Reassessment of inclusion body-based production as a versatile opportunity for difficult-to-express recombinant proteins

References

• Miroux B, Walker JE. 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;260:289–298.
   PubMed Web of Science ®Google Scholar
• Makino T, Skretas G, Georgiou G. Strain engineering for improved expression of recombinant proteins in bacteria. Microb Cell Fact. 2011;10:32.
   PubMed Web of Science ®Google Scholar
• Kane KF, Hartley DL. Formation of recombinant protein inclusion bodies in Escherichia coli. TIBTECH. 1988;695–101.
   Web of Science ®Google Scholar
• Mitraki A, King J. Protein Folding Intermediates and Inclusion Body Formation. Nat Biotechnol. 1989;7:690–697.
   Google Scholar
• Strandberg L, Enfors SO. Factors influencing inclusion body formation in the production of a fused protein in Escherichia coli. Appl Environ Microbiol. 1991;57:1669–1674.
   PubMed Web of Science ®Google Scholar
• Speed MA, Wang DI, King J. Specific aggregation of partially folded polypeptide chains: the molecular basis of inclusion body composition. Nat Biotechnol. 1996;14:1283–1287.
   PubMed Web of Science ®Google Scholar
• Ramón A, Señorale-Pose M, Marín M. Inclusion bodies: not that bad…. Front Microbiol. 2014;5:56.
   PubMed Web of Science ®Google Scholar
• Carrió MM, Villaverde A. Construction and deconstruction of bacterial inclusion bodies. J Biotechnol. 2002;96:3–12.
   PubMed Web of Science ®Google Scholar
• Carrió MM, Corchero JL, Villaverde A. Dynamics of in vivo protein aggregation: building inclusion bodies in recombinant bacteria. FEMS Microbiol Lett. 1998;169:9–15.
   PubMed Web of Science ®Google Scholar
• Tokatlidis K, Dhurjati P, Millet J, et al. High activity of inclusion bodies formed in Escherichia coli overproducing Clostridium thermocellum endoglucanase D. FEBS Lett. 1991;282:205–208.
   PubMed Web of Science ®Google Scholar
• Worrall DM, Goss NH. The formation of biologically active beta-galactosidase inclusion bodies in Escherichia coli. Aust J Biotechnol. 1989;3:28–32.
   PubMedGoogle Scholar
• García-Fruitós E, González-Montalbán N, Morell M, et al. Aggregation as bacterial inclusion bodies does not imply inactivation of enzymes and fluorescent proteins. Microb Cell Fact. 2005;4:27.
   PubMed Web of Science ®Google Scholar
• García-Fruitós E, Vázquez E, Díez-Gil C, et al. Bacterial inclusion bodies: making gold from waste. Trends Biotechnol. 2012;30:65–70.
   PubMed Web of Science ®Google Scholar
• Diener M, Kopka B, Pohl M, et al. Fusion of a coiled-coil domain facilitates the high-level production of catalytically active enzyme inclusion bodies. ChemCatChem. 2016;8:142–152.
   Web of Science ®Google Scholar
• Nahálka J. Physiological aggregation of maltodextrin phosphorylase from Pyrococcus furiosus and its application in a process of batch starch degradation to alpha-D-glucose-1-phosphate. J Ind Microbiol Biotechnol. 2008;35:219–223.
   PubMed Web of Science ®Google Scholar
• Nahálka J, Nidetzky B. Fusion to a pull-down domain: a novel approach of producing Trigonopsis variabilis D-amino acid oxidase as insoluble enzyme aggregates. Biotechnol Bioeng. 2007;97:454–461.
   PubMed Web of Science ®Google Scholar
• Nahálka J, Pätoprstý V. Enzymatic synthesis of sialylation substrates powered by a novel polyphosphate kinase (PPK3). Org Biomol Chem. 2009;7:1778.
   PubMed Web of Science ®Google Scholar
• Nahálka J, Vikartovská A, Hrabárová E. A crosslinked inclusion body process for sialic acid synthesis. J Biotechnol. 2008;134:146–153.
   PubMed Web of Science ®Google Scholar
• Kloß R, Jäger V, Diener M, et al. Catalytically active inclusion bodies: a new carrier-free enzyme immobilization method. Chem Ing Tech. 2016;88:1247. Abstract. Poster presented at the ProcessNet annual conference and 32nd DECHEMA annual conference of biotechnologists. Aachen. 12–15 Sep 2016. (ProcessNet-Jahrestagung und 32. DECHEMA-Jahrestagung der Biotechnologen 2016; vol. 88).
   Google Scholar
• Torrealba D, Parra D, Seras-Franzoso J, et al. Nanostructured recombinant cytokines: a highly stable alternative to short-lived prophylactics. Biomaterials. 2016;107:102–114.
   PubMed Web of Science ®Google Scholar
• Vazquez E, Corchero JL, Burgueno JF, et al. Functional inclusion bodies produced in bacteria as naturally occurring nanopills for advanced cell therapies. Adv Mater. 2012;24:1742–1747.
   PubMed Web of Science ®Google Scholar
• Seras-Franzoso J, Sanchez-Chardi A, Garcia-Fruitos E, et al. Cellular uptake and intracellular fate of protein releasing bacterial amyloids in mammalian cells. Soft Matter. 2016;12:3451–3460.
   PubMed Web of Science ®Google Scholar
• Rueda F, Cano-Garrido O, Mamat U, et al. Production of functional inclusion bodies in endotoxin-free Escherichia coli. Appl Microbiol Biotechnol. 2014;98:9229–9238.
   PubMed Web of Science ®Google Scholar
• Steinmann B, Christmann A, Heiseler T, et al. In vivo enzyme immobilization by inclusion body display. Appl Environ Microbiol. 2010;76:5563–5569.
   PubMed Web of Science ®Google Scholar
• Choi S-L, Lee SJ, Yeom S-J, et al. Controlled localization of functionally active proteins to inclusion bodies using leucine zippers. PLoS One. 2014;9:e97093.
   PubMed Web of Science ®Google Scholar
• Lin Z, Zhao Q, Xing L, et al. Aggregating tags for column-free protein purification. Biotechnol J. 2015;10:1877–1886.
   PubMed Web of Science ®Google Scholar
• Müller H, Salzig D, Czermak P. Considerations for the process development of insect-derived antimicrobial peptide production. Biotechnol Progress. 2015;31:1–11.
   PubMed Web of Science ®Google Scholar
• Yeboah A, Cohen RI, Rabolli C, et al. Elastin-like polypeptides: a strategic fusion partner for biologics. Biotechnol Bioeng. 2016;113:1617–1627.
   PubMed Web of Science ®Google Scholar
• Kleid DG, Yansura D, Small B, et al. Cloned viral protein vaccine for foot-and-mouth disease: responses in cattle and swine. Science. 1981;214:1125–1129.
   PubMed Web of Science ®Google Scholar
• Chen W, Cotten ML. Expression, purification, and micelle reconstitution of antimicrobial piscidin 1 and piscidin 3 for NMR studies. Protein Expr Purif. 2014;102:63–68.
   PubMed Web of Science ®Google Scholar
• Haught C, Davis GD, Subramanian R, et al. Recombinant production and purification of novel antisense antimicrobial peptide in Escherichia coli. Biotechnol Bioeng. 1998;57:55–61.
   PubMed Web of Science ®Google Scholar
• Kuliopulos A, Walsh CT. Production, purification, and cleavage of tandem repeats of recombinant peptides. J Am Chem Soc. 1994;116:4599–4607.
   Web of Science ®Google Scholar
• Rodríguez V, Asenjo JA, Andrews BA. Design and implementation of a high yield production system for recombinant expression of peptides. Microb Cell Fact. 2014;13:65.
   PubMed Web of Science ®Google Scholar
• Soundrarajan N, Cho H-s, Ahn B, et al. Green fluorescent protein as a scaffold for high efficiency production of functional bacteriotoxic proteins in Escherichia coli. Sci Rep. 2016;6:20661.
   PubMed Web of Science ®Google Scholar
• Hwang PM, Pan JS, Sykes BD. A PagP fusion protein system for the expression of intrinsically disordered proteins in Escherichia coli. Protein Expr Purif. 2012;85:148–151.
   PubMed Web of Science ®Google Scholar
• Lee JH, Kim JH, Hwang SW, et al. High-level expression of antimicrobial peptide mediated by a fusion partner reinforcing formation of inclusion bodies. Biochem Biophys Res Commun. 2000;277:575–580.
   PubMed Web of Science ®Google Scholar
• Rao XC, Li S, Hu JC, et al. A novel carrier molecule for high-level expression of peptide antibiotics in Escherichia coli. Protein Expr Purif. 2004;36:11–18.
   PubMed Web of Science ®Google Scholar
• Vidovic V, Prongidi-Fix L, Bechinger B, et al. labeling of antimicrobial peptides in Escherichia coli by means of a novel fusion partner that enables high-yield insoluble expression and fast purification. J Pept Sci. 2009;15:278–284.
   PubMed Web of Science ®Google Scholar
• Pane K, Durante L, Pizzo E, et al. Rational design of a carrier protein for the production of recombinant toxic peptides in Escherichia coli. PLoS One. 2016;11:e0146552.
   PubMed Web of Science ®Google Scholar
• Li Y, Chen Z. RAPD: a database of recombinantly-produced antimicrobial peptides. FEMS Microbiol Lett. 2008;289:126–129.
   PubMed Web of Science ®Google Scholar
• Jevševar S, Gaberc‐Porekar V, et al. Production of nonclassical inclusion bodies from which correctly folded protein can be extracted. Biotechnol Progress. 2005;21:632–639.
   PubMed Web of Science ®Google Scholar
• Peternel S, Grdadolnik J, Gaberc-Porekar V, et al. Engineering inclusion bodies for non denaturing extraction of functional proteins. Microb Cell Fact. 2008;7:34.
   PubMed Web of Science ®Google Scholar
• Mukherjee J, Nath Gupta M. Paradigm shifts in our views on inclusion bodies. Curr Biochem Eng. 2015;3:47–55.
   Google Scholar
• Arié JP, Miot M, Sassoon N, et al. Formation of active inclusion bodies in the periplasm of Escherichia coli. Mol Microbiol. 2006;62:427–437.
   PubMed Web of Science ®Google Scholar
• Choi S-L, Lee SJ, Ha J-S, et al. Generation of catalytic protein particles in Escherichia coli cells using the cellulose-binding domain from Cellulomonas fimi as a fusion partner. Biotechnol Bioprocess Eng. 2011;16:1173–1179.
   Web of Science ®Google Scholar
• Nahálka J, Mislovičová D, Kavcová H. Targeting lectin activity into inclusion bodies for the characterisation of glycoproteins. Mol BioSyst. 2009;5:819.
   PubMed Web of Science ®Google Scholar
• Park S-Y, Park S-H, Choi S-K. Active inclusion body formation using Paenibacillus polymyxa PoxB as a fusion partner in Escherichia coli. Anal Biochem. 2012;426:63–65.
   PubMed Web of Science ®Google Scholar
• Carrió M, González-Montalbán N, Vera A, et al. Amyloid-like properties of bacterial inclusion bodies. J Mol Biol. 2005;347:1025–1037.
   PubMed Web of Science ®Google Scholar
• Morell M, Bravo R, Espargaró A, et al. Inclusion bodies: specificity in their aggregation process and amyloid-like structure. Biochim Biophys Acta. 2008;1783:1815–1825.
   PubMed Web of Science ®Google Scholar
• Rueda F, Gasser B, Sánchez-Chardi A, et al. Functional inclusion bodies produced in the yeast Pichia pastoris. Microb Cell Fact. 2016;15:1385.
   Web of Science ®Google Scholar
• de Groot NS, Aviles FX, Vendrell J, et al. Mutagenesis of the central hydrophobic cluster in Abeta42 Alzheimer’s peptide. Side-chain properties correlate with aggregation propensities. FEBS J. 2006;273:658–668.
   PubMed Web of Science ®Google Scholar
• Kim W, Hecht MH. Sequence determinants of enhanced amyloidogenicity of Alzheimer A{beta}42 peptide relative to A{beta}40. J Biol Chem. 2005;280:35069–35076.
   PubMed Web of Science ®Google Scholar
• Zhou B, Xing L, Wu W, et al. Small surfactant-like peptides can drive soluble proteins into active aggregates. Microb Cell Fact. 2012;11:10.
   PubMed Web of Science ®Google Scholar
• Xing L, Xu W, Zhou B, et al. Facile expression and purification of the antimicrobial peptide histatin 1 with a cleavable self-aggregating tag (cSAT) in Escherichia coli. Protein Exp Purif. 2013;88:248–253.
   PubMed Web of Science ®Google Scholar
• Xing L, Wu W, Zhou B, et al. Streamlined protein expression and purification using cleavable self-aggregating tags. Microb Cell Fact. 2011;10:42.
   PubMed Web of Science ®Google Scholar
• Wu W, Xing L, Zhou B, et al. Active protein aggregates induced by terminally attached self-assembling peptide ELK16 in Escherichia coli. Microb Cell Fact. 2011;10:9.
   PubMed Web of Science ®Google Scholar
• Wang X, Zhou B, Hu W, et al. Formation of active inclusion bodies induced by hydrophobic self-assembling peptide GFIL8. Microb Cell Fact. 2015;14:88. eng.
   Web of Science ®Google Scholar
• Lin Z, Zhou B, Wu W, et al. Self-assembling amphipathic alpha-helical peptides induce the formation of active protein aggregates in vivo. Faraday Discuss. 2013;166:243–256.
   PubMed Web of Science ®Google Scholar
• Jong WSP, Vikstrom D, Houben D, et al. Application of an E. coli signal sequence as a versatile inclusion body tag. Microb Cell Fact. 2017;16:50.
   PubMed Web of Science ®Google Scholar
• Huang Z, Zhang C, Chen S, et al. Active inclusion bodies of acid phosphatase PhoC: aggregation induced by GFP fusion and activities modulated by linker flexibility. Microb Cell Fact. 2013;12:25.
   PubMed Web of Science ®Google Scholar
• Li G, Huang Z, Zhang C, et al. Construction of a linker library with widely controllable flexibility for fusion protein design. Appl Microbiol Biotechnol. 2016;100:215–225.
   PubMed Web of Science ®Google Scholar
• Huang Z, Li G, Zhang C, et al. A study on the effects of linker flexibility on acid phosphatase PhoC-GFP fusion protein using a novel linker library. Enzyme Microb Technol. 2016;83:1–6.
   PubMed Web of Science ®Google Scholar
• Seo JH, Li L, Yeo JS, et al. Baculoviral polyhedrin as a novel fusion partner for formation of inclusion body in Escherichia coli. Biotechnol Bioeng. 2003;84:467–473.
   PubMed Web of Science ®Google Scholar
• Hayakawa T, Sato S, Iwamoto S, et al. Novel strategy for protein production using a peptide tag derived from Bacillus thuringiensis Cry4Aa. FEBS J. 2010;277:2883–2891.
   PubMed Web of Science ®Google Scholar
• Hayashi M, Iwamoto S, Sato S, et al. Efficient production of recombinant cystatin C using a peptide-tag, 4AaCter, that facilitates formation of insoluble protein inclusion bodies in Escherichia coli. Protein Expr Purif. 2013;88:230–234.
   PubMed Web of Science ®Google Scholar
• Wakankar AA, Borchardt RT. Formulation considerations for proteins susceptible to asparagine deamidation and aspartate isomerization. J Pharm Sci. 2006;95:2321–2336.
   PubMed Web of Science ®Google Scholar
• Nellis DF, Michiel DF, Jiang M-S, et al. Characterization of recombinant human IL-15 deamidation and its practical elimination through substitution of asparagine 77. Pharm Res. 2012;29:722–738.
   PubMed Web of Science ®Google Scholar
• Middelberg APJ. Process-scale disruption of microorganisms. Biotechnol Adv. 1995;13:491–551.
   PubMed Web of Science ®Google Scholar
• Harrison STL. Bacterial cell disruption: a key unit operation in the recovery of intracellular products. Biotechnol Adv. 1991;9:217–240.
   PubMed Web of Science ®Google Scholar
• Meagher MM, Barlett RT, Rai VR, et al. Extraction of rIL-2 inclusion bodies from Escherichia coli using cross-flow filtration. Biotechnol Bioeng. 1994;43:969–977.
   PubMed Web of Science ®Google Scholar
• Agerkvist I, Enfors SO. Characterization of E. coli cell disintegrates from a bead mill and high pressure homogenizers. Biotechnol Bioeng. 1990;36:1083–1089.
   PubMed Web of Science ®Google Scholar
• Wong HH, O'Neill BK, Middelberg AP. Centrifugal processing of cell debris and inclusion bodies from recombinant Escherichia coli. Bioseparation. 1995;6:361–372.
   Google Scholar
• Wong HH, O'Neill BK, Middelberg AP. Cumulative sedimentation analysis of Escherichia coli debris size. Biotechnol Bioeng. 1997;55:556–564.
   PubMed Web of Science ®Google Scholar
• Tin Lee C, Morreale G, Middelberg APJ. Combined in-fermenter extraction and cross-flow microfiltration for improved inclusion body processing. Biotechnol Bioeng. 2004;85:103–113.
   PubMed Web of Science ®Google Scholar
• Choe W-s, Middelberg APJ. Selective precipitation of DNA by spermine during the chemical extraction of insoluble cytoplasmic protein. Biotechnol Prog. 2001;17:1107–1113.
   PubMed Web of Science ®Google Scholar
• van Hee P, Middelberg APJ, Van Der Lans, et al. Relation between cell disruption conditions, cell debris particle size, and inclusion body release. Biotechnol Bioeng. 2004;88:100–110.
   PubMed Web of Science ®Google Scholar
• Peternel S, Komel R. Isolation of biologically active nanomaterial (inclusion bodies) from bacterial cells. Microb Cell Fact. 2010;9:66.
   PubMed Web of Science ®Google Scholar
• Ehgartner D, Sagmeister P, Langemann T, et al. A novel method to recover inclusion body protein from recombinant E. coli fed-batch processes based on phage PhiX174-derived lysis protein E. Appl Microbiol Biotechnol. 2017;101:5603–5614.
   Web of Science ®Google Scholar
• Middelberg APJ, O'Neill BK. Harvesting recombinant protein inclusion bodies. In: Subramanian G, editor. Bioseparation and bioprocessing. Weinheim, New-York: Wiley-VCH; 1998. p. 81–106.
   Google Scholar
• Harrison RG, Todd P, Rudge SR, Petrides DP. Bioseparations science and engineering. New York, NY: Oxford University Press; 2015.
   Google Scholar
• Ambler C. Theory of centrifugation. Ind Eng Chem. 1961;53:430–433.
   Google Scholar
• Hwang S. Effect of inclusion bodies on the buoyant density of recombinant Escherichia coli. Biotechnol Tech. 1996;10:157–160.
   Google Scholar
• Taylor G, Hoare M, Gray, et al. Size and density of protein inclusion bodies. Nat Biotechnol. 1986;4:553–557.
   Google Scholar
• Shi T, Zhang L, Li Z, et al. Expression, purification and renaturation of truncated human integrin β1 from inclusion bodies of Escherichia coli. Protein Expr Purif. 2015;107:13–19.
   PubMed Web of Science ®Google Scholar
• Marston FAO, Lowe PA, Doel MT, et al. Purification of calf prochymosin (Prorennin) synthesized in Escherichia coli. Nat Biotechnol. 1984;2:800–804.
   Google Scholar
• Palmer I, Wingfield PT. Preparation and extraction of insoluble (inclusion-body) proteins from Escherichia coli. Curr Protoc Protein Sci. 2004;Chapter 6:3.1–3.18.
   Google Scholar
• Schoner RG, Ellis LF, Schoner BE. Isolation and purification of protein granules from Escherichia coli cells overproducing bovine growth hormone. Nat Biotechnol. 1985;3:151–154.
   Google Scholar
• Singh SM, Eshwari ANS, Garg LC, et al. Isolation, solubilization, refolding, and chromatographic purification of human growth hormone from inclusion bodies of Escherichia coli Cells. In: Smales CM, James DC, editors. Therapeutic proteins. New York, NY: Springer; 2005. p. 163–176.
   Google Scholar
• Rodríguez-Carmona E, Cano-Garrido O, Seras-Franzoso J, et al. Isolation of cell-free bacterial inclusion bodies. Microb Cell Fact. 2010;9:71.
   PubMed Web of Science ®Google Scholar
• Middelberg APJ. Large-scale recovery of protein inclusion bodies by continuous centrifugation. In: Desai MA, editor. Downstream processing of proteins: methods and protocols (Methods in biotechnology, vol. 9). Totowa, NJ: Humana Press; 2000. p. 47–58.
   Google Scholar
• Batas B, Schiraldi C, Chaudhuri JB. Inclusion body purification and protein refolding using microfiltration and size exclusion chromatography. J Biotechnol. 1999;68:149–158.
   PubMed Web of Science ®Google Scholar
• Forman SM, DeBernardez ER, Feldberg RS, et al. Crossflow filtration for the separation of inclusion bodies from soluble proteins in recombinant Escherichia coli cell lysate. J Membrane Sci. 1990;48:263–279.
   Web of Science ®Google Scholar
• Abdelrasoul A, Doan H, Lohi A. Fouling in membrane filtration and remediation methods. In: Nakajima H, editor. Mass transfer advances in sustainable energy and environment oriented numerical modeling. Rijeka, Croatia: InTech; 2014.
   Google Scholar
• Field R. Fundamentals of fouling. In: Peinemann KV, Nunes SP, editors. Membranes for water treatment, fundamentals of fouling (Membrane technology). Weinheim: Wiley-VCH; 2010. p. 1–23.
   Google Scholar
• Lee T, D’Amore T. Membrane separation theoretical and applicable considerations for optimum industrial bioprocessing. J Bioproces Biotech. 2011;1:101e.
   Google Scholar
• Bailey SM, Meagher MM. Crossflow microfiltration of recombinant Escherichia coli lysates after high pressure homogenization. Biotechnol Bioeng. 1997;56:304–310.
   PubMed Web of Science ®Google Scholar
• Vicente T, Burri S, Wellnitz S, et al. Fully aseptic single-use cross flow filtration system for clarification and concentration of cytomegalovirus-like particles. Eng Life Sci. 2014;14:318–326.
   Web of Science ®Google Scholar
• Crespo JG, Böddeker KW. Membrane processes in separation and purification (NATO ASI Series, Series E: Applied Sciences; vol. 272). Dordrecht: Springer; 1994.
   Google Scholar
• Bailey SM, Meagher MM. Separation of soluble protein from inclusion bodies in Escherichia coli lysate using crossflow microfiltration. J Membrane Sci. 2000;166:137–146.
   Web of Science ®Google Scholar
• Ledung E, Eriksson P-O, Oscarsson S. A strategic crossflow filtration methodology for the initial purification of promegapoietin from inclusion bodies. J Biotechnol. 2009;141:64–72.
   PubMed Web of Science ®Google Scholar
• Bailey SM, Meagher MM. The effect of denaturants on the crossflow membrane filtration of Escherichia coli lysates containing inclusion bodies. J Membr Sci. 1997;131:29–38.
   Web of Science ®Google Scholar
• Ouellette T, Destrau S, Zhu J, et al. Production and purification of refolded recombinant human IL-7 from inclusion bodies. Protein Expr Purif. 2003;30:156–166.
   PubMed Web of Science ®Google Scholar
• Venkiteshwaran A, Heider P, Matosevic S, et al. Optimized removal of soluble host cell proteins for the recovery of met-human growth hormone inclusion bodies from Escherichia coli cell lysate using crossflow microfiltration. Biotechnol Progress. 2007;23:667–672.
   PubMed Web of Science ®Google Scholar
• Fikar M, Kovács Z, Czermak P. Dynamic optimization of batch diafiltration processes. J Membr Sci. 2010;355:168–174.
   Web of Science ®Google Scholar
• Paulen R, Foley G, Fikar M, et al. Minimizing the process time for ultrafiltration/diafiltration under gel polarization conditions. J Membr Sci. 2011;380:148–154.
   Web of Science ®Google Scholar
• Singh A, Upadhyay V, Upadhyay AK, et al. Protein recovery from inclusion bodies of Escherichia coli using mild solubilization process. Microb Cell Fact. 2015;14:41.
   PubMed Web of Science ®Google Scholar
• Eiberle MK, Jungbauer A. Technical refolding of proteins: do we have freedom to operate? Biotechnol J. 2010;5:547–559.
   PubMed Web of Science ®Google Scholar
• Datar RV, Cartwright T, Rosen CG. Process economics of animal cell and bacterial fermentations: a case study analysis of tissue plasminogen activator. Nat Biotechnol. 1993;11:349–357.
   Google Scholar
• Gieseler G, Pepelanova I, Stuckenberg L, et al. Purification of bone morphogenetic protein-2 from refolding mixtures using mixed-mode membrane chromatography. Appl Microbiol Biotechnol. 2016;101:123–130.
   PubMed Web of Science ®Google Scholar
• Falconer RJ, O'Neill BK, Middelberg AP. Chemical treatment of Escherichia coli. II. Direct extraction of recombinant protein from cytoplasmic inclusion bodies in intact cells. Biotechnol Bioeng. 1998;57:381–386.
   PubMed Web of Science ®Google Scholar
• Falconer RJ, O'Neill BK, Middelberg AP. Chemical treatment of Escherichia coli: 3. Selective extraction of a recombinant protein from cytoplasmic inclusion bodies in intact cells. Biotechnol Bioeng. 1999;62:455–460.
   PubMed Web of Science ®Google Scholar
• Wang Q, Liu Y, Zhang C, et al. High hydrostatic pressure enables almost 100% refolding of recombinant human ciliary neurotrophic factor from inclusion bodies at high concentration. Protein Expr Purif. 2017;133:152–159.
   PubMed Web of Science ®Google Scholar
• Rodrigues D, Farinha-Arcieri LE, Ventura AM, et al. Effect of pressure on refolding of recombinant pentameric cholera toxin B. J Biotechnol. 2014;173:98–105.
   PubMed Web of Science ®Google Scholar
• Qi X, Sun Y, Xiong S. A single freeze-thawing cycle for highly efficient solubilization of inclusion body proteins and its refolding into bioactive form. Microb Cell Fact. 2015;14:24.
   PubMed Web of Science ®Google Scholar
• Puri NK, Crivelli E, Cardamone M, et al. Solubilization of growth hormone and other recombinant proteins from Escherichia coli inclusion bodies by using a cationic surfactant. Biochem J. 1992;285:871–879.
   PubMed Web of Science ®Google Scholar
• Patra AK, Mukhopadhyay R, Mukhija R, et al. Optimization of inclusion body solubilization and renaturation of recombinant human growth hormone from Escherichia coli. Protein Expr Purif. 2000;18:182–192.
   PubMed Web of Science ®Google Scholar
• Heiker JT, Kloting N, Bluher M, et al. Access to gram scale amounts of functional globular adiponectin from E. coli inclusion bodies by alkaline-shock solubilization. Biochem Biophys Res Commun. 2010;398:32–37.
   PubMed Web of Science ®Google Scholar
• Carvajal P, Gibert J, Campos N, et al. Activity of maize transglutaminase overexpressed in Escherichia coli inclusion bodies: an alternative to protein refolding. Biotechnol Progress. 2011;27:232–240.
   PubMed Web of Science ®Google Scholar
• Achmüller C, Kaar W, Ahrer K, et al. N(pro) fusion technology to produce proteins with authentic N termini in E. coli. Nat Methods. 2007;4:1037–1043.
   PubMed Web of Science ®Google Scholar
• Schmoeger E, Berger E, Trefilov A, et al. Matrix-assisted refolding of autoprotease fusion proteins on an ion exchange column. J Chromatogr A. 2009;1216:8460–8469.
   PubMed Web of Science ®Google Scholar
• Hahn R, Seifert M, Greinstetter S, et al. Peptide affinity chromatography media that bind N(pro) fusion proteins under chaotropic conditions. J Chromatogr A. 2010;1217:6203–6213.
   PubMed Web of Science ®Google Scholar