A novel fusion protein system for the production of native human pepsinogen in the bacterial periplasm

Walsh, 2003, Pharmaceutical biotechnology products approved within the European Union, Eur. J. Pharm. Biopharm., 55, 3, 10.1016/S0939-6411(02)00165-0 Baneyx, 1999, Recombinant protein expression in Escherichia coli, Curr. Opin. Biotechnol., 10, 411, 10.1016/S0958-1669(99)00003-8 Hannig, 1998, Strategies for optimizing heterologous protein expression in Escherichia coli, Trends Biotechnol., 16, 54, 10.1016/S0167-7799(97)01155-4 Swarts, 2001, Advances in Escherichia coli production of therapeutic proteins, Curr. Opin. Biotechnol., 12, 195, 10.1016/S0958-1669(00)00199-3 Pavlou, 2004, Recombinant protein therapeutics—success rates, market trends and values to 2010, Nat. Biotechnol., 22, 1513, 10.1038/nbt1204-1513 Fruton, 2002, A history of pepsin and related enzymes, Q. Rev. Biol., 77, 127, 10.1086/340729 Tang, 2004, Pepsin A, vol. 1, 19 Rawlings, 2004, Introduction: aspartic peptidases and their clans, vol. 1, 3 Sinha, 1999, Purification and cloning of amyloid precursor protein ß-secretase from human brain, Nature, 402, 537, 10.1038/990114 Vassar, 1999, Beta-secretase cleavage of Alzheimer’s amyloid precursor protein by the transmembrane aspartic protease BACE, Science, 286, 735, 10.1126/science.286.5440.735 Suzuki, 2004, Renin, vol. 1, 54 Erickson-Viitanen, 1989, Cleavage of HIV-1 gag polyprotein synthesized in vitro: sequential cleavage by the viral protease, AIDS Res. Hum. Retroviruses, 5, 577, 10.1089/aid.1989.5.577 Scorilas, 1999, Immunoenzymatically determined pepsinogen C concentration in breast tumor cytosols: an independent favorable prognostic factor in node-positive patients, Clin. Cancer Res., 5, 1778 Conner, 2004, Cathepsin D, vol. 1, 43 Hewitt, 1997, Natural processing sites for human cathepsin E and cathepsin D in tetanus toxin. Implications for T cell epitope generation, J. Immunol., 159, 4693, 10.4049/jimmunol.159.10.4693 Maric, 1994, Endosomal aspartic proteases are required for invariant-chain processing, Proc. Natl. Acad. Sci. USA, 91, 2171, 10.1073/pnas.91.6.2171 Sachdev, 1998, Solubility of proteins isolated from inclusion bodies is enhanced by fusion to maltose-binding protein or thioredoxin, Protein Expr. Purif., 12, 122, 10.1006/prep.1997.0826 Scarborough, 1994, Redesign of the substrate specificity of human cathepsin D: the dominant role of position 287 in the S2 subsite, Protein Eng., 7, 495, 10.1093/protein/7.4.495 X. Lin, Universal procedure for refolding of recombinant proteins, USP 6,585,268 (2003). Malik, 2005, Use of enhanced green fluorescent protein EGFP to determine pepsin at high sensitivity, Anal. Biochem., 340, 252, 10.1016/j.ab.2005.02.022 Chung, 1983, Purification from Escherichia coli of a periplasmic protein that is a potent inhibitor of pancreatic proteases, J. Biol. Chem., 258, 11032, 10.1016/S0021-9258(17)44382-1 Eggers, 2004, The periplasmic serine protease inhibitor ecotin protects bacteria against neutrophil elastase, Biochem. J., 379, 107, 10.1042/bj20031790 McGrath, 1994, Macromolecular chelation as an improved mechanism of protease inhibition: structure of the ecotin-trypsin complex, EMBO J., 13, 1502, 10.1002/j.1460-2075.1994.tb06411.x Stoop, 2003, Engineering of a macromolecular scaffold to develop specific protease inhibitors, Nature Biotechnol., 21, 1063, 10.1038/nbt860 Wang, 1995, Isolation of a high affinity inhibitor of urokinase-type plasminogen activator by phage display of ecotin, J. Biol. Chem., 270, 12250, 10.1074/jbc.270.20.12250 Kang, 1994, Effect of modification of connecting peptide of proinsulin on its export, J. Biotechnol., 36, 45, 10.1016/0168-1656(94)90022-1 Rathore, 2003, Optimization of an osmotic shock procedure for isolation of a protein product expressed in E. coli, Biotechnol. Prog., 19, 1541, 10.1021/bp034030s Bradford, 1976, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding, Anal. Biochem., 72, 248, 10.1016/0003-2697(76)90527-3 Amann, 1988, Tightly regulated tac promoter vectors useful for the expression of unfused and fused protein in Escherichia coli, Gene, 69, 301, 10.1016/0378-1119(88)90440-4 Guzman, 1995, Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter, J. Bacteriol., 177, 4121, 10.1128/jb.177.14.4121-4130.1995 Lee, 1991, Molecular cloning of the ecotin gene in Escherichia coli, FEBS Lett., 287, 53, 10.1016/0014-5793(91)80014-T Hottenrott, 1997, The Escherichia coli SlyD is a metal ion-regulated peptidyl-prolyl cis/trans-isomerase, J. Biol. Chem., 272, 15697, 10.1074/jbc.272.25.15697 Wülfing, 1994, An Escherichia coli protein consisting of a domain homologous to FK506-binding proteins (FKBP) and a new metal binding motif, J. Biol. Chem., 269, 2895, 10.1016/S0021-9258(17)42026-6 Bustin, 1971, Intramolecular activation of porcine pepsinogen, J. Biol. Chem., 246, 615, 10.1016/S0021-9258(18)62458-5 Lin, 1989, Synthesis, purification, and active site mutagenesis of recombinant porcine pepsinogen, J. Biol. Chem., 264, 4482, 10.1016/S0021-9258(18)83769-3 Marciniszyn, 1976, Mechanism of intramolecular activation of pepsinogen. Evidence for an intermediate delta and the involvement of the active site of pepsin in the intramolecular activation of pepsinogen, J. Biol. Chem., 251, 7095, 10.1016/S0021-9258(17)32946-0 Hartsuck, 1992, The high-resolution crystal structure of porcine pepsinogen, Proteins, 13, 1, 10.1002/prot.340130102 Richter, 1998, Mechanism of activation of the gastric aspartic proteinases: pepsinogen, progastricsin and prochymosin, Biochem. J., 335, 481, 10.1042/bj3350481 Kageyama, 1989, Difference of activation processes and structure of activation peptides in human pepsinogens A and progastricsin, J. Biochem. (Tokyo), 105, 15, 10.1093/oxfordjournals.jbchem.a122610 Josefsson, 1981, Different exported proteins in E. coli show differences in the temporal mode of processing in vivo, Cell, 25, 151, 10.1016/0092-8674(81)90239-7 Liu, 1989, Physiological role during export fro the retardation of folding by the leader peptide of maltose-binding protein, Proc. Natl. Acad. Sci. USA, 86, 9213, 10.1073/pnas.86.23.9213 Schierle, 2003, The DsbA signal sequence directes efficient, cotranslational export of passenger proteins to the Escherichia coli periplasm via the signal recognition particle pathway, J. Bacteriol., 185, 5706, 10.1128/JB.185.19.5706-5713.2003 Kajava, 2000, The net charge of the first 18 residues of the mature sequence affects protein translocation across the cytoplasmic membrane of gram-negative bacteria, J. Bacteriol., 182, 2163, 10.1128/JB.182.8.2163-2169.2000 Summers, 1989, Illicit secretion of a cytoplasmic protein into the periplasm of Escherichia coli requires a signal peptide plus a portion of the cognate secreted protein, J. Biol. Chem., 264, 20074, 10.1016/S0021-9258(19)47220-7 Summers, 1989, A conservative amino acid substitution, arginine for lysine, abolishes export of a hybrid protein in Escherichia coli, J. Biol. Chem., 264, 20082, 10.1016/S0021-9258(19)47221-9 di Guana, 1988, Vectors that facilitate the expression and purification of foreign peptides in Escherichia coli by fusion to maltose-binding protein, Gene, 67, 21, 10.1016/0378-1119(88)90004-2 Randall, 1983, Translocation domains of nascent periplasmic proteins across the cytoplasmic membrane is independent of elongation, Cell, 33, 231, 10.1016/0092-8674(83)90352-5 Collier, 1988, The antifolding activity of SecB promotes the export of the E. coli maltose-binding protein, Cell, 53, 273, 10.1016/0092-8674(88)90389-3 Nilsson, 1985, Immobilization and purification of enzymes with staphylococcal protein A gene fusion vectors, EMBO J., 4, 1075, 10.1002/j.1460-2075.1985.tb03741.x Hellebust, 1998, Expression of the second epidermal growth factor-like domain of human factor VII in Escherichia coli, J. Biotechnol., 66, 203, 10.1016/S0168-1656(98)00165-5 Mergulhao, 2004, Evaluation of bottlenecks in proinsulin secretion by Escherichia coli, J. Biotechnol., 109, 10.1016/j.jbiotec.2003.10.024 Moks, 1987, Expression of human insulin-like growth factor I in bacteria: use of optimized gene fusion vectors to facilitate protein purification, Biochemistry, 26, 5239, 10.1021/bi00391a005 Collins-Racie, 1995, Production of recombinant bovine enterokinase catalytic subunit in Escherichia coli using the novel secretory fusion partner DsbA, Biotechnology, 13, 982, 10.1038/nbt0995-982 Winter, 2000, Increased production of human proinsulin in the periplasmic space of Escherichia coli fusion to DsbA, J. Biotechnol., 84, 175, 10.1016/S0168-1656(00)00356-4 Schmoldt, 2005, A fusion protein system for the recombinant production of short disulfide bond rich cystine knot peptides using barnase as a purification handle, Protein Expr. Purif., 39, 82, 10.1016/j.pep.2004.09.016 Tanaka, 1996, Expression of soluble cloned porcine pepsinogen A in Escherichia coli, Biochem. J., 315, 443, 10.1042/bj3150443 Yoshimasu, 2002, Soluble expression and purification of porcine pepsinogen from Pichia pastoris, Protein Expr. Purif., 25, 229, 10.1016/S1046-5928(02)00003-1