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Silk Fibroin in Wound Healing Process

  • Md. Tipu Sultan
  • Ok Joo Lee
  • Soon Hee Kim
  • Hyung Woo Ju
  • Chan Hum ParkEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1077)

Abstract

Silk fibroin (SF), a natural bioproduct, has been extensively used in biological and biomedical fields including wound healing due to its robust biocompatibility, less immunogenic, non-toxic, non-carcinogenic, and biodegradable properties. SF in different morphologic forms, such as hydrogels, sponges, films, electrospun nanofiber mats, and hydrocolloid dressings, have been successfully used for therapeutic use as wound dressings to induce the healing process. SF has also been known to promote wound healing by increasing the cell growth, proliferation, and migration of different cells types involved in the different phase of wound healing process. In this review, we summarize the different morphologic forms of SF that have been used in the treatment of various wound healing process. We also discuss the effect of SF on various cells types during the SF-induced healing process. Furthermore, we highlight molecular signaling aspects of the SF-induced healing process.

Keywords

Silk fibroin Shape Wound healing Wound dressings Signaling pathways 

Notes

Acknowledgements

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIP; grant No.: NRF-2016R1E1A1A01942120), by the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, South Korea (grant No.: HI17C1229), and Hallym University research fund.

References

  1. 1.
    Abdel-Naby W et al (2017) Treatment with solubilized Silk-Derived Protein (SDP) enhances rabbit corneal epithelial wound healing. PLoS One 12:e0188154.  https://doi.org/10.1371/journal.pone.0188154 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Akturk O et al (2016) Wet electrospun silk fibroin/gold nanoparticle 3D matrices for wound healing applications. RSC Adv 6:13234–13250.  https://doi.org/10.1039/c5ra24225h CrossRefGoogle Scholar
  3. 3.
    Altman GH et al (2003) Silk-based biomaterials. Biomaterials 24:401–416CrossRefGoogle Scholar
  4. 4.
    Aykac A, Karanlik B, Sehirli AO (2018) Protective effect of silk fibroin in burn injury in rat model. Gene 641:287–291.  https://doi.org/10.1016/j.gene.2017.10.036 CrossRefPubMedGoogle Scholar
  5. 5.
    Aytemiz D et al (2013) Small-diameter silk vascular grafts (3 mm diameter) with a double-raschel knitted silk tube coated with silk fibroin sponge. Adv Healthcare Mater 2:361–368.  https://doi.org/10.1002/adhm.201200227 CrossRefGoogle Scholar
  6. 6.
    Bao P, Kodra A, Tomic-Canic M, Golinko MS, Ehrlich HP, Brem H (2009) The role of vascular endothelial growth factor in wound healing. J Surg Res 153:347–358.  https://doi.org/10.1016/j.jss.2008.04.023 CrossRefGoogle Scholar
  7. 7.
    Bini E, Foo CW, Huang J, Karageorgiou V, Kitchel B, Kaplan DL (2006) RGD-functionalized bioengineered spider dragline silk biomaterial. Biomacromolecules 7:3139–3145.  https://doi.org/10.1021/bm0607877 CrossRefPubMedGoogle Scholar
  8. 8.
    Bouhadir KH, Lee KY, Alsberg E, Damm KL, Anderson KW, Mooney DJ (2001) Degradation of partially oxidized alginate and its potential application for tissue engineering. Biotechnol Prog 17:945–950.  https://doi.org/10.1021/bp010070p CrossRefPubMedGoogle Scholar
  9. 9.
    Burdick JA, Prestwich GD (2011) Hyaluronic acid hydrogels for biomedical applications. Adv Mater 23:H41–H56.  https://doi.org/10.1002/adma.201003963 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Chen J et al (2003) Human bone marrow stromal cell and ligament fibroblast responses on RGD-modified silk fibers. J Biomed Mater Res A 67:559–570.  https://doi.org/10.1002/jbm.a.10120 CrossRefPubMedGoogle Scholar
  11. 11.
    Chen J, Chen Y, Yang Z, You B, Ruan YC, Peng Y (2016) Epidermal CFTR suppresses MAPK/NF-kappaB to promote cutaneous. Wound Healing Cell Physiol Biochem 39:2262–2274.  https://doi.org/10.1159/000447919 CrossRefPubMedGoogle Scholar
  12. 12.
    Cheng F, Shen Y, Mohanasundaram P, Lindstrom M, Ivaska J, Ny T, Eriksson JE (2016) Vimentin coordinates fibroblast proliferation and keratinocyte differentiation in wound healing via TGF-beta-Slug signaling. Proc Natl Acad Sci U S A 113:E4320–E4327.  https://doi.org/10.1073/pnas.1519197113 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Chiarini A, Petrini P, Bozzini S, Dal Pra I, Armato U (2003) Silk fibroin/poly(carbonate)-urethane as a substrate for cell growth: in vitro interactions with human cells. Biomaterials 24:789–799CrossRefGoogle Scholar
  14. 14.
    Chung EJ, Ju HW, Park HJ, Park CH (2015) Three-layered scaffolds for artificial esophagus using poly(varepsilon-caprolactone) nanofibers and silk fibroin: an experimental study in a rat model. J Biomed Mater Res A 103:2057–2065.  https://doi.org/10.1002/jbm.a.35347 CrossRefPubMedGoogle Scholar
  15. 15.
    Chutipakdeevong J, Ruktanonchai UR, Supaphol P (2013) Process optimization of electrospun silk fibroin fiber mat for accelerated wound healing. J Appl Polym Sci 130:3634–3644.  https://doi.org/10.1002/app.39611 CrossRefGoogle Scholar
  16. 16.
    Drury JL, Mooney DJ (2003) Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 24:4337–4351CrossRefGoogle Scholar
  17. 17.
    Eming SA, Martin P, Tomic-Canic M (2014) Wound repair and regeneration: mechanisms, signaling, and translation. Sci Transl Med 6:265sr266.  https://doi.org/10.1126/scitranslmed.3009337 CrossRefGoogle Scholar
  18. 18.
    Falanga V (2005) Wound healing and its impairment in the diabetic foot. Lancet 366:1736–1743.  https://doi.org/10.1016/S0140-6736(05)67700-8 CrossRefPubMedGoogle Scholar
  19. 19.
    Fan S, Zhang Y, Shao H, Hu X (2013) Electrospun regenerated silk fibroin mats with enhanced mechanical properties. Int J Biol Macromol 56:83–88.  https://doi.org/10.1016/j.ijbiomac.2013.01.033 CrossRefPubMedGoogle Scholar
  20. 20.
    Fini M et al (2005) The healing of confined critical size cancellous defects in the presence of silk fibroin hydrogel. Biomaterials 26:3527–3536 doi:S0142-9612(04)00869-5 [pii].  https://doi.org/10.1016/j.biomaterials.2004.09.040 CrossRefPubMedGoogle Scholar
  21. 21.
    Forrest L (1983) Current concepts in soft connective tissue wound healing. Br J Surg 70:133–140CrossRefGoogle Scholar
  22. 22.
    Fu SC, Chau YP, Lu KS, Kung HN (2011) beta-lapachone accelerates the recovery of burn-wound skin. Histol Histopathol 26:905-914 doi:10.14670/HH-26.905Google Scholar
  23. 23.
    Gil ES, Hudson SM (2007) Effect of silk fibroin interpenetrating networks on swelling/deswelling kinetics and rheological properties of poly(N-isopropylacrylamide) hydrogels. Biomacromolecules 8:258–264.  https://doi.org/10.1021/bm060543m CrossRefPubMedGoogle Scholar
  24. 24.
    Gonzalez AC, Costa TF, Andrade ZA, Medrado AR (2016) Wound healing – a literature review. An Bras Dermatol 91:614–620 doi:S0365-05962016000500614 [pii].  https://doi.org/10.1590/abd1806-4841.20164741 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Grinnell F, Ho CH, Wysocki A (1992) Degradation of fibronectin and vitronectin in chronic wound fluid: analysis by cell blotting, immunoblotting, and cell adhesion assays. J Invest Dermatol 98:410–416 doi:S0022-202X(92)91008-W [pii]CrossRefGoogle Scholar
  26. 26.
    Guo S, Dipietro LA (2010) Factors affecting wound healing. J Dent Res 89:219–229 doi:0022034509359125 [pii].  https://doi.org/10.1177/0022034509359125 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Gurtner GC, Werner S, Barrandon Y, Longaker MT (2008) Wound repair and regeneration. Nature 453:314–321 doi:nature07039 [pii].  https://doi.org/10.1038/nature07039 CrossRefGoogle Scholar
  28. 28.
    Haas AF, Wong JW, Iwahashi CK, Halliwell B, Cross CE, Davis PA (1998) Redox regulation of wound healing? NF-kappaB activation in cultured human keratinocytes upon wounding and the effect of low energy HeNe irradiation. Free Radic Biol Med 25:998–1005 doi:S0891-5849(98)00135-X [pii]CrossRefGoogle Scholar
  29. 29.
    Heo SC, Jeon ES, Lee IH, Kim HS, Kim MB, Kim JH (2011) Tumor necrosis factor-alpha-activated human adipose tissue-derived mesenchymal stem cells accelerate cutaneous wound healing through paracrine mechanisms. J Invest Dermatol 131:1559–1567 doi:S0022-202X(15)35324-0 [pii].  https://doi.org/10.1038/jid.2011.64 CrossRefPubMedGoogle Scholar
  30. 30.
    Hersel U, Dahmen C, Kessler H (2003) RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials 24:4385–4415CrossRefGoogle Scholar
  31. 31.
    Irrera N et al (2015) Epoetin alpha and epoetin zeta: a comparative study on stimulation of angiogenesis and wound repair in an experimental model of burn. Injury Biomed Res Int 2015:968927.  https://doi.org/10.1155/2015/968927 CrossRefPubMedGoogle Scholar
  32. 32.
    Jin HJ, Fridrikh SV, Rutledge GC, Kaplan DL (2002) Electrospinning Bombyx mori silk with poly(ethylene oxide). Biomacromolecules 3:1233–1239CrossRefGoogle Scholar
  33. 33.
    Ju HW et al (2016) Wound healing effect of electrospun silk fibroin nanomatrix in burn-model. Int J Biol Macromol 85:29–39 doi:S0141-8130(15)30243-9 [pii].  https://doi.org/10.1016/j.ijbiomac.2015.12.055 CrossRefPubMedGoogle Scholar
  34. 34.
    Ju HW et al (2014) Silk fibroin based hydrogel for regeneration of burn induced wounds. Tissue Eng Regen Med 11:203–210.  https://doi.org/10.1007/s13770-014-0010-2 CrossRefGoogle Scholar
  35. 35.
    Kamoun EA, Kenawy ES, Chen X (2017) A review on polymeric hydrogel membranes for wound dressing applications: PVA-based hydrogel dressings. J Adv Res 8:217–233.  https://doi.org/10.1016/j.jare.2017.01.005S2090-1232(17)30024-3 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Kapoor S, Kundu SC (2016) Silk protein-based hydrogels: promising advanced materials for biomedical applications. Acta Biomater 31:17–32 doi:S1742-7061(15)30210-5 [pii].  https://doi.org/10.1016/j.actbio.2015.11.034 CrossRefPubMedGoogle Scholar
  37. 37.
    Kawakami M, Tomita N, Shimada Y, Yamamoto K, Tamada Y, Kachi N, Suguro T (2011) Chondrocyte distribution and cartilage regeneration in silk fibroin sponge. Biomed Mater Eng 21:53–61.  https://doi.org/10.3233/BME-2011-0656 CrossRefPubMedGoogle Scholar
  38. 38.
    Kim HJ, Kim UJ, Vunjak-Novakovic G, Min BH, Kaplan DL (2005a) Influence of macroporous protein scaffolds on bone tissue engineering from bone marrow stem cells. Biomaterials 26:4442–4452 doi:S0142-9612(04)00993-7 [pii].  https://doi.org/10.1016/j.biomaterials.2004.11.013 CrossRefPubMedGoogle Scholar
  39. 39.
    Kim JH et al (2016a) Osteoinductive silk fibroin/titanium dioxide/hydroxyapatite hybrid scaffold for bone tissue engineering. Int J Biol Macromol 82:160–167 doi:S0141-8130(15)00535-8 [pii].  https://doi.org/10.1016/j.ijbiomac.2015.08.001 CrossRefPubMedGoogle Scholar
  40. 40.
    Kim KH et al (2005b) Biological efficacy of silk fibroin nanofiber membranes for guided bone regeneration. J Biotechnol 120:327–339.  https://doi.org/10.1016/j.jbiotec.2005.06.033 CrossRefPubMedGoogle Scholar
  41. 41.
    Kim SH et al (2016b) Fabrication of duck's feet collagen-silk hybrid biomaterial for tissue engineering. Int J Biol Macromol 85:442–450 doi:S0141-8130(15)30273-7 [pii].  https://doi.org/10.1016/j.ijbiomac.2015.12.086 CrossRefPubMedGoogle Scholar
  42. 42.
    Kim UJ, Park J, Li C, Jin HJ, Valluzzi R, Kaplan DL (2004) Structure and properties of silk hydrogels. Biomacromolecules 5:786–792.  https://doi.org/10.1021/bm0345460 CrossRefPubMedGoogle Scholar
  43. 43.
    Kimura T, Yamada H, Tsubouchi K, Doi K (2007) Accelerating effects of silk fibroin on wound healing in hairless descendants of mexican hairless dogs. J Appl Sci Res 3:1306–1314Google Scholar
  44. 44.
    Konrad D, Tsunoda M, Weber K, Corney SJ, Ullmann L (2002) Effects of a topical silver sulfadiazine polyurethane dressing (Mikacure) on wound healing in experimentally infected wounds in the pig. A pilot study. J Exp Animal Sci 42:31–43.  https://doi.org/10.1016/S0939-8600(02)80004-9 CrossRefGoogle Scholar
  45. 45.
    Lee JM, Sultan MT, Kim SH, Kumar V, Yeon YK, Lee OJ, Park CH (2017) Artificial auricular cartilage using silk fibroin and polyvinyl alcohol hydrogel. Int J Mol Sci 18 doi:ijms18081707 [pii].  https://doi.org/10.3390/ijms18081707
  46. 46.
    Lee MS, Seo SR, Kim JC (2012) A beta-cyclodextrin, polyethyleneimine and silk fibroin hydrogel containing Centella asiatica extract and hydrocortisone acetate: releasing properties and in vivo efficacy for healing of pressure sores. Clin Exp Dermatol 37:762–771.  https://doi.org/10.1111/j.1365-2230.2011.04331.x CrossRefPubMedGoogle Scholar
  47. 47.
    Lee OJ et al (2014) Development of artificial dermis using 3D electrospun silk fibroin nanofiber matrix. J Biomed Nanotechnol 10:1294–1303CrossRefGoogle Scholar
  48. 48.
    Lee OJ et al (2016) Fabrication and characterization of hydrocolloid dressing with silk fibroin nanoparticles for wound healing. Tissue Engineering and Regenerative Medicine 13:218–226.  https://doi.org/10.1007/s13770-016-9058-5 CrossRefGoogle Scholar
  49. 49.
    Liu H, Fan H, Wang Y, Toh SL, Goh JC (2008) The interaction between a combined knitted silk scaffold and microporous silk sponge with human mesenchymal stem cells for ligament tissue engineering. Biomaterials 29:662–674.  https://doi.org/10.1016/j.biomaterials.2007.10.035 CrossRefPubMedGoogle Scholar
  50. 50.
    Liu NG, Chen YJ, Huang XH (2002) Expression of EIIIA-fibronectin in injured rat skin used in estimation of wound interval. Fa Yi Xue Za Zhi 18:129–131PubMedGoogle Scholar
  51. 51.
    Makaya K, Terada S, Ohgo K, Asakura T (2009) Comparative study of silk fibroin porous scaffolds derived from salt/water and sucrose/hexafluoroisopropanol in cartilage formation. J Biosci Bioeng 108:68–75 doi:S1389-1723(09)00134-0 [pii].  https://doi.org/10.1016/j.jbiosc.2009.02.015 CrossRefPubMedGoogle Scholar
  52. 52.
    Martinez-Mora C, Mrowiec A, Garcia-Vizcaino EM, Alcaraz A, Cenis JL, Nicolas FJ (2012) Fibroin and sericin from Bombyx mori silk stimulate cell migration through upregulation and phosphorylation of c-Jun. PLoS One 7:e42271.  https://doi.org/10.1371/journal.pone.0042271 PONE-D-12-08826 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Midwood KS, Williams LV, Schwarzbauer JE (2004) Tissue repair and the dynamics of the extracellular matrix. Int J Biochem Cell Biol 36:1031–1037.  https://doi.org/10.1016/j.biocel.2003.12.003 S1357272503004291 [pii]CrossRefGoogle Scholar
  54. 54.
    Min BM, Lee G, Kim SH, Nam YS, Lee TS, Park WH (2004) Electrospinning of silk fibroin nanofibers and its effect on the adhesion and spreading of normal human keratinocytes and fibroblasts in vitro. Biomaterials 25:1289–1297CrossRefGoogle Scholar
  55. 55.
    Moon BM et al (2017) Novel fabrication method of the peritoneal dialysis filter using silk fibroin with urease fixation system. J Biomed Mater Res B Appl Biomater 105:2136–2144.  https://doi.org/10.1002/jbm.b.33751 CrossRefPubMedGoogle Scholar
  56. 56.
    Murakami K et al (2010) Hydrogel blends of chitin/chitosan, fucoidan and alginate as healing-impaired wound dressings. Biomaterials 31:83–90 doi:S0142-9612(09)00961-2 [pii].  https://doi.org/10.1016/j.biomaterials.2009.09.031 CrossRefPubMedGoogle Scholar
  57. 57.
    Mutsaers SE, Bishop JE, McGrouther G, Laurent GJ (1997) Mechanisms of tissue repair: from wound healing to fibrosis. Int J Biochem Cell Biol 29:5–17 doi:S135727259600115X [pii]CrossRefGoogle Scholar
  58. 58.
    Nam YS, Yoon JJ, Park TG (2000) A novel fabrication method of macroporous biodegradable polymer scaffolds using gas foaming salt as a porogen additive. J Biomed Mater Res 53:1–7.  https://doi.org/10.1002/(SICI)1097-4636(2000)53:1<1::AID-JBM1>3.0.CO;2-R [pii]CrossRefPubMedGoogle Scholar
  59. 59.
    Niiyama H, Kuroyanagi Y (2014) Development of novel wound dressing composed of hyaluronic acid and collagen sponge containing epidermal growth factor and vitamin C derivative. J Artif Organs 17:81–87.  https://doi.org/10.1007/s10047-013-0737-x CrossRefPubMedGoogle Scholar
  60. 60.
    Nishida A, Yamada M, Kanazawa T, Takashima Y, Ouchi K, Okada H (2010) Use of silk protein, sericin, as a sustained-release material in the form of a gel, sponge and film. Chem Pharm Bull 58:1480–1486CrossRefGoogle Scholar
  61. 61.
    Olczyk P, Komosinska-Vassev K, Wisowski G, Mencner L, Stojko J, Kozma EM (2014) Propolis modulates fibronectin expression in the matrix of thermal injury. Biomed Res Int 2014:748101.  https://doi.org/10.1155/2014/748101 CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Omenetto FG, Kaplan DL (2010) New opportunities for an ancient material. Science 329:528–531. doi:329/5991/528 [pii] 10.1126/science.1188936CrossRefGoogle Scholar
  63. 63.
    Ong SY, Wu J, Moochhala SM, Tan MH, Lu J (2008) Development of a chitosan-based wound dressing with improved hemostatic and antimicrobial properties. Biomaterials 29:4323–4332 doi:S0142-9612(08)00512-7 [pii].  https://doi.org/10.1016/j.biomaterials.2008.07.034 CrossRefPubMedGoogle Scholar
  64. 64.
    Ota S et al (2011) Intramuscular transplantation of muscle-derived stem cells accelerates skeletal muscle healing after contusion injury via enhancement of angiogenesis. Am J Sports Med 39:1912–1922 doi:0363546511415239 [pii].  https://doi.org/10.1177/0363546511415239 CrossRefPubMedGoogle Scholar
  65. 65.
    Padol AR, Jayakumar K, Shridhar NB, Narayana Swamy HD, Narayana Swamy M, Mohan K (2011) Safety evaluation of silk protein film (a novel wound healing agent) in terms of acute dermal toxicity, acute dermal irritation and skin sensitization. Toxicol Int 18:17–21.  https://doi.org/10.4103/0971-6580.75847 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Park HJ et al (2015) Fabrication of 3D porous silk scaffolds by particulate (salt/sucrose) leaching for bone tissue reconstruction. Int J Biol Macromol 78:215–223 doi:S0141-8130(15)00216-0 [pii].  https://doi.org/10.1016/j.ijbiomac.2015.03.064 CrossRefPubMedGoogle Scholar
  67. 67.
    Park YR et al (2016) Three-dimensional electrospun silk-fibroin nanofiber for skin tissue engineering. Int J Biol Macromol 93:1567–1574 doi:S0141-8130(16)30867-4 [pii].  https://doi.org/10.1016/j.ijbiomac.2016.07.047 CrossRefPubMedGoogle Scholar
  68. 68.
    Park YR et al (2017) NF-kappaB signaling is key in the wound healing processes of silk fibroin. Acta Biomater doi:S1742-7061(17)30762-6 [pii].  https://doi.org/10.1016/j.actbio.2017.12.006
  69. 69.
    Petrini P, Parolari C, Tanzi MC (2001) Silk fibroin-polyurethane scaffolds for tissue engineering. J Mater Sci Mater Med 12:849–853 doi:381126 [pii]CrossRefGoogle Scholar
  70. 70.
    Powell HM, Supp DM, Boyce ST (2008) Influence of electrospun collagen on wound contraction of engineered skin substitutes. Biomaterials 29:834–843 doi:S0142-9612(07)00858-7 [pii].  https://doi.org/10.1016/j.biomaterials.2007.10.036 CrossRefPubMedGoogle Scholar
  71. 71.
    Rajan V, Murray RZ (2008) The duplicitous nature of inflammation in wound repair. Wound Practice Res 16:122–129Google Scholar
  72. 72.
    Ribeiro M, de Moraes MA, Beppu MM, Monteiro FJ, Ferraz MP (2014) The role of dialysis and freezing on structural conformation, thermal properties and morphology of silk fibroin hydrogels. Biomatter 4:e28536.  https://doi.org/10.4161/biom.28536 CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Rivard A et al (1999) Rescue of diabetes-related impairment of angiogenesis by intramuscular gene therapy with adeno-VEGF. Am J Pathol 154:355–363 doi:S0002-9440(10)65282-0 [pii].  https://doi.org/10.1016/S0002-9440(10)65282-0 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Roh D-H et al (2006a) Wound healing effect of silk fibroin/alginate-blended sponge in full thickness skin defect of rat. J Mater Sci Mater Med 17:547–552.  https://doi.org/10.1007/s10856-006-8938-y CrossRefPubMedGoogle Scholar
  75. 75.
    Roh DH et al (2006b) Wound healing effect of silk fibroin/alginate-blended sponge in full thickness skin defect of rat. J Mater Sci Mater Med 17:547–552.  https://doi.org/10.1007/s10856-006-8938-y CrossRefPubMedGoogle Scholar
  76. 76.
    Schneider A, Wang XY, Kaplan DL, Garlick JA, Egles C (2009) Biofunctionalized electrospun silk mats as a topical bioactive dressing for accelerated wound healing. Acta Biomater 5:2570–2578 doi:S1742-7061(08)00405-4 [pii].  https://doi.org/10.1016/j.actbio.2008.12.013 CrossRefPubMedGoogle Scholar
  77. 77.
    Seah CC, Phillips TJ, Howard CE, Panova IP, Hayes CM, Asandra AS, Park HY (2005) Chronic wound fluid suppresses proliferation of dermal fibroblasts through a Ras-mediated signaling pathway. J Invest Dermatol 124:466–474 doi:S0022-202X(15)32153-9 [pii].  https://doi.org/10.1111/j.0022-202X.2004.23557.x CrossRefPubMedGoogle Scholar
  78. 78.
    Seaman S (2002) Dressing selection in chronic wound management. J Am Podiatr Med Assoc 92:24–33CrossRefGoogle Scholar
  79. 79.
    Sheikh FA et al (2015) 3D electrospun silk fibroin nanofibers for fabrication of artificial skin. Nanomedicine 11:681–691 doi:S1549-9634(14)00571-1 [pii].  https://doi.org/10.1016/j.nano.2014.11.007 CrossRefPubMedGoogle Scholar
  80. 80.
    Sheikh FA et al (2014) A comparative mechanical and biocompatibility study of poly(ε-caprolactone), hybrid poly(ε-caprolactone)–silk, and silk nanofibers by colloidal electrospinning technique for tissue engineering. J Bioact Compat Polym 29:500–514.  https://doi.org/10.1177/0883911514549717 CrossRefGoogle Scholar
  81. 81.
    Shen W, Chen X, Chen J, Yin Z, Heng BC, Chen W, Ouyang HW (2010) The effect of incorporation of exogenous stromal cell-derived factor-1 alpha within a knitted silk-collagen sponge scaffold on tendon regeneration. Biomaterials 31:7239–7249.  https://doi.org/10.1016/j.biomaterials.2010.05.040 CrossRefGoogle Scholar
  82. 82.
    Shi Y et al (2015) Wnt and Notch signaling pathway involved in wound healing by targeting c-Myc and Hes1 separately. Stem Cell Res Ther 6:120 doi:10.1186/s13287-015-0103-4 10.1186/s13287-015-0103-4 [pii]CrossRefGoogle Scholar
  83. 83.
    Singer AJ, Clark RA (1999) Cutaneous wound healing. N Engl J Med 341:738–746.  https://doi.org/10.1056/NEJM199909023411006 CrossRefGoogle Scholar
  84. 84.
    Srivastava CM, Purwar R, Kannaujia R, Sharma D (2015) Flexible silk fibroin films for wound dressing. Fibers Polym 16:1020–1030.  https://doi.org/10.1007/s12221-015-1020-y CrossRefGoogle Scholar
  85. 85.
    Stadelmann WK, Digenis AG, Tobin GR (1998) Physiology and healing dynamics of chronic cutaneous wounds. Am J Surg 176:26S–38SCrossRefGoogle Scholar
  86. 86.
    Sugihara A et al (2000) Promotive effects of a silk film on epidermal recovery from full-thickness skin wounds. Proc Soc Exp Biol Med 225:58–64 doi:pse22507 [pii]CrossRefGoogle Scholar
  87. 87.
    Sultan MT et al (2017) Fabrication and characterization of the porous duck's feet collagen sponge for wound healing applications. J Biomater Sci Polym Ed:1–12.  https://doi.org/10.1080/09205063.2017.1367636 CrossRefGoogle Scholar
  88. 88.
    Szabowski A, Maas-Szabowski N, Andrecht S, Kolbus A, Schorpp-Kistner M, Fusenig NE, Angel P (2000) c-Jun and JunB antagonistically control cytokine-regulated mesenchymal-epidermal interaction in skin. Cell 103:745–755 doi:S0092-8674(00)00178-1 [pii]CrossRefGoogle Scholar
  89. 89.
    Thangavel P, Ramachandran B, Kannan R, Muthuvijayan V (2017) Biomimetic hydrogel loaded with silk and l-proline for tissue engineering and wound healing applications. J Biomed Mater Res B Appl Biomater 105:1401–1408.  https://doi.org/10.1002/jbm.b.33675 CrossRefPubMedGoogle Scholar
  90. 90.
    Thuraisingam T et al (2010) MAPKAPK-2 signaling is critical for cutaneous wound healing. J Invest Dermatol 130:278–286 doi:S0022-202X(15)34516-4 [pii].  https://doi.org/10.1038/jid.2009.209 CrossRefPubMedGoogle Scholar
  91. 91.
    Unger RE, Peters K, Wolf M, Motta A, Migliaresi C, Kirkpatrick CJ (2004) Endothelialization of a non-woven silk fibroin net for use in tissue engineering: growth and gene regulation of human endothelial cells. Biomaterials 25:5137–5146.  https://doi.org/10.1016/j.biomaterials.2003.12.040 S0142961203011670 [pii]CrossRefPubMedGoogle Scholar
  92. 92.
    Uppal R, Ramaswamy GN, Arnold C, Goodband R, Wang Y (2011) Hyaluronic acid nanofiber wound dressing–production, characterization, and in vivo behavior. J Biomed Mater Res B Appl Biomater 97:20–29.  https://doi.org/10.1002/jbm.b.31776 CrossRefPubMedGoogle Scholar
  93. 93.
    Vassallo IM, Formosa C (2015) Comparing calcium alginate dressings to vacuum-assisted closure: a clinical trial. Wounds 27:180–190PubMedGoogle Scholar
  94. 94.
    Verma V, Verma P, Kar S, Ray P, Ray AR (2007) Fabrication of agar-gelatin hybrid scaffolds using a novel entrapment method for in vitro tissue engineering applications. Biotechnol Bioeng 96:392–400.  https://doi.org/10.1002/bit.21111 CrossRefPubMedGoogle Scholar
  95. 95.
    Wang L, Wu X, Shi T, Lu L (2013) Epidermal growth factor (EGF)-induced corneal epithelial wound healing through nuclear factor kappaB subtype-regulated CCCTC binding factor (CTCF) activation. J Biol Chem 288:24363–24371 doi:M113.458141 [pii].  https://doi.org/10.1074/jbc.M113.458141 CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Werner S, Grose R (2003) Regulation of wound healing by growth factors and cytokines. Physiol Rev 83:835–870.  https://doi.org/10.1152/physrev.00031.200283/3/835 [pii]CrossRefPubMedGoogle Scholar
  97. 97.
    Wharram SE, Zhang X, Kaplan DL, McCarthy SP (2010) Electrospun silk material systems for wound healing. Macromol Biosci 10:246–257.  https://doi.org/10.1002/mabi.200900274 CrossRefPubMedGoogle Scholar
  98. 98.
    Wyatt D, McGowan DN, Najarian MP (1990) Comparison of a hydrocolloid dressing and silver sulfadiazine cream in the outpatient management of second-degree burns. J Trauma 30:857–865CrossRefGoogle Scholar
  99. 99.
    Wysocki AB, Grinnell F (1990) Fibronectin profiles in normal and chronic wound fluid. Lab Investig 63:825–831PubMedGoogle Scholar
  100. 100.
    Xia Q et al (2004) A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306:1937–1940 doi:306/5703/1937 [pii] 10.1126/science.1102210CrossRefGoogle Scholar
  101. 101.
    Xing W et al (2015) Acemannan accelerates cell proliferation and skin wound healing through AKT/mTOR signaling pathway. J Dermatol Sci 79:101–109 doi:S0923-1811(15)00116-4 [pii] 10.1016/j.jdermsci.2015.03.016CrossRefGoogle Scholar
  102. 102.
    Yamada H, Igarashi Y, Takasu Y, Saito H, Tsubouchi K (2004) Identification of fibroin-derived peptides enhancing the proliferation of cultured human skin fibroblasts. Biomaterials 25:467–472 doi:S0142961203005404 [pii]CrossRefGoogle Scholar
  103. 103.
    Yan LP, Oliveira JM, Oliveira AL, Caridade SG, Mano JF, Reis RL (2012) Macro/microporous silk fibroin scaffolds with potential for articular cartilage and meniscus tissue engineering applications. Acta Biomater 8:289–301 doi:S1742-7061(11)00430-2 [pii] 10.1016/j.actbio.2011.09.037CrossRefGoogle Scholar
  104. 104.
    Yoon JJ, Park TG (2001) Degradation behaviors of biodegradable macroporous scaffolds prepared by gas foaming of effervescent salts. J Biomed Mater Res 55:401–408 doi:10.1002/1097-4636(20010605)55:3<401::AID-JBM1029>3.0.CO;2-H [pii]CrossRefGoogle Scholar
  105. 105.
    Zhang W et al (2017) Silk fibroin biomaterial shows safe and effective wound healing in animal models and a randomized controlled clinical Trial. Adv Healthc Mater:6.  https://doi.org/10.1002/adhm.201700121 CrossRefGoogle Scholar
  106. 106.
    Zhang X, Cao C, Ma X, Li Y (2012) Optimization of macroporous 3-D silk fibroin scaffolds by salt-leaching procedure in organic solvent-free conditions. J Mater Sci Mater Med 23:315–324.  https://doi.org/10.1007/s10856-011-4476-3 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Md. Tipu Sultan
    • 1
  • Ok Joo Lee
    • 1
  • Soon Hee Kim
    • 1
  • Hyung Woo Ju
    • 1
  • Chan Hum Park
    • 1
    • 2
    Email author
  1. 1.Nano-Bio Regenerative Medical Institute, College of MedicineHallym UniversityChuncheonSouth Korea
  2. 2.Department of Otorhinolaryngology-Head and Neck Surgery, Chuncheon Sacred Heart HospitalHallym University College of MedicineChuncheonSouth Korea

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