Activity and Effectiveness of Recombinant hEGF Excreted by Escherichia coli BL21 on Wound Healing in Induced Diabetic Mice

References

• Martí-Carvajal AJ, Gluud C, Nicola S, et al. Growth factors for treating diabetic foot ulcers. Cochrane Database Syst Rev. 2015. doi:10.1002/14651858.CD008548.pub2
   Web of Science ®Google Scholar
• Sridharan K, Sivaramakrishnan G. Growth factors for diabetic foot ulcers: mixed treatment comparison analysis of randomized clinical trials. Br J Clin Pharmacol. 2018;84(3):434–444. doi:10.1111/bcp.13470
   PubMed Web of Science ®Google Scholar
• Khanbanha N, Atyabi F, Taheri A, Talaie F, Mahbod M, Dinarvand R. Healing efficacy of an EGF impregnated triple gel based wound dressing: in vitro and in vivo studies. Biomed Res Int. 2014;2014:1–10. doi:10.1155/2014/493732
   Web of Science ®Google Scholar
• Grazul-Bilska AT, Johnson ML, Bilski JJ, et al. Wound healing: the role of growth factors. Drugs Today. 2003;39(10):787. doi:10.1358/dot.2003.39.10.799472
   PubMed Web of Science ®Google Scholar
• Bodnar RJ. Epidermal growth factor and epidermal growth factor receptor: the Yin and Yang in the treatment of cutaneous wounds and cancer. Adv Wound Care. 2013;2(1):24–29. doi:10.1089/wound.2011.0326
   Google Scholar
• Hardwicke J, Schmaljohann D, Boyce D, Thomas D. Epidermal growth factor therapy and wound healing — past, present and future perspectives. Surg. 2008;6(3):172–177. doi:10.1016/S1479-666X(08)80114-X
   Web of Science ®Google Scholar
• Tarnuzzer RW, Macauley SP, Mast BA, et al. Epidermal growth factor in wound healing: a model for the molecular pathogenesis of chronic wounds. In: Ziegler T, Pierce GF, Herndon DN, editors. Growth Factors and Wound Healing. New York: Springer; 1997:206–228. doi:10.1007/978-1-4612-1876-0_12
   Google Scholar
• Yamakawa S, Hayashida K. Advances in surgical applications of growth factors for wound healing. Burn Trauma. 2019;7. doi:10.1186/s41038-019-0148-1.
   Web of Science ®Google Scholar
• Wojtowicz AM, Oliveira S, Carlson MW, Zawadzka A, Rousseau CF, Baksh D. The importance of both fibroblasts and keratinocytes in a bilayered living cellular construct used in wound healing. Wound Repair Regen. 2014;22(2):246–255. doi:10.1111/wrr.12154
   PubMed Web of Science ®Google Scholar
• Seeger MA, Paller AS. The roles of growth factors in keratinocyte migration. Adv Wound Care. 2015;4(4):213–224. doi:10.1089/wound.2014.0540
   Web of Science ®Google Scholar
• Schultz G, Clark W, Rotatori DS. EGF and TGF-α in wound healing and repair. J Cell Biochem. 1991;45(4):346–352. doi:10.1002/jcb.240450407
   Web of Science ®Google Scholar
• Park J, Hwang S, Yoon I-S. Advanced growth factor delivery systems in wound management and skin regeneration. Molecules. 2017;22(8):1259. doi:10.3390/molecules22081259
   PubMed Web of Science ®Google Scholar
• Tsang MW, Wong WKR, Hung CS, et al. Human epidermal growth factor enhances healing of diabetic foot ulcers. Diabetes Care. 2003;26(6):1856–1861. doi:10.2337/diacare.26.6.1856
   Web of Science ®Google Scholar
• Park KH, Han SH, Hong JP, et al. Topical epidermal growth factor spray for the treatment of chronic diabetic foot ulcers: A Phase III multicenter, double-blind, randomized, placebo-controlled trial. Diabetes Res Clin Pract. 2018;142:335–344. doi:10.1016/j.diabres.2018.06.002
   PubMed Web of Science ®Google Scholar
• Zhang J, Hu W, Diao Q, et al. Therapeutic effect of the epidermal growth factor on diabetic foot ulcer and the underlying mechanisms. Exp Ther Med. 2018. doi:10.3892/etm.2018.7133
   Web of Science ®Google Scholar
• Berlanga-Acosta J, Mendoza-Mari Y, Garcia-Ojalvo A, Acosta-Buxado JA, Fernandez-Mayola M, Guillen Nieto G. Epidermal Growth Factor (EGF) intralesional infiltrations: from the bench to the diabetic ulcers cells. Integr Mol Med. 2019;6(1). doi:10.15761/IMM.1000354
   Google Scholar
• Berlanga-Acosta J, Fernández-Montequín J, Valdés-Pérez C, et al. Diabetic foot ulcers and epidermal growth factor: revisiting the local delivery route for a successful outcome. Biomed Res Int. 2017;2017:2923759. doi:10.1155/2017/2923759
   PubMed Web of Science ®Google Scholar
• Tiaka EK, Papanas N, Manolakis AC, Georgiadis GS. Epidermal growth factor in the treatment of diabetic foot ulcers: an update. Perspect Vasc Surg Endovasc Ther. 2012;24(1):37–44. doi:10.1177/1531003512442093
   PubMedGoogle Scholar
• Hong JP, Jung HD, Kim YW. Recombinant human epidermal growth factor (EGF) to enhance healing for diabetic foot ulcers. Ann Plast Surg. 2006;56(4):394–398. doi:10.1097/01.sap.0000198731.12407.0c
   PubMed Web of Science ®Google Scholar
• Singla S, Singla S, Kumar A, Singla M. Role of epidermal growth factor in healing of diabetic foot ulcers. Indian J Surg. 2012;74(6):451–455. doi:10.1007/s12262-012-0447-2
   Web of Science ®Google Scholar
• Alewood D, Nielsen K, Alewood PF, et al. The role of disulfide bonds in the structure and function of murine epidermal growth factor (mEGF). Growth Factors. 2005;23(2):97–110. doi:10.1080/08977190500096061
   PubMed Web of Science ®Google Scholar
• Chang J-Y, Schindler P, Ramseier U, Lai P-H. The disulfide folding pathway of human epidermal growth factor. J Biol Chem. 1995;270(16):9207–9216. doi:10.1074/jbc.270.16.9207
   Web of Science ®Google Scholar
• Feige MJ, Braakman I, Hendershot LM. Disulfide Bonds in Protein Folding and Stability. London: The Royal Society of Chemistry; 2018:1–33. doi:10.1039/9781788013253-00001
   Google Scholar
• Joseph BC, Pichaimuthu S, Srimeenakshi S. An overview of the parameters for recombinant protein expression in Escherichia coli. J Cell Sci Ther. 2015;6:5. doi:10.4172/2157-7013.1000221
   Google Scholar
• Okumura M, Shimamoto S, Hidaka Y. A chemical method for investigating disulfide-coupled peptide and protein folding. FEBS J. 2012;279(13):2283–2295. doi:10.1111/j.1742-4658.2012.08596.x
   PubMed Web of Science ®Google Scholar
• Landgraf BJ, Ren G, Masuch T, Boyd D, Berkmen M. From biology to biotechnology: disulfide bond formation in escherichia coli. In: Escherichia Coli - Recent Advances on Physiology, Pathogenesis and Biotechnological Applications. InTech; 2017:359–382. doi10.5772/67393
   Google Scholar
• Berkmen M. Production of disulfide-bonded proteins in Escherichia coli. Protein Expr Purif. 2012;82(1):240–251. doi:10.1016/j.pep.2011.10.009
   PubMed Web of Science ®Google Scholar
• Tyo KE, Liu Z, Petranovic D, Nielsen J. Imbalance of heterologous protein folding and disulfide bond formation rates yields runaway oxidative stress. BMC Biol. 2012;10(1):16. doi:10.1186/1741-7007-10-16
   Web of Science ®Google Scholar
• Razis AFA, Ismail EN, Hambali Z, Abdullah MNH, Ali AM, Lila MAM. The periplasmic expression of recombinant human epidermal growth factor (hEGF) in Escherichia coli. Asia-Pacific J Mol Biol Biotechnol. 2006;14(2):41–45.
   Google Scholar
• Zheng X, Wu X, Fu X, Dai D, Wang F. Expression and purification of human epidermal growth factor (hEGF) fused with GB1. Biotechnol Biotechnol Equip. 2016;30(4):813–818. doi:10.1080/13102818.2016.1166984
   Web of Science ®Google Scholar
• Indriyani A, Anggraeni NI, Maksum IP. Optimization extracellular secretion of recombinant human epidermal growth factor (hEGF) in Escherichia coli BL21 (DE3) pD881-OmpA-hEGF by using response surface method (RSM). Int J Res Pharm Sci. 2019;10(3):1824–1831. doi:10.26452/ijrps.v10i3.1378
   Google Scholar
• Abdull Razis AF, Ismail EN, Hambali Z, Abdullah MNH, Ali AM, Mohd Lila MA. Expression of recombinant human epidermal growth factor in Escherichia coli and characterization of its biological activity. Appl Biochem Biotechnol. 2008;144(3):249–261. doi:10.1007/s12010-007-8019-9
   Web of Science ®Google Scholar
• Ma Y, Yu J, Lin J, Wu S, Li S, Wang J. High efficient expression, purification, and functional characterization of native human epidermal growth factor in Escherichia coli. Biomed Res Int. 2016;2016:1–7. doi:10.1155/2016/3758941
   Web of Science ®Google Scholar
• Pouranvari S, Ebrahimi F, Javadi G, Maddah B. Cloning, expression, and cost effective purification of authentic human epidermal growth factor with high activity. Iran Red Crescent Med J. 2016;18:3. doi:10.5812/ircmj.24966
   Web of Science ®Google Scholar
• Melati R, Indriyani A, Gaffar S, Maksum IP. Comparison of extracellular secretion of recombinant human epidermal growth factor using TORA and PELB signal peptides in Escherichia coli BL21 (DE3). Asian J Pharm Clin Res. 2019;81–84. doi:10.22159/ajpcr.2019.v12i11.35316
   Google Scholar
• Sriwidodo S, Subroto T, Maksum I, et al. Optimization of secreted recombinant human epidermal growth factor production using pectate lyase B from Escherichia coli BL21(DE3) by central composite design and its production in high cell density culture. J Pharm Bioallied Sci. 2019;11(8):562. doi:10.4103/jpbs.JPBS_207_19
   Web of Science ®Google Scholar
• Maksum IP, Rostinawati NR, Subroto T. Extracellular secretion recombinant of human epidermal growth factor (hEGF) using pectate lyase B (PelB) signal peptide in Escherichia coli BL21(DE3). Int J Res Pharm Sci. 2017;8(1):33–40.
   Google Scholar
• Maksum IP, Utama E, Sriwidodo ST. Extracellular secretion of recombinant human epidermal growth factor by using trimethylamine N-Oxide reductase a (TORA) signal peptide in Escherichia coli BL21 (DE3). J Pharm Sci Res. 2017;9(6):1007–1016.
   Google Scholar
• Botusan IR, Sunkari VG, Savu O, et al. Stabilization of HIF-1α is critical to improve wound healing in diabetic mice. Proc Natl Acad Sci U S A. 2008;105(49):19426–19431. doi:10.1073/pnas.0805230105
   PubMed Web of Science ®Google Scholar
• Pratoomsoot C, Hou Q, Chau DYS, et al. A biosynthetic bandage for corneal wound repair. Abstract presented at: TERMIS-EU 2008 Porto Meeting; June 22–26; 2008; Porto Congress Center–Alfândega Portugal.
   Google Scholar
• Ginouves M, Carme B, Couppie P, Prevot G. Comparison of tetrazolium salt assays for evaluation of drug activity against leishmania spp. J Clin Microbiol. 2014;52(6):2131–2138. doi:10.1128/JCM.00201-14
   PubMed Web of Science ®Google Scholar
• Aslantürk ÖS. Vitro cytotoxicity and cell viability assays: principles, advantages, and disadvantages. In: Genotoxicity - a Predictable Risk to Our Actual World. InTech; 2018:1–17. doi10.5772/intechopen.71923
   Google Scholar
• Tiwari K, Wavdhane M, Haque S, et al. A sensitive WST-8-based bioassay for PEGylated granulocyte colony stimulating factor using the NFS-60 cell line. Pharm Biol. 2015;53(6):849–854. doi:10.3109/13880209.2014.943248
   PubMed Web of Science ®Google Scholar
• Chamchoy K, Pakotiprapha D, Pumirat P, Leartsakulpanich U, Boonyuen U. Application of WST-8 based colorimetric NAD(P)H detection for quantitative dehydrogenase assays. BMC Biochem. 2019;20(1):4. doi:10.1186/s12858-019-0108-1
   PubMed Web of Science ®Google Scholar
• Riss TL, Moravec RA, Niles AL, Benink HA, Worzlla TJ, Minor L. Cell viability assays. Assay Guid Man. 2004;1–23. doi:10.1007/978-1-61779-108-6_6
   Google Scholar
• Pastar I, Stojadinovic O, Yin NC, et al. Epithelialization in wound healing: a comprehensive review. Adv Wound Care. 2014;3(7):445–464. doi:10.1089/wound.2013.0473
   PubMedGoogle Scholar
• Grada A, Otero-Vinas M, Prieto-Castrillo F, Obagi Z, Falanga V. Research techniques made simple: analysis of collective cell migration using the wound healing assay. J Invest Dermatol. 2017;137(2):e11–e16. doi:10.1016/j.jid.2016.11.020
   PubMed Web of Science ®Google Scholar
• Yarrow JC, Perlman ZE, Westwood NJ, Mitchison TJ. A high-throughput cell migration assay using scratch wound healing, a comparison of image-based readout methods. BMC Biotechnol. 2004;4(1):21. doi:10.1186/1472-6750-4-21
   PubMed Web of Science ®Google Scholar
• Liang -C-C, Park AY, Guan J. In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc. 2007;2(2):329–333. doi:10.1038/nprot.2007.30
   PubMed Web of Science ®Google Scholar
• Cappiello F, Casciaro B, Mangoni ML. A novel in vitro wound healing assay to evaluate cell migration. J Vis Exp. 2018;133. doi:10.3791/56825.
   Web of Science ®Google Scholar
• Jonkman JEN, Cathcart JA, Xu F, et al. An introduction to the wound healing assay using live-cell microscopy. Cell Adh Migr. 2014;8(5):440–451. doi:10.4161/cam.36224
   PubMed Web of Science ®Google Scholar
• Nolte C, Kirchhoff F, Kettenmann H. Epidermal growth factor is a motility factor for microglial cells in vitro: evidence for EGF receptor expression. Eur J Neurosci. 1997;9(8):1690–1698. doi:10.1111/j.1460-9568.1997.tb01526.x
   Web of Science ®Google Scholar
• Green H, Hamerman D. Production of hyaluronate and collagen by fibroblast clones in culture. Nature. 1964;201(4920):710. doi:10.1038/201710a0
   Web of Science ®Google Scholar
• Narayanan AS, Page RC, Swanson J. Collagen synthesis by human fibroblasts. Regulation by transforming growth factor-β in the presence of other inflammatory mediators. Biochem J. 1989;260(2):463–469. doi:10.1042/bj2600463
   PubMed Web of Science ®Google Scholar
• Cole MA, Quan T, Voorhees JJ, Fisher GJ. Extracellular matrix regulation of fibroblast function: redefining our perspective on skin aging. J Cell Commun Signal. 2018;12(1):35–43. doi:10.1007/s12079-018-0459-1
   PubMed Web of Science ®Google Scholar
• Johnson KE, Wilgus TA. Vascular endothelial growth factor and angiogenesis in the regulation of cutaneous wound repair. Adv Wound Care. 2014;3(10):647–661. doi:10.1089/wound.2013.0517
   PubMedGoogle Scholar
• Kumar P, Kumar S, Udupa EP, Kumar U, Rao P, Honnegowda T. Role of angiogenesis and angiogenic factors in acute and chronic wound healing. Plast Aesthetic Res. 2015;2(5):243. doi:10.4103/2347-9264.165438
   Google Scholar
• Ucuzian AA, Gassman AA, East AT, Greisler HP. Molecular mediators of angiogenesis. J Burn Care Res. 2010;31(1):158–175. doi:10.1097/BCR.0b013e3181c7ed82
   PubMed Web of Science ®Google Scholar
• Sorg H, Tilkorn DJ, Mirastschijski U, Hauser J, Kraemer R. Panta Rhei: neovascularization, angiogenesis and nutritive perfusion in wound healing. Eur Surg Res. 2018;59(3–4):232–241. doi:10.1159/000492410
   Web of Science ®Google Scholar
• Pfeiffer, H. Reinhard B. Dettmeyer. Forensic Histopathology: Fundamentals and Perspectives. Int J Legal Med. 2012;126:185. doi:10.1007/s00414-011-0645-7
   Google Scholar
• Rutland CS. Histological and histochemical methods 4th edition. J Anat. 2008;213(3):356. doi:10.1111/j.1469-7580.2008.00957.x
   Google Scholar
• Petreaca M, Martins-Green M. Cell–ECM interactions in repair and regeneration. Lanza R, Atala A, editors. In: Handbook of Stem Cells. Elsevier; 2013:191–226. doi:10.1016/B978-0-12-385942-6.00017-2
   Google Scholar