Controlled release of vascular endothelial growth factor (VEGF) in alginate and hyaluronic acid (ALG–HA) bead system to promote wound healing in punch-induced wound rat model

References

• Kang BS, Na YC, Jin YW. Comparison of the wound healing effect of cellulose and gelatin: an in vivo study. Arch Plast Surg. 2012;39(4):317–321.
   PubMedGoogle Scholar
• Koh TJ, DiPietro LA. Inflammation and wound healing: the role of the macrophage. Expert Rev Mol Med. 2011;13:E23.
   PubMed Web of Science ®Google Scholar
• Mohiti Asli M, Saha S, Murphy S, et al. Ibuprofen loaded PLA nanofibrous scaffolds increase proliferation of human skin cells in vitro and promote healing of full thickness incision wounds in vivo. J Biomed Mater Res B Appl Biomater. 2017;105(2):327–339.
   PubMed Web of Science ®Google Scholar
• Shaw TJ, Martin P. Wound repair at a glance. J Cell Sci. 2009;122(Pt 18):3209–3213.
   PubMed Web of Science ®Google Scholar
• Eming SA, Krieg T, Davidson JM. Inflammation in wound repair: molecular and cellular mechanisms. J Invest Dermatol. 2007;127(3):514–525.
   PubMed Web of Science ®Google Scholar
• Kumar V. Robbins & cotran-patologia bases patológicas das doenças. 8th ed. Brasil: Elsevier; 2010.
   Google Scholar
• Gethin G, Probst S, Stryja J, et al. Evidence for person-centred care in chronic wound care: a systematic review and recommendations for practice. J Wound Care. 2020;29(Sup9b):S1–S22.
   PubMedGoogle Scholar
• Edwards JV, Yager DR, Cohen IK, et al. Modified cotton gauze dressings that selectively absorb neutrophil elastase activity in solution. Wound Repair Regen. 2001;9(1):50–58.
   PubMed Web of Science ®Google Scholar
• Kamoun EA, Kenawy E-RS, Chen X. A review on polymeric hydrogel membranes for wound dressing applications: PVA-based hydrogel dressings. J Adv Res. 2017;8(3):217–233.
   PubMed Web of Science ®Google Scholar
• Razzak M, Dewi S, Lely H, et al. The characterization of dressing component materials and radiation formation of PVA–PVP hydrogel. Radiat Phys Chem. 1999;55(2):153–165.
   Web of Science ®Google Scholar
• Li Y, Jiang H, Zheng W, et al. Bacterial cellulose–hyaluronan nanocomposite biomaterials as wound dressings for severe skin injury repair. J Mater Chem B. 2015;3(17):3498–3507.
   PubMed Web of Science ®Google Scholar
• Zahedi P, Rezaeian I, Ranaei Siadat SO, et al. A review on wound dressings with an emphasis on electrospun nanofibrous polymeric bandages. Polym Adv Technol. 2010;21(2):77–95.
   Web of Science ®Google Scholar
• Zubair M, Ahmad J. Role of growth factors and cytokines in diabetic foot ulcer healing: a detailed review. Rev Endocr Metab Disord. 2019;20(2):207–217.
   PubMed Web of Science ®Google Scholar
• Hinnis AR. The tumour suppressor p53 and apoptotic regulatory proteins in breast cancer survival and response to therapy. Leicester, UK: University of Leicester; 2005.
   Google Scholar
• Ehrenreich M, Ruszczak Z. Tissue-engineered temporary wound coverings. Important options for the clinician. Acta Dermatovenerol Alp Panon Adriat. 2006;15(1):5.
   PubMedGoogle Scholar
• Smith D, McHugh T, Phillips LG, et al. Biosynthetic compound dressings—management of hand burns. Burns Incl Therm Inj. 1988;14(5):405–408.
   PubMedGoogle Scholar
• Williams DF. Challenges with the development of biomaterials for sustainable tissue engineering. Front Bioeng Biotechnol. 2019;7:127.
   PubMed Web of Science ®Google Scholar
• Ali M, Payne SL. Biomaterial-based cell delivery strategies to promote liver regeneration. Biomater Res. 2021;25(1):5–21.
   PubMedGoogle Scholar
• Wang P, Song Y, Weir MD, et al. A self-setting iPSMSC-alginate-calcium phosphate paste for bone tissue engineering. Dent Mater. 2016;32(2):252–263.
   PubMed Web of Science ®Google Scholar
• Amirian J, Van TTT, Bae S-H, et al. Examination of in vitro and in vivo biocompatibility of alginate-hyaluronic acid microbeads as a promising method in cell delivery for kidney regeneration. Int J Biol Macromol. 2017;105(Pt 1):143–153.
   PubMedGoogle Scholar
• Taz M, Makkar P, Imran KM, et al. Bone regeneration of multichannel biphasic calcium phosphate granules supplemented with hyaluronic acid. Mater Sci Eng C Mater Biol Appl. 2019;99:1058–1066.
   PubMed Web of Science ®Google Scholar
• Senger DR, Galli SJ, Dvorak AM, et al. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science. 1983;219(4587):983–985.
   PubMed Web of Science ®Google Scholar
• Senger DR, Connolly DT, Van De Water L, et al. Purification and NH2-terminal amino acid sequence of guinea pig tumor-secreted vascular permeability factor. Cancer Res. 1990;50(6):1774–1778.
   PubMed Web of Science ®Google Scholar
• Brkovic A, Sirois MG. Vascular permeability induced by VEGF family members in vivo: role of endogenous PAF and NO synthesis. J Cell Biochem. 2007;100(3):727–737.
   PubMed Web of Science ®Google Scholar
• Yamagishi S, Yonekura H, Yamamoto Y, et al. Vascular endothelial growth factor acts as a pericyte mitogen under hypoxic conditions. Lab Invest. 1999;79(4):501–509.
   PubMed Web of Science ®Google Scholar
• Yoshida A, Anand-Apte B, Zetter BR. Differential endothelial migration and proliferation to basic fibroblast growth factor and vascular endothelial growth factor. Growth Factors. 1996;13(1-2):57–64.
   PubMed Web of Science ®Google Scholar
• Noiri E, Lee E, Testa J, et al. Podokinesis in endothelial cell migration: role of nitric oxide. Am J Physiol. 1998;274(1):C236–44C244.
   PubMedGoogle Scholar
• Tischer E, Mitchell R, Hartman T, et al. The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J Biol Chem. 1991;266(18):11947–11954.
   PubMed Web of Science ®Google Scholar
• Houck KA, Ferrara N, Winer J, et al. The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol Endocrinol. 1991;5(12):1806–1814.
   PubMed Web of Science ®Google Scholar
• Houck KA, Leung D, Rowland A, et al. Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J Biol Chem. 1992;267(36):26031–26037.
   PubMed Web of Science ®Google Scholar
• Poltorak Z, Cohen T, Sivan R, et al. VEGF145, a secreted vascular endothelial growth factor isoform that binds to extracellular matrix. J Biol Chem. 1997;272(11):7151–7158.
   PubMed Web of Science ®Google Scholar
• Stojadinovic O. A novel non-angiogenic mechanism of VEGF: Stimulation of keratinocyte and fibroblast migration. Wound Repair Regen. 2007;15:A30.
   Web of Science ®Google Scholar
• Lindenhayn K, Perka C, Spitzer RS, et al. Retention of hyaluronic acid in alginate beads: aspects for in vitro cartilage engineering. J Biomed Mater Res. 1999;44(2):149–155.
   PubMed Web of Science ®Google Scholar
• Rajaram A, Schreyer DJ, Chen DX. Use of the polycation polyethyleneimine to improve the physical properties of alginate–hyaluronic acid hydrogel during fabrication of tissue repair scaffolds. J Biomater Sci Polym Ed. 2015;26(7):433–445.
   PubMed Web of Science ®Google Scholar
• Amirian J, Makkar P, Lee GH, et al. Incorporation of alginate-hyaluronic acid microbeads in injectable calcium phosphate cement for improved bone regeneration. Mater Lett. 2020;272:127830.
   Web of Science ®Google Scholar
• Tanaka H, Matsumura M, Veliky IA. Diffusion characteristics of substrates in Ca‐alginate gel beads. Biotechnol Bioeng. 1984;26(1):53–58.
   PubMed Web of Science ®Google Scholar
• Won K, Kim S, Kim K-J, et al. Optimization of lipase entrapment in Ca-alginate gel beads. Process Biochem. 2005;40(6):2149–2154.
   Web of Science ®Google Scholar
• Hu Y, Zheng M, Dong X, et al. Preparation and characterization of alginate-hyaluronic acid-chitosan based composite gel beads. J Wuhan Univ Technol Mater Sci Ed. 2015;30(6):1297–1303.
   Web of Science ®Google Scholar
• Moya ML, Cheng M-H, Huang J-J, et al. The effect of FGF-1 loaded alginate microbeads on neovascularization and adipogenesis in a vascular pedicle model of adipose tissue engineering. Biomaterials. 2010;31(10):2816–2826.
   PubMed Web of Science ®Google Scholar
• Corstens MN, Berton-Carabin CC, Elichiry-Ortiz PT, et al. Emulsion-alginate beads designed to control in vitro intestinal lipolysis: towards appetite control. J Funct Foods. 2017;34:319–328.
   Web of Science ®Google Scholar
• Salehi M, Ehterami A, Farzamfar S, et al. Accelerating healing of excisional wound with alginate hydrogel containing naringenin in rat model. Drug Deliv Transl Res. 2021;11(1):142–153.
   PubMed Web of Science ®Google Scholar
• Kurowiak J, Kaczmarek-Pawelska A, Mackiewicz AG, et al. Analysis of the degradation process of alginate-based hydrogels in artificial urine for use as a bioresorbable material in the treatment of urethral injuries. Processes. 2020;8(3):304.
   Web of Science ®Google Scholar
• Singh A, Kar AK, Singh D, et al. pH-responsive eco-friendly chitosan modified cenosphere/alginate composite hydrogel beads as carrier for controlled release of imidacloprid towards sustainable pest control. Chem Eng J. 2022;427:131215.
   Web of Science ®Google Scholar
• Dave V, Yadav RB, Kushwaha K, et al. Lipid-polymer hybrid nanoparticles: development & statistical optimization of norfloxacin for topical drug delivery system. Bioact Mater. 2017;2(4):269–280.
   PubMed Web of Science ®Google Scholar
• Aprilliza M. Characterization and properties of sodium alginate from brown algae used as an ecofriendly superabsorbent. IOP Conf Ser Mater Sci Eng. 2017;188(1):012019.
   Google Scholar
• Liu Q, Li Q, Xu S, et al. Preparation and properties of 3D printed alginate–chitosan polyion complex hydrogels for tissue engineering. Polymers. 2018;10(6):664.
   PubMed Web of Science ®Google Scholar
• He S, Shi D, Han Z, et al. Heparinized silk fibroin hydrogels loading FGF1 promote the wound healing in rats with full-thickness skin excision. BioMed Eng OnLine. 2019;18(1):1–12.
   PubMed Web of Science ®Google Scholar
• Peng Y, He D, Ge X, et al. Construction of heparin-based hydrogel incorporated with Cu5.4O ultrasmall nanozymes for wound healing and inflammation inhibition. Bioact Mater. 2021;6(10):3109–3124.
   PubMed Web of Science ®Google Scholar
• Chen L, He Z, Chen B, et al. Loading of VEGF to the heparin cross-linked demineralized bone matrix improves vascularization of the scaffold. J Mater Sci Mater Med. 2010;21(1):309–317. [Mismatch
   PubMed Web of Science ®Google Scholar
• Pike DB, Cai S, Pomraning KR, et al. Heparin-regulated release of growth factors in vitro and angiogenic response in vivo to implanted hyaluronan hydrogels containing VEGF and bFGF. Biomaterials. 2006;27(30):5242–5251.
   PubMed Web of Science ®Google Scholar
• MacLauchlan S, Yu J, Parrish M, et al. Endothelial nitric oxide synthase controls the expression of the angiogenesis inhibitor thrombospondin 2. Proc Natl Acad Sci USA. 2011;108(46):E1137–45E1145.
   PubMed Web of Science ®Google Scholar
• Zeng Z, Huang WD, Gao Q, et al. Arnebin-1 promotes angiogenesis by inducing eNOS, VEGF and HIF-1α expression through the PI3K-dependent pathway. Int J Mol Med. 2015;36(3):685–697.
   PubMed Web of Science ®Google Scholar
• Cavender DE. Lymphocyte adhesion to endothelial cells in vitro: models for the study of normal lymphocyte recirculation and lymphocyte emigration into chronic inflammatory lesions. J Invest Dermatol. 1989;93(2):S88–S95.
   Web of Science ®Google Scholar
• Shimizu Y, Newman W, Tanaka Y, et al. Lymphocyte interactions with endothelial cells. Immunol Today. 1992;13(3):106–112.
   PubMedGoogle Scholar
• Kang H-J, Park S-S, Saleh T, et al. In vitro and in vivo evaluation of Ca/P-hyaluronic acid/gelatin based novel dental plugs for one-step socket preservation. Mater Des. 2020;194:108891.
   Web of Science ®Google Scholar
• Dumont M, Villet R, Guirand M, et al. Processing and antibacterial properties of chitosan-coated alginate fibers. Carbohydr Polym. 2018;190:31–42.
   PubMed Web of Science ®Google Scholar
• Benavides S, Villalobos-Carvajal R, Reyes J. Physical, mechanical and antibacterial properties of alginate film: Effect of the crosslinking degree and oregano essential oil concentration. J Food Eng. 2012;110(2):232–239.
   Web of Science ®Google Scholar
• Elçin YM, Dixit V, Gitnick G. Extensive in vivo angiogenesis following controlled release of human vascular endothelial cell growth factor: implications for tissue engineering and wound healing. Artif Organs. 2001;25(7):558–565.
   PubMed Web of Science ®Google Scholar
• Tellechea A, Silva EA, Min J, et al. Alginate and DNA gels are suitable delivery systems for diabetic wound healing. Int J Low Extrem Wounds. 2015;14(2):146–153.
   PubMed Web of Science ®Google Scholar
• Peters MC, Isenberg BC, Rowley JA, et al. Release from alginate enhances the biological activity of vascular endothelial growth factor. J Biomater Sci Polym Ed. 1998;9(12):1267–1278.
   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.
   PubMedGoogle Scholar
• Nogami M, Hoshi T, Kinoshita M, et al. Vascular endothelial growth factor expression in rat skin incision wound. Med Mol Morphol. 2007;40(2):82–87.
   PubMed Web of Science ®Google Scholar
• Han Y-F, Han Y-Q, Pan Y-G, et al. Transplantation of microencapsulated cells expressing VEGF improves angiogenesis in implanted xenogeneic acellular dermis on wound. Transplantation Proceedings. 2010;42(5):1935–1943.
   PubMed Web of Science ®Google Scholar
• Chen Z, Zhao L, Zhao F, et al. Tetrandrine suppresses lung cancer growth and induces apoptosis, potentially via the VEGF/HIF-1α/ICAM-1 signaling pathway. Oncol Lett. 2018;15(5):7433–7437.
   PubMed Web of Science ®Google Scholar
• Yang X, Luo LX, Guo M, et al. Tubeimoside I promotes angiogenesis via activation of eNOS-VEGF signaling pathway. J Ethnopharmacol. 2021;267:113642.
   PubMed Web of Science ®Google Scholar
• Ratanavaraporn J, Chuma N, Kanokpanont S, et al. Beads fabricated from alginate, hyaluronic acid, and gelatin using ionic crosslinking and layer‐by‐layer coating techniques for controlled release of gentamicin. J Appl Polym Sci. 2019;136(1):46893.
   Web of Science ®Google Scholar
• Chou K-C, Chen C-T, Cherng J-H, et al. Cutaneous regeneration mechanism of β-Sheet silk fibroin in a rat burn wound healing model. Polymers. 2021;13(20):3537.
   PubMed Web of Science ®Google Scholar
• Larjava H, Koivisto L, Häkkinen L. Keratinocyte interactions with fibronectin during wound healing. Madame Curie Bioscience Database. [Internet]. Landes Bioscience; 2013.
   Google Scholar
• Li W, Fan J, Chen M, et al. Mechanism of human dermal fibroblast migration driven by type I collagen and platelet-derived growth factor-BB. Mol Biol Cell. 2004;15(1):294–309.
   PubMed Web of Science ®Google Scholar