Site-directed mutagenesis of cysteine to serine residues affects heparin binding and mitogenicity in fibroblast growth factor 4 produced in Escherichia coli

References

• Itoh N, Ornitz DM. Fibroblast growth factors: from molecular evolution to roles in development, metabolism and disease. J Biochem. 2011;149:121–130.
   PubMed Web of Science ®Google Scholar
• Tanaka S, Kunath T, Hadjantonakis A, et al. Promotion of trophoblast stem cell proliferation by FGF4. Science. 1998;282:2072–2075.
   PubMed Web of Science ®Google Scholar
• Feldman B, Poueymirou W, Papaioannou VE, et al. Requirement of FGF-4 for postimplantation mouse development. Science. 1995;267:246–249.
   PubMed Web of Science ®Google Scholar
• Niswander L, Martin GR. Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development. 1992;114:755–768.
   PubMed Web of Science ®Google Scholar
• Danopoulos S, Schlieve CR, Grikscheit TC, et al. Fibroblast growth factors in the gastrointestinal tract: twists and turns. Dev Dyn. 2017;246:344–352.
   PubMed Web of Science ®Google Scholar
• Cancilla B, Ford-Perriss MD, Bertram JF. Expression and localization of fibroblast growth factors and fibroblast growth factor receptors in the developing rat kidney. Kidney Int. 1999;56:2025–2039.
   PubMed Web of Science ®Google Scholar
• Kratochwil K, Galceran J, Tontsch S, et al. FGF4, a direct target of LEF1 and Wnt signaling, can rescue the arrest of tooth organogenesis in Lef1(-/-) mice. Genes Dev. 2002;16:3173–3185.
   PubMed Web of Science ®Google Scholar
• Spence JR, Mayhew CN, Rankin SA, et al. Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature. 2011;470:105–109.
   PubMed Web of Science ®Google Scholar
• Leslie JL, Huang S, Opp JS, et al. Persistence and toxin production by Clostridium difficile within human intestinal organoids result in disruption of epithelial paracellular barrier function. Infect Immun. 2015;83:138–145.
   PubMed Web of Science ®Google Scholar
• Xie M, Li JP. Heparan sulfate proteoglycan – a common receptor for diverse cytokines. Cell Signal. 2019;54:115–121.
   PubMed Web of Science ®Google Scholar
• Guimond S, Maccarana M, Olwin BB, et al. Activating and inhibitory heparin sequences for FGF-2 (basic FGF). Distinct requirements for FGF-1. FGF-2, and FGF-4. J Biol Chem. 1993;268:23906–23914.
   PubMed Web of Science ®Google Scholar
• Ishihara M, Shaklee PN, Yang Z, et al. Structural features in heparin which modulate specific biological activities mediated by basic fibroblast growth factor. Glycobiology. 1994;4:451–458.
   PubMed Web of Science ®Google Scholar
• Ishihara M. Structural requirements in heparin for binding and activation of FGF-1 and FGF-4 are different from that for FGF-2. Glycobiology. 1994;4:817–824.
   PubMed Web of Science ®Google Scholar
• Allen BL, Filla MS, Rapraeger AC. Role of heparan sulfate as a tissue-specific regulator of FGF-4 and FGF receptor recognition. J Cell Biol. 2001;155:845–858.
   PubMed Web of Science ®Google Scholar
• Shimokawa K, Kimura-Yoshida C, Nagai N, et al. Cell surface heparan sulfate chains regulate local reception of FGF signaling in the mouse embryo. Dev Cell. 2011;21:257–272.
   PubMed Web of Science ®Google Scholar
• Arakawa T, Hsu YR, Schiffer SG, et al. Characterization of a cysteine-free analog of recombinant human basic fibroblast growth factor. Biochem Biophys Res Commun. 1989;161:335–341.
   PubMed Web of Science ®Google Scholar
• Caccia P, Nitti G, Cletini O, et al. Stabilization of recombinant human basic fibroblast growth factor by chemical modifications of cysteine residues. Eur J Biochem. 1992;204:649–655.
   PubMedGoogle Scholar
• Linemeyer DL, Menke JG, Kelly LJ, et al. Disulfide bonds are neither required, present, nor compatible with full activity of human recombinant acidic fibroblast growth factor. Growth Factors. 1990;3:287–298.
   PubMed Web of Science ®Google Scholar
• Ortega S, Schaeffer MT, Soderman D, et al. Conversion of cysteine to serine residues alters the activity, stability, and heparin dependence of acidic fibroblast growth factor. J Biol Chem. 1991;266:5842–5846.
   PubMed Web of Science ®Google Scholar
• Bare LA, Brown M, Goyal S, et al. Effect of cysteine substitutions on the mitogenic activity and stability of recombinant human keratinocyte growth factor. Biochem Biophys Res Commun. 1994;205:872–879.
   PubMed Web of Science ®Google Scholar
• Seno M, Sasada R, Iwane M, et al. Stabilizing basic fibroblast growth factor using protein engineering. Biochem Biophys Res Commun. 1988;151:701–708.
   PubMed Web of Science ®Google Scholar
• Sugawara S, Ito T, Sato S, et al. Production of an aminoterminally truncated, stable type of bioactive mouse fibroblast growth factor 4 in Escherichia coli. J Biosci Bioeng. 2014;117:525–530.
   PubMed Web of Science ®Google Scholar
• Nelson MD, Fitch DH. Overlap extension PCR: an efficient method for transgene construction. Methods Mol Biol. 2011;772:459–470.
   PubMedGoogle Scholar
• Hosoi Y, Ando Y, Arakawa M, et al. Production of mouse fibroblast growth factor 4 in E. coli and its application for isolation and maintenance of mouse trophoblast stem cells in vitro. J Reprod Dev. 2011;57:650–654.
   PubMed Web of Science ®Google Scholar
• Iha M, Watanabe M, Kihara Y, et al. Effect of ectopic expression of homeoprotein EGAM1C on the cell morphology, growth, and differentiation in a mouse embryonic stem cell line, MG1.19 cells. Reproduction. 2012;143:477–489.
   PubMed Web of Science ®Google Scholar
• Mori Y, Sakuraoka M, Suzuki T, et al. Exogenous TPRX1 homeoprotein modulates the gene expression of lineage-specific transcription factors in human embryonal carcinoma cells. Biotechnol Biotec Eq. 2018;32:646–652.
   Web of Science ®Google Scholar
• Sato S, Takahashi T, Nishinomiya H, et al. Common nucleotide sequence of structural gene encoding fibroblast growth factor 4 in eight cattle derived from three breeds. Anim Sci J. 2012;83:260–262.
   PubMed Web of Science ®Google Scholar
• Sugawara S, Ito T, Suzuki H, et al. Common amino acid sequences deduced from coding exons of the porcine FGF4 gene in two breeds and production of the encoded protein in Escherichia coli. Biosci Biotechnol Biochem. 2013;77:173–177.
   PubMed Web of Science ®Google Scholar
• Li Y, Sun C, Yates EA, et al. Heparin binding preference and structures in the fibroblast growth factor family parallel their evolutionary diversification. Open Biol. 2016; [cited 2019 Jan 05]6.
   Web of Science ®Google Scholar
• Bellosta P, Iwahori A, Plotnikov AN, et al. Identification of receptor and heparin binding sites in fibroblast growth factor 4 by structure-based mutagenesis. Mol Cell Biol. 2001;21:5946–5957.
   PubMed Web of Science ®Google Scholar
• Lee J, Blaber M. Structural basis of conserved cysteine in the fibroblast growth factor family: evidence for a vestigial half-cystine. J Mol Biol. 2009;393:128–139.
   PubMed Web of Science ®Google Scholar
• Culajay JF, Blaber SI, Khurana A, et al. Thermodynamic characterization of mutants of human fibroblast growth factor 1 with an increased physiological half-life. Biochemistry. 2000;39:7153–7158.
   PubMed Web of Science ®Google Scholar