De Geyter, J.; Šoštaric´, N.; Economou, A.; Karamanou, S. Protein export through the bacterial Sec pathway. Nat. Rev. Microbiol., 2017, 15(1), 21-36.
[http://dx.doi.org/10.1038/nrmicro.2016.161] [PMID: 27890920]
[12]
Rusch, S.L.; Kendall, D.A. Interactions that drive Sec-dependent bacterial protein transport. Biochemistry, 2007, 46(34), 9665-9673.
[http://dx.doi.org/10.1021/bi7010064] [PMID: 17676771]
[13]
Denks, K.; Vogt, A.; Sachelaru, I.; Petriman, N.A.; Kudva, R.; Koch, H.G. The Sec translocon mediated protein transport in prokaryotes and eukaryotes. Mol. Membr. Biol., 2014, 31(2-3), 58-84.
[http://dx.doi.org/10.3109/09687688.2014.907455] [PMID: 24762201]
[14]
Elvekrog, M.M.; Walter, P. Dynamics of co-translational protein targeting. Curr. Opin. Chem. Biol., 2015, 29, 79-86.
[http://dx.doi.org/10.1016/j.cbpa.2015.09.016] [PMID: 26517565]
[15]
Kusukawa, N.; Yura, T.; Ueguchi, C.; Akiyama, Y.; Ito, K. Effects of mutations in heat-shock genes groES and groEL on protein export in Escherichia coli. EMBO J., 1989, 8(11), 3517-3521.
[http://dx.doi.org/10.1002/j.1460-2075.1989.tb08517.x] [PMID: 2573517]
[16]
Bechtluft, P.; Nouwen, N.; Tans, S.J.; Driessen, A.J.M. SecB—A chaperone dedicated to protein translocation. Mol. Biosyst., 2010, 6(4), 620-627.
[http://dx.doi.org/10.1039/B915435C] [PMID: 20237639]
[17]
Herbort, M.; Klein, M.; Manting, E.H.; Driessen, A.J.M.; Freudl, R. Temporal expression of the Bacillus subtilis secA gene, encoding a central component of the preprotein translocase. J. Bacteriol., 1999, 181(2), 493-500.
[http://dx.doi.org/10.1128/JB.181.2.493-500.1999] [PMID: 9882663]
[18]
Wild, J.; Altman, E.; Yura, T.; Gross, C.A. DnaK and DnaJ heat shock proteins participate in protein export in Escherichia coli. Genes Dev., 1992, 6(7), 1165-1172.
[http://dx.doi.org/10.1101/gad.6.7.1165] [PMID: 1628824]
[19]
Lycklama a Nijeholt, J.A.; Driessen, A.J.M. The bacterial Sec-translocase: Structure and mechanism. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2012, 367(1592), 1016-1028.
[http://dx.doi.org/10.1098/rstb.2011.0201] [PMID: 22411975]
[20]
Tsukazaki, T.; Mori, H.; Echizen, Y.; Ishitani, R.; Fukai, S.; Tanaka, T.; Perederina, A.; Vassylyev, D.G.; Kohno, T.; Maturana, A.D.; Ito, K.; Nureki, O. Structure and function of a membrane component SecDF that enhances protein export. Nature, 2011, 474(7350), 235-238.
[http://dx.doi.org/10.1038/nature09980] [PMID: 21562494]
[21]
Dalbey, R.E.; Wang, P.; van Dijl, J.M. Membrane proteases in the bacterial protein secretion and quality control pathway. Microbiol. Mol. Biol. Rev., 2012, 76(2), 311-330.
[http://dx.doi.org/10.1128/MMBR.05019-11] [PMID: 22688815]
[22]
Palmer, T.; Berks, B.C. The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol., 2012, 10(7), 483-496.
[http://dx.doi.org/10.1038/nrmicro2814] [PMID: 22683878]
[23]
Sargent, F.; Stanley, N.R.; Berks, B.C.; Palmer, T. Sec-independent protein translocation in Escherichia coli. A distinct and pivotal role for the TatB protein. J. Biol. Chem., 1999, 274(51), 36073-36082.
[http://dx.doi.org/10.1074/jbc.274.51.36073] [PMID: 10593889]
[24]
Alami, M.; Lüke, I.; Deitermann, S.; Eisner, G.; Koch, H.G.; Brunner, J.; Müller, M. Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli. Mol. Cell, 2003, 12(4), 937-946.
[http://dx.doi.org/10.1016/S1097-2765(03)00398-8] [PMID: 14580344]
[25]
Lüke, I.; Handford, J.I.; Palmer, T.; Sargent, F. Proteolytic processing of Escherichia coli twin-arginine signal peptides by LepB. Arch. Microbiol., 2009, 191(12), 919-925.
[http://dx.doi.org/10.1007/s00203-009-0516-5] [PMID: 19809807]
[26]
Futatsumori-Sugai, M.; Tsumoto, K. Signal peptide design for improving recombinant protein secretion in the baculovirus expression vector system. Biochem. Biophys. Res. Commun., 2010, 391(1), 931-935.
[http://dx.doi.org/10.1016/j.bbrc.2009.11.167] [PMID: 19962965]
[27]
Low, K.O.; Muhammad Mahadi, N.; Md Illias, R. Optimisation of signal peptide for recombinant protein secretion in bacterial hosts. Appl. Microbiol. Biotechnol., 2013, 97(9), 3811-3826.
[http://dx.doi.org/10.1007/s00253-013-4831-z] [PMID: 23529680]
[28]
Chou, M.M.; Kendall, D.A. Polymeric sequences reveal a functional interrelationship between hydrophobicity and length of signal peptides. J. Biol. Chem., 1990, 265(5), 2873-2880.
[http://dx.doi.org/10.1016/S0021-9258(19)39882-5] [PMID: 2154463]
[29]
Mori, H.; Araki, M.; Hikita, C.; Tagaya, M.; Mizushima, S. The hydrophobic region of signal peptides is involved in the interaction with membrane-bound SecA. Biochim. Biophys. Acta Biomembr., 1997, 1326(1), 23-36.
[http://dx.doi.org/10.1016/S0005-2736(97)00004-7] [PMID: 9188797]
[30]
Fu, L.; Xu, Z.; Shuai, J.; Hu, C.; Dai, W.; Li, W. High-level secretion of a chimeric thermostable lichenase from Bacillus subtilis by screening of site-mutated signal peptides with structural alterations. Curr. Microbiol., 2008, 56(3), 287-292.
[http://dx.doi.org/10.1007/s00284-007-9077-5] [PMID: 18172721]
[31]
Román, R.; Miret, J.; Scalia, F.; Casablancas, A.; Lecina, M.; Cairó, J.J. Enhancing heterologous protein expression and secretion in HEK293 cells by means of combination of CMV promoter and IFNα2 signal peptide. J. Biotechnol., 2016, 239, 57-60.
[http://dx.doi.org/10.1016/j.jbiotec.2016.10.005] [PMID: 27725209]
[32]
Zhang, L.; Leng, Q.; Mixson, A. J. Alteration in the IL-2 signal peptide affects secretion of proteins in vitro and in vivo. J Gene Med, 2005, 7(3), 354-65.
[33]
Zhou, Y.; Liu, P.; Gan, Y.; Sandoval, W.; Katakam, A.K.; Reichelt, M.; Rangell, L.; Reilly, D. Enhancing full-length antibody production by signal peptide engineering. Microb. Cell Fact., 2016, 15(1), 47.
[http://dx.doi.org/10.1186/s12934-016-0445-3] [PMID: 26935575]
[34]
Hikita, C.; Mizushima, S. The requirement of a positive charge at the amino terminus can be compensated for by a longer central hydrophobic stretch in the functioning of signal peptides. J. Biol. Chem., 1992, 267(17), 12375-12379.
[http://dx.doi.org/10.1016/S0021-9258(19)49850-5] [PMID: 1318317]
[35]
Rusch, S.; Mascolo, C.; Kebir, M.; Kendall, D. Juxtaposition of signal-peptide charge and core region hydrophobicity is critical for functional signal peptides. Arch. Microbiol., 2002, 178(4), 306-310.
[http://dx.doi.org/10.1007/s00203-002-0453-z] [PMID: 12209265]
[36]
Ismail, N.F.; Hamdan, S.; Mahadi, N.M.; Murad, A.M.A.; Rabu, A.; Bakar, F.D.A.; Klappa, P.; Illias, R.M. A mutant l-asparaginase II signal peptide improves the secretion of recombinant cyclodextrin glucanotransferase and the viability of Escherichia coli. Biotechnol. Lett., 2011, 33(5), 999-1005.
[http://dx.doi.org/10.1007/s10529-011-0517-8] [PMID: 21234789]
[37]
Jonet, M.A.; Mahadi, N.M.; Murad, A.M.A.; Rabu, A.; Bakar, F.D.A.; Rahim, R.A.; Low, K.O.; Illias, R.M. Optimization of a heterologous signal peptide by site-directed mutagenesis for improved secretion of recombinant proteins in Escherichia coli. J. Mol. Microbiol. Biotechnol., 2012, 22(1), 48-58.
[PMID: 22456489]
[38]
Inouye, S.; Soberon, X.; Franceschini, T.; Nakamura, K.; Itakura, K.; Inouye, M. Role of positive charge on the amino-terminal region of the signal peptide in protein secretion across the membrane. Proc. Natl. Acad. Sci. USA, 1982, 79(11), 3438-3441.
[http://dx.doi.org/10.1073/pnas.79.11.3438] [PMID: 7048305]
[39]
Takimura, Y.; Kato, M.; Ohta, T.; Yamagata, H.; Udaka, S. Secretion of human interleukin-2 in biologically active form by Bacillus brevis directly into culture medium. Biosci. Biotechnol. Biochem., 1997, 61(11), 1858-1861.
[http://dx.doi.org/10.1271/bbb.61.1858] [PMID: 9404065]
[40]
Wankel, S.D.; Mosier, A.C.; Hansel, C.M.; Paytan, A.; Francis, C.A. Spatial variability in nitrification rates and ammonia-oxidizing microbial communities in the agriculturally impacted Elkhorn Slough estuary, California. Appl. Environ. Microbiol., 2011, 77(1), 269-280.
[http://dx.doi.org/10.1128/AEM.01318-10] [PMID: 21057023]
[41]
Nesmeyanova, M.A.; Karamyshev, A.L.; Karamysheva, Z.N.; Kalinin, A.E.; Ksenzenko, V.N.; Kajava, A.V. Positively charged lysine at the N-terminus of the signal peptide of the Escherichia coli alkaline phosphatase provides the secretion efficiency and is involved in the interaction with anionic phospholipids. FEBS Lett., 1997, 403(2), 203-207.
[http://dx.doi.org/10.1016/S0014-5793(97)00052-5] [PMID: 9042967]
[42]
Guo, X.; Zhang, Y.; Zhang, X.; Wang, S.; Lu, C. Recognition of signal peptide by protein translocation machinery in middle silk gland of silkworm <italic>Bombyx mori</italic>. Acta Biochim. Biophys. Sin. (Shanghai), 2008, 40(1), 38-46.
[http://dx.doi.org/10.1111/j.1745-7270.2008.00376.x] [PMID: 18180852]
[43]
Le Loir, Y.; Gruss, A.; Ehrlich, S.D.; Langella, P. A nine-residue synthetic propeptide enhances secretion efficiency of heterologous proteins in Lactococcus lactis. J. Bacteriol., 1998, 180(7), 1895-1903.
[http://dx.doi.org/10.1128/JB.180.7.1895-1903.1998] [PMID: 9537390]
[44]
Le Loir, Y.; Nouaille, S.; Commissaire, J.; Brétigny, L.; Gruss, A.; Langella, P. Signal peptide and propeptide optimization for heterologous protein secretion in Lactococcus lactis. Appl. Environ. Microbiol., 2001, 67(9), 4119-4127.
[http://dx.doi.org/10.1128/AEM.67.9.4119-4127.2001] [PMID: 11526014]
[45]
Davis, A.; Moore, I.B.; Parker, D.S.; Taniuchi, H. Nuclease B. A possible precursor of nuclease A, an extracellular nuclease of Staphylococcus aureus. J. Biol. Chem., 1977, 252(18), 6544-6553.
[http://dx.doi.org/10.1016/S0021-9258(17)39992-1] [PMID: 893427]
[46]
Hytönen, V.P.; Laitinen, O.H.; Airenne, T.T.; Kidron, H.; Meltola, N.J.; Porkka, E.J.; Hörhä, J.; Paldanius, T.; Määttä, J.A.E.; Nordlund, H.R.; Johnson, M.S.; Salminen, T.A.; Airenne, K.J.; Ylä-Herttuala, S.; Kulomaa, M.S. Efficient production of active chicken avidin using a bacterial signal peptide in Escherichia coli. Biochem. J., 2004, 384(2), 385-390.
[http://dx.doi.org/10.1042/BJ20041114] [PMID: 15324300]
[47]
Costa, S.J.; Almeida, A.; Castro, A.; Domingues, L.; Besir, H. The novel Fh8 and H fusion partners for soluble protein expression in Escherichia coli: A comparison with the traditional gene fusion technology. Appl. Microbiol. Biotechnol., 2013, 97(15), 6779-6791.
[http://dx.doi.org/10.1007/s00253-012-4559-1] [PMID: 23160981]
[48]
Liang, X.; Jia, S.; Sun, Y.; Chen, M.; Chen, X.; Zhong, J.; Huan, L. Secretory expression of nattokinase from Bacillus subtilis YF38 in Escherichia coli. Mol. Biotechnol., 2007, 37(3), 187-194.
[http://dx.doi.org/10.1007/s12033-007-0060-y] [PMID: 17952663]
[49]
Doozandeh-Juibari, A.; Ghovvati, S.; Vaziri, H.R.; Sohani, M.M.; Pezeshkian, Z. Cloning, expression, purification and evaluation of the biological properties of the recombinant human growth hormone (hGH) in Escherichia coli. Int. J. Pept. Res. Ther., 2020, 26(1), 487-495.
[http://dx.doi.org/10.1007/s10989-019-09854-y]
[50]
Samant, S.; Gupta, G.; Karthikeyan, S.; Haq, S.F.; Nair, A.; Sambasivam, G.; Sukumaran, S. Effect of codon-optimized E. coli signal peptides on recombinant Bacillus stearothermophilus maltogenic amylase periplasmic localization, yield and activity. J. Ind. Microbiol. Biotechnol., 2014, 41(9), 1435-1442.
[http://dx.doi.org/10.1007/s10295-014-1482-8] [PMID: 25038884]
[51]
Low, K.O.; Jonet, M.A.; Ismail, N.F.; Illias, R.M. Optimization of a Bacillus sp signal peptide for improved recombinant protein secretion and cell viability in Escherichia coli. Bioengineered, 2012, 3(6), 334-338.
[http://dx.doi.org/10.4161/bioe.21454] [PMID: 22892592]
[52]
Zamani, M.; Nezafat, N.; Negahdaripour, M.; Dabbagh, F.; Ghasemi, Y. In silico evaluation of different signal peptides for the secretory production of human growth hormone in E. coli. Int. J. Pept. Res. Ther., 2015, 21(3), 261-268.
[http://dx.doi.org/10.1007/s10989-015-9454-z]
[53]
Hajihassan, Z.; Sohrabi, M.; Rajabi Bazl, M.; Eftekhary, H. Expression of human nerve growth factor beta and bacterial protein disulfide isomerase (DsbA) as a fusion protein (DsbA: hNGF) significantly enhances periplasmic production of hNGF beta in Escherichia coli. Rom. Biotechnol. Lett., 2016, 21(5), 11850-11856.
[54]
Yıldırım, Z.; Çelik, E. Periplasmic and extracellular production of cellulase from recombinant Escherichia coli cells. J. Chem. Technol. Biotechnol., 2017, 92(2), 319-324.
[http://dx.doi.org/10.1002/jctb.5008]
[55]
Shi, L.; Liu, H.; Gao, S.; Weng, Y.; Zhu, L. Enhanced extracellular production of is PETase in Escherichia coli via engineering of the pelB signal peptide. J. Agric. Food Chem., 2021, 69(7), 2245-2252.
[http://dx.doi.org/10.1021/acs.jafc.0c07469] [PMID: 33576230]
[56]
Seo, H.; Kim, S.; Son, H.F.; Sagong, H.Y.; Joo, S.; Kim, K.J. Production of extracellular PETase from Ideonella sakaiensis using sec-dependent signal peptides in E. coli. Biochem. Biophys. Res. Commun., 2019, 508(1), 250-255.
[http://dx.doi.org/10.1016/j.bbrc.2018.11.087] [PMID: 30477746]
[57]
Jong, W.S.P.; Vikström, D.; Houben, D.; van den Berg van Saparoea, H.B.; de Gier, J.W.; Luirink, J. Application of an E. coli signal sequence as a versatile inclusion body tag. Microb. Cell Fact., 2017, 16(1), 50.
[http://dx.doi.org/10.1186/s12934-017-0662-4] [PMID: 28320377]
[58]
Singh, P.; Sharma, L.; Kulothungan, S.R.; Adkar, B.V.; Prajapati, R.S.; Ali, P.S.S.; Krishnan, B.; Varadarajan, R. Effect of signal peptide on stability and folding of Escherichia coli thioredoxin. PLoS One, 2013, 8(5), e63442.
[http://dx.doi.org/10.1371/journal.pone.0063442] [PMID: 23667620]
[59]
Beena, K.; Udgaonkar, J.B.; Varadarajan, R. Effect of signal peptide on the stability and folding kinetics of maltose binding protein. Biochemistry, 2004, 43(12), 3608-3619.
[http://dx.doi.org/10.1021/bi0360509] [PMID: 15035631]
[60]
Cui, Y.; Meng, Y.; Zhang, J.; Cheng, B.; Yin, H.; Gao, C.; Xu, P.; Yang, C. Efficient secretory expression of recombinant proteins in Escherichia coli with a novel actinomycete signal peptide. Protein Expr. Purif., 2017, 129, 69-74.
[http://dx.doi.org/10.1016/j.pep.2016.09.011] [PMID: 27664436]
[61]
Fallah, M.; Akbari, B.; Saeidi, N. A.; Karimi, M.; Vaez, M.; Zeyn, A. M.; Soleymani, M.; Maghsoudi, N. Overexpression of Recombinant Human Granulocyte Colony-Stimulating Factor (huG-CSF) in E.coli. Iranian J Med Sci, 2003, 28(3), 131-134.
[62]
Tehrani, S.S.; Goodarzi, G.; Naghizadeh, M.; Khatami, S.H.; Movahedpour, A.; Abbasi, A.; Shabaninejad, Z.; Khalaf, N.; Taheri-Anganeh, M.; Savardashtaki, A. Suitable signal peptides for secretory production of recombinant granulocyte colony stimulating factor in Escherichia coli. Recent Pat. Biotechnol., 2020, 14(4), 269-282.
[http://dx.doi.org/10.2174/1872208314999200730115018] [PMID: 32838727]
[63]
Jeong, K.J.; Lee, S.Y. Secretory production of human granulocyte colony-stimulating factor in Escherichia coli. Protein Expr. Purif., 2001, 23(2), 311-318.
[http://dx.doi.org/10.1006/prep.2001.1508] [PMID: 11676607]
[64]
Huber, D.; Cha, M.; Debarbieux, L.; Planson, A.G.; Cruz, N.; López, G.; Tasayco, M.L.; Chaffotte, A.; Beckwith, J. A selection for mutants that interfere with folding of Escherichia coli thioredoxin-1 in vivo. Proc. Natl. Acad. Sci. USA, 2005, 102(52), 18872-18877.
[http://dx.doi.org/10.1073/pnas.0509583102] [PMID: 16357193]
[65]
Schierle, C.F.; Berkmen, M.; Huber, D.; Kumamoto, C.; Boyd, D.; Beckwith, J. The DsbA signal sequence directs efficient, cotranslational export of passenger proteins to the Escherichia coli periplasm via the signal recognition particle pathway. J. Bacteriol., 2003, 185(19), 5706-5713.
[http://dx.doi.org/10.1128/JB.185.19.5706-5713.2003] [PMID: 13129941]
[66]
Li, C.; Wang, Y.; Liu, T.; Niklasch, M.; Qiao, K.; Durand, S.; Chen, L.; Liang, M.; Baumert, T.F.; Tong, S.; Nassal, M.; Wen, Y.M.; Wang, Y.X. An E. coli-produced single-chain variable fragment (scFv) targeting hepatitis B virus surface protein potently inhibited virion secretion. Antiviral Res., 2019, 162, 118-129.
[http://dx.doi.org/10.1016/j.antiviral.2018.12.019] [PMID: 30599174]
[67]
Lobstein, J.; Emrich, C.A.; Jeans, C.; Faulkner, M.; Riggs, P.; Berkmen, M. SHuffle, a novel Escherichia coli protein expression strain capable of correctly folding disulfide bonded proteins in its cytoplasm. Microb. Cell Fact., 2012, 11(1), 753.
[http://dx.doi.org/10.1186/1475-2859-11-56] [PMID: 22569138]
[68]
Robinson, M.P.; Ke, N.; Lobstein, J.; Peterson, C.; Szkodny, A.; Mansell, T.J.; Tuckey, C.; Riggs, P.D.; Colussi, P.A.; Noren, C.J.; Taron, C.H.; DeLisa, M.P.; Berkmen, M. Efficient expression of full-length antibodies in the cytoplasm of engineered bacteria. Nat. Commun., 2015, 6(1), 8072.
[http://dx.doi.org/10.1038/ncomms9072] [PMID: 26311203]
[69]
Yusakul, G.; Nuntawong, P.; Sakamoto, S.; Ratnatilaka Na Bhuket, P.; Kohno, T.; Kikkawa, N.; Rojsitthisak, P.; Shimizu, K.; Tanaka, H.; Morimoto, S. Bacterial expression of a single-chain variable fragment (scFv) antibody against ganoderic acid A: A cost-effective approach for quantitative analysis using the scFv-based enzyme-linked immunosorbent assay. Biol. Pharm. Bull., 2017, 40(10), 1767-1774.
[http://dx.doi.org/10.1248/bpb.b17-00531] [PMID: 28966249]
[70]
Gaciarz, A.; Veijola, J.; Uchida, Y.; Saaranen, M.J.; Wang, C.; Hörkkö, S.; Ruddock, L.W. Systematic screening of soluble expression of antibody fragments in the cytoplasm of E. coli. Microb. Cell Fact., 2016, 15(1), 22.
[http://dx.doi.org/10.1186/s12934-016-0419-5] [PMID: 26809624]
[71]
Hatahet, F.; Nguyen, V.D.; Salo, K.E.H.; Ruddock, L.W. Disruption of reducing pathways is not essential for efficient disulfide bond formation in the cytoplasm of E. coli. Microb. Cell Fact., 2010, 9(1), 67.
[http://dx.doi.org/10.1186/1475-2859-9-67] [PMID: 20836848]
[72]
Hatahet, F.; Ruddock, L.W. Topological plasticity of enzymes involved in disulfide bond formation allows catalysis in either the periplasm or the cytoplasm. J. Mol. Biol., 2013, 425(18), 3268-3276.
[http://dx.doi.org/10.1016/j.jmb.2013.04.034] [PMID: 23810903]
[73]
Nguyen, V.D.; Hatahet, F.; Salo, K.E.H.; Enlund, E.; Zhang, C.; Ruddock, L.W. Pre-expression of a sulfhydryl oxidase significantly increases the yields of eukaryotic disulfide bond containing proteins expressed in the cytoplasm of E. coli. Microb. Cell Fact., 2011, 10(1), 1-13.
[http://dx.doi.org/10.1186/1475-2859-10-1] [PMID: 21211066]
[74]
Wang, Y.; Yuan, W.; Guo, S.; Li, Q.; Chen, X.; Li, C.; Liu, Q.; Sun, L.; Chen, Z.; Yuan, Z.; Luo, C.; Chen, S.; Tong, S.; Nassal, M.; Wen, Y.M.; Wang, Y.X. A 33-residue peptide tag increases solubility and stability of Escherichia coli produced single-chain antibody fragments. Nat. Commun., 2022, 13(1), 4614.
[http://dx.doi.org/10.1038/s41467-022-32423-9] [PMID: 35941164]
[75]
Dalmora, S.; de Oliveira, J.E.; Affonso, R.; Gimbo, E.; Ribela, M.T.C.P.; Bartolini, P. Analysis of recombinant human growth hormone directly in osmotic shock fluids. J. Chromatogr. A, 1997, 782(2), 199-210.
[http://dx.doi.org/10.1016/S0021-9673(97)00493-7] [PMID: 9368400]
[76]
Chart, H.; Smith, H.R.; La Ragione, R.M.; Woodward, M.J. An investigation into the pathogenic properties of Escherichia coli strains BLR, BL21, DH5α and EQ1. J. Appl. Microbiol., 2000, 89(6), 1048-1058.
[http://dx.doi.org/10.1046/j.1365-2672.2000.01211.x] [PMID: 11123478]
[77]
Prinz, W.A.; Åslund, F.; Holmgren, A.; Beckwith, J. The role of the thioredoxin and glutaredoxin pathways in reducing protein disulfide bonds in the Escherichia coli cytoplasm. J. Biol. Chem., 1997, 272(25), 15661-15667.
[http://dx.doi.org/10.1074/jbc.272.25.15661] [PMID: 9188456]
[78]
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]
[79]
Dumon-Seignovert, L.; Cariot, G.; Vuillard, L. The toxicity of recombinant proteins in Escherichia coli: A comparison of overexpression in BL21(DE3), C41(DE3), and C43(DE3). Protein Expr. Purif., 2004, 37(1), 203-206.
[http://dx.doi.org/10.1016/j.pep.2004.04.025] [PMID: 15294299]
[80]
Baumgarten, T.; Schlegel, S.; Wagner, S.; Löw, M.; Eriksson, J.; Bonde, I.; Herrgård, M.J.; Heipieper, H.J.; Nørholm, M.H.H.; Slotboom, D.J.; de Gier, J.W. Isolation and characterization of the E. coli membrane protein production strain Mutant56(DE3). Sci. Rep., 2017, 7(1), 45089.
[http://dx.doi.org/10.1038/srep45089] [PMID: 28338018]
[81]
Sone, M.; Kishigami, S.; Yoshihisa, T.; Ito, K. Roles of disulfide bonds in bacterial alkaline phosphatase. J. Biol. Chem., 1997, 272(10), 6174-6178.
[http://dx.doi.org/10.1074/jbc.272.10.6174] [PMID: 9045630]
[82]
Wagner, S.; Klepsch, M.M.; Schlegel, S.; Appel, A.; Draheim, R.; Tarry, M.; Högbom, M.; van Wijk, K.J.; Slotboom, D.J.; Persson, J.O.; de Gier, J.W. Tuning Escherichia coli for membrane protein overexpression. Proc. Natl. Acad. Sci. USA, 2008, 105(38), 14371-14376.
[http://dx.doi.org/10.1073/pnas.0804090105] [PMID: 18796603]
[83]
Schumann, W.; Ferreira, L.C.S. Production of recombinant proteins in Escherichia coli. Genet. Mol. Biol., 2004, 27(3), 442-453.
[http://dx.doi.org/10.1590/S1415-47572004000300022]
[84]
Kaur, J.; Kumar, A.; Kaur, J. Strategies for optimization of heterologous protein expression in E. coli: Roadblocks and reinforcements. Int. J. Biol. Macromol., 2018, 106, 803-822.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.08.080] [PMID: 28830778]
[85]
Polisky, B.; Bishop, R.J.; Gelfand, D.H. A plasmid cloning vehicle allowing regulated expression of eukaryotic DNA in bacteria. Proc. Natl. Acad. Sci. USA, 1976, 73(11), 3900-3904.
[http://dx.doi.org/10.1073/pnas.73.11.3900] [PMID: 1069275]
[86]
de Boer, H.A.; Comstock, L.J.; Vasser, M. The tac promoter: A functional hybrid derived from the trp and lac promoters. Proc. Natl. Acad. Sci. USA, 1983, 80(1), 21-25.
[http://dx.doi.org/10.1073/pnas.80.1.21] [PMID: 6337371]
[87]
Brosius, J.; Erfle, M.; Storella, J. Spacing of the -10 and -35 regions in the tac promoter. Effect on its in vivo activity. J. Biol. Chem., 1985, 260(6), 3539-3541.
[http://dx.doi.org/10.1016/S0021-9258(19)83655-4] [PMID: 2579077]
[88]
Guzman, L.M.; Belin, D.; Carson, M.J.; Beckwith, J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol., 1995, 177(14), 4121-4130.
[http://dx.doi.org/10.1128/jb.177.14.4121-4130.1995] [PMID: 7608087]
[89]
Studier, F.W. Use of bacteriophage T7 lysozyme to improve an inducible T7 expression system. J. Mol. Biol., 1991, 219(1), 37-44.
[http://dx.doi.org/10.1016/0022-2836(91)90855-Z] [PMID: 2023259]
[90]
Sethia, P.P.; Rao, K.K.; Noronha, S.B. A dps promoter based expression system for improved solubility of expressed proteins in Escherichia coli. Biotechnol. Bioprocess Eng.; BBE, 2014, 19(5), 790-797.
[http://dx.doi.org/10.1007/s12257-013-0722-5]
[91]
Johnson, A.D.; Poteete, A.R.; Lauer, G.; Sauer, R.T.; Ackers, G.K.; Ptashne, M. λ Repressor and cro—components of an efficient molecular switch. Nature, 1981, 294(5838), 217-223.
[http://dx.doi.org/10.1038/294217a0] [PMID: 6457992]
[92]
Mieschendahl, M.; Petri, T.; Hänggi, U. A novel prophage independent trp regulated lambda PL expression system. Bio/Technology, 1986, 4(9), 802-808.
[93]
Love, C.A.; Lilley, P.E.; Dixon, N.E. Stable high-copy-number bacteriophage λ promoter vectors for overproduction of proteins in Escherichia coli. Gene, 1996, 176(1-2), 49-53.
[http://dx.doi.org/10.1016/0378-1119(96)00208-9] [PMID: 8918231]
[94]
Vélez, A.M.; Horta, A.C.L.; da Silva, A.J.; Iemma, M.R.C.; Giordano, R.L.C.; Zangirolami, T.C. Enhanced production of recombinant thermo-stable lipase in Escherichia coli at high induction temperature. Protein Expr. Purif., 2013, 90(2), 96-103.
[http://dx.doi.org/10.1016/j.pep.2013.05.005] [PMID: 23727254]
[95]
Francis, D. M.; Page, R. Strategies to optimize protein expression in E. coli. Curr Protoc Protein Sci, 2010, 61(1), 25.24. 21-25.24. 29.
[96]
Mairhofer, J.; Cserjan-Puschmann, M.; Striedner, G.; Nöbauer, K.; Razzazi-Fazeli, E.; Grabherr, R. Marker-free plasmids for gene therapeutic applications—Lack of antibiotic resistance gene substantially improves the manufacturing process. J. Biotechnol., 2010, 146(3), 130-137.
[http://dx.doi.org/10.1016/j.jbiotec.2010.01.025] [PMID: 20138928]
[97]
Sørensen, H.P.; Mortensen, K.K. Advanced genetic strategies for recombinant protein expression in Escherichia coli. J. Biotechnol., 2005, 115(2), 113-128.
[http://dx.doi.org/10.1016/j.jbiotec.2004.08.004] [PMID: 15607230]
[98]
Selzer, G.; Som, T.; Itoh, T.; Tomizawa, J. The origin of replication of plasmid p15A and comparative studies on the nucleotide sequences around the origin of related plasmids. Cell, 1983, 32(1), 119-129.
[http://dx.doi.org/10.1016/0092-8674(83)90502-0] [PMID: 6186390]
[99]
Sørensen, H.; Mortensen, K. Soluble expression of recombinant proteins in the cytoplasm of Escherichia coli. Microb. Cell Fact., 2005, 4(1), 1-8.
[http://dx.doi.org/10.1186/1475-2859-4-1] [PMID: 15629064]
[100]
de Groot, N.S.; Ventura, S. Effect of temperature on protein quality in bacterial inclusion bodies. FEBS Lett., 2006, 580(27), 6471-6476.
[http://dx.doi.org/10.1016/j.febslet.2006.10.071] [PMID: 17101131]
[101]
Mizukami, T.; Komatsu, Y.; Hosoi, N.; Itoh, S.; Oka, T. Production of active human interferon-? in E. coli I. Preferential production by lower culture temperature. Biotechnol. Lett., 1986, 8(9), 605-610.
[http://dx.doi.org/10.1007/BF01025964]
[102]
Voulgaridou, G.P.; Mantso, T.; Chlichlia, K.; Panayiotidis, M.I.; Pappa, A. Efficient E. coli expression strategies for production of soluble human crystallin ALDH3A1. PLoS One, 2013, 8(2), e56582.
[http://dx.doi.org/10.1371/journal.pone.0056582] [PMID: 23451057]
[103]
Chen, J.; Acton, T.B.; Basu, S.K.; Montelione, G.T.; Inouye, M. Enhancement of the solubility of proteins overexpressed in Escherichia coli by heat shock. J. Mol. Microbiol. Biotechnol., 2002, 4(6), 519-524.
[PMID: 12432951]
[104]
Ramírez, O.T.; Zamora, R.; Espinosa, G.; Merino, E.; Bolívar, F.; Quintero, R. Kinetic study of penicillin acylase production by recombinant E. coli in batch cultures. Process Biochem., 1994, 29(3), 197-206.
[http://dx.doi.org/10.1016/0032-9592(94)85004-6]
[105]
Tolia, N.H.; Joshua-Tor, L. Strategies for protein coexpression in Escherichia coli. Nature methods2006, 3 (1), 55-64. Baneyx, F.; Mujacic, M. Recombinant protein folding and misfolding in Escherichia coli. Nat. Biotechnol., 2004, 22(11), 1399-1408.
[PMID: 15529165]
[106]
García-Fraga, B.; da Silva, A.F.; López-Seijas, J.; Sieiro, C. Optimized expression conditions for enhancing production of two recombinant chitinolytic enzymes from different prokaryote domains. Bioprocess Biosyst. Eng., 2015, 38(12), 2477-2486.
[http://dx.doi.org/10.1007/s00449-015-1485-5] [PMID: 26470707]
[107]
Hai, T.N. Expression of flagellin FLjB derived from Salmonella enterica serovar typhimurium in Escherichia coli BL21. Academia Journal of Biology, 2014, 36(4), 506-514.

Rights & Permissions Print Cite
© 2025 Bentham Science Publishers | Privacy Policy