Tissue Engineering and Regenerative Medicine

, Volume 14, Issue 6, pp 699–718 | Cite as

Electrospun Collagen Nanofibers and Their Applications in Skin Tissue Engineering

  • Jia Xian Law
  • Ling Ling Liau
  • Aminuddin Saim
  • Ying Yang
  • Ruszymah Idrus
Review Article
  • 164 Downloads

Abstract

Electrospinning is a simple and versatile technique to fabricate continuous fibers with diameter ranging from micrometers to a few nanometers. To date, the number of polymers that have been electrospun has exceeded 200. In recent years, electrospinning has become one of the most popular scaffold fabrication techniques to prepare nanofiber mesh for tissue engineering applications. Collagen, the most abundant extracellular matrix protein in the human body, has been electrospun to fabricate biomimetic scaffolds that imitate the architecture of native human tissues. As collagen nanofibers are mechanically weak in nature, it is commonly cross-linked or blended with synthetic polymers to improve the mechanical strength without compromising the biological activity. Electrospun collagen nanofiber mesh has high surface area to volume ratio, tunable diameter and porosity, and excellent biological activity to regulate cell function and tissue formation. Due to these advantages, collagen nanofibers have been tested for the regeneration of a myriad of tissues and organs. In this review, we gave an overview of electrospinning, encompassing the history, the instrument settings, the spinning process and the parameters that affect fiber formation, with emphasis given to collagen nanofibers’ fabrication and application, especially the use of collagen nanofibers in skin tissue engineering.

Keywords

Electrospinning Collagen Skin Tissue engineering Nanofiber Scaffold 

Notes

Authors’ contributions

All the authors participate in drafting the article and revising it critically for important intellectual content. All the authors give final approval of the version to be published.

Compliance with ethical standards

Conflict of interest

The authors have no financial conflicts of interest.

Ethical statement

There is no animal experimental carried out for this article.

Supplementary material

13770_2017_75_MOESM1_ESM.docx (15 kb)
Supplementary material 1 (DOCX 15 kb)
13770_2017_75_MOESM2_ESM.docx (30 kb)
Supplementary material 2 (DOCX 29 kb)

References

  1. 1.
    Tam J, Wang Y, Farinelli WA, Jiménez-Lozano J, Franco W, Sakamoto FH, et al. Fractional skin harvesting: autologous skin grafting without donor-site morbidity. Plast Reconstr Surg Glob Open. 2013;1:e47.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Langer R, Vacanti J. Tissue engineering. Science. 1993;260:920–6.PubMedCrossRefGoogle Scholar
  3. 3.
    O’brien FJ. Biomaterials & scaffolds for tissue engineering. Mater Today. 2011;14:88–95.CrossRefGoogle Scholar
  4. 4.
    Law JX, Musa F, Ruszymah BHI, El Haj AJ, Yang Y. A comparative study of skin cell activities in collagen and fibrin constructs. Med Eng Phys. 2016;38:854–61.PubMedCrossRefGoogle Scholar
  5. 5.
    Maarof M, Law JX, Chowdhury SR, Khairoji KA, Saim AB, Idrus RBH. Secretion of wound healing mediators by single and bi-layer skin substitutes. Cytotechnology. 2016;68:1873–84.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Xian LJ, Chowdhury SR, Saim AB, Idrus RBH. Concentration-dependent effect of platelet-rich plasma on keratinocyte and fibroblast wound healing. Cytotherapy. 2015;17:293–300.PubMedCrossRefGoogle Scholar
  7. 7.
    Law JX, Chowdhury SR, Saim AB, Idrus RBH. Platelet-rich plasma with keratinocytes and fibroblasts enhance healing of full-thickness wounds. J Tissue Viability. 2017;26:208–15.PubMedCrossRefGoogle Scholar
  8. 8.
    Chan B, Leong K. Scaffolding in tissue engineering: general approaches and tissue-specific considerations. Eur Spine J. 2008;17:467–79.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Maghsoudlou P, Georgiades F, Smith H, Milan A, Shangaris P, Urbani L, et al. Optimization of liver decellularization maintains extracellular matrix micro-architecture and composition predisposing to effective cell seeding. PLoS ONE. 2016;11:e0155324.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Caralt M, Uzarski JS, Iacob S, Obergfell KP, Berg N, Bijonowski BM, et al. Optimization and critical evaluation of decellularization strategies to develop renal extracellular matrix scaffolds as biological templates for organ engineering and transplantation. Am J Transplant. 2015;15:64–75.PubMedCrossRefGoogle Scholar
  11. 11.
    Shevchenko RV, James SL, James SE. A review of tissue-engineered skin bioconstructs available for skin reconstruction. J R Soc Interface. 2010;7:229–58.PubMedCrossRefGoogle Scholar
  12. 12.
    Macneil S. Progress and opportunities for tissue-engineered skin. Nature. 2007;445:874–80.PubMedCrossRefGoogle Scholar
  13. 13.
    Parenteau-Bareil R, Gauvin R, Berthod F. Collagen-based biomaterials for tissue engineering applications. Materials. 2010;3:1863–87.PubMedCentralCrossRefGoogle Scholar
  14. 14.
    Tseng AA, Notargiacomo A, Chen T. Nanofabrication by scanning probe microscope lithography: a review. J Vac Sci Technol B. 2005;23:877–94.CrossRefGoogle Scholar
  15. 15.
    He B, Yuan X, Jiang D. Molecular self-assembly guides the fabrication of peptide nanofiber scaffolds for nerve repair. RSC Adv. 2014;4:23610–21.CrossRefGoogle Scholar
  16. 16.
    Nada AA, James R, Shelke NB, Harmon MD, Awad HM, Nagarale RK, et al. A smart methodology to fabricate electrospun chitosan nanofiber matrices for regenerative engineering applications. Polym Adv Technol. 2014;25:507–15.CrossRefGoogle Scholar
  17. 17.
    Ramakrishna S, Fujihara K, Teo WE, Yong T, Ma Z, Ramaseshan R. Electrospun nanofibers: solving global issues. Mater Today. 2006;9:40–50.CrossRefGoogle Scholar
  18. 18.
    Garg K, Bowlin GL. Electrospinning jets and nanofibrous structures. Biomicrofluidics. 2011;5:13403.PubMedCrossRefGoogle Scholar
  19. 19.
    Rayleigh LXX. On the equilibrium of liquid conducting masses charged with electricity. Philos Mag. 1882;14:184–6.CrossRefGoogle Scholar
  20. 20.
    Zeleny J. The electrical discharge from liquid points, and a hydrostatic method of measuring the electric intensity at their surfaces. Phys Rev. 1914;3:69–91.CrossRefGoogle Scholar
  21. 21.
    Anton F. Process and apparatus for preparing artificial threads. US Patent 1,975,504; 1934.Google Scholar
  22. 22.
    Anton F. Artificial thread and method of producing same. US Patent 2,187,306; 1940.Google Scholar
  23. 23.
    Anton F. Production of artificial fibers from fiber forming liquids. US Patent 2,323,025; 1943.Google Scholar
  24. 24.
    Norton CL. Method of and apparatus for producing fibrous or filamentary material. US Patent 2,048,651; 1936.Google Scholar
  25. 25.
    Taylor G. Electrically driven jets. Presented at: Proc R Soc Lond A; 1969. doi:10.1098/rspa.1969.0205.
  26. 26.
    Baumgarten PK. Electrostatic spinning of acrylic microfibers. J Colloid Interface Sci. 1971;36:71–9.CrossRefGoogle Scholar
  27. 27.
    Larrondo L, John Manley R. Electrostatic fiber spinning from polymer melts. I. Experimental observations on fiber formation and properties. J Polym Sci Part B Polym Phys. 1981;19:909–20.CrossRefGoogle Scholar
  28. 28.
    Reneker DH, Yarin AL, Fong H, Koombhongse S. Bending instability of electrically charged liquid jets of polymer solutions in electrospinning. J Appl Phys. 2000;87:4531–47.CrossRefGoogle Scholar
  29. 29.
    Yarin AL, Koombhongse S, Reneker DH. Bending instability in electrospinning of nanofibers. J Appl Phys. 2001;89:3018–26.CrossRefGoogle Scholar
  30. 30.
    Hohman MM, Shin M, Rutledge G, Brenner MP. Electrospinning and electrically forced jets. I. Stability theory. Phys Fluids. 2001;13:2201–20.CrossRefGoogle Scholar
  31. 31.
    Annis D, Bornat A, Edwards R, Higham A, Loveday B, Wilson J. An elastomeric vascular prosthesis. ASAIO J. 1978;24:209–14.Google Scholar
  32. 32.
    Fisher A, De Cossart L, How T, Annis D. Long term in vivo performance of an electrostatically-spun small bore arterial prosthesis: the contribution of mechanical compliance and anti-platelet therapy. Life Support Syst. 1985;3:462–5.PubMedGoogle Scholar
  33. 33.
    Bhardwaj N, Kundu SC. Electrospinning: a fascinating fiber fabrication technique. Biotechnol Adv. 2010;28:325–47.PubMedCrossRefGoogle Scholar
  34. 34.
    Huang ZM, Zhang YZ, Kotaki M, Ramakrishna S. A review on polymer nanofibers by electrospinning and their applications in nanocomposites. Compos Sci Technol. 2003;63:2223–53.CrossRefGoogle Scholar
  35. 35.
    Ru C, Wang F, Pang M, Sun L, Chen R, Sun Y. Suspended, shrinkage-free, electrospun PLGA nanofibrous scaffold for skin tissue engineering. ACS Appl Mater Interfaces. 2015;7:10872–7.PubMedCrossRefGoogle Scholar
  36. 36.
    Uyar T, Besenbacher F. Electrospinning of uniform polystyrene fibers: the effect of solvent conductivity. Polymer. 2008;49:5336–43.CrossRefGoogle Scholar
  37. 37.
    Kim SJ, Lee CK, Kim SI. Effect of ionic salts on the processing of poly(2-acrylamido-2-methyl-1-propane sulfonic acid) nanofibers. J Appl Polym Sci. 2005;96:1388–93.CrossRefGoogle Scholar
  38. 38.
    Yang Y, Wimpenny I, Ahearne M. Portable nanofiber meshes dictate cell orientation throughout three-dimensional hydrogels. Nanomedicine. 2011;7:131–6.PubMedCrossRefGoogle Scholar
  39. 39.
    Weightman A, Jenkins S, Pickard M, Chari D, Yang Y. Alignment of multiple glial cell populations in 3D nanofiber scaffolds: toward the development of multicellular implantable scaffolds for repair of neural injury. Nanomedicine. 2014;10:291–5.PubMedCrossRefGoogle Scholar
  40. 40.
    Kim HS, Kim K, Jin HJ, Chin IJ. Morphological characterization of electrospun nano-fibrous membranes of biodegradable poly(l-lactide) and poly(lactide-co-glycolide). Presented at: Macromolecular Symposia; 2005. doi:10.1002/masy.200550613.
  41. 41.
    Liu H, Hsieh YL. Ultrafine fibrous cellulose membranes from electrospinning of cellulose acetate. J Polym Sci Part B Polym Phys. 2002;40:2119–29.CrossRefGoogle Scholar
  42. 42.
    Sun Z, Zussman E, Yarin AL, Wendorff JH, Greiner A. Compound core–shell polymer nanofibers by co-electrospinning. Adv Mater. 2003;15:1929–32.CrossRefGoogle Scholar
  43. 43.
    Li D, Babel A, Jenekhe SA, Xia Y. Nanofibers of conjugated polymers prepared by electrospinning with a two-capillary spinneret. Adv Mater. 2004;16:2062–6.CrossRefGoogle Scholar
  44. 44.
    Wang M, Yu JH, Kaplan DL, Rutledge GC. Production of submicron diameter silk fibers under benign processing conditions by two-fluid electrospinning. Macromolecules. 2006;39:1102–7.CrossRefGoogle Scholar
  45. 45.
    Yu D, Branford-White C, White K, Chatterton N, Zhu L, Huang L, et al. A modified coaxial electrospinning for preparing fibers from a high concentration polymer solution. Express Polym Lett. 2011;5:732–41.CrossRefGoogle Scholar
  46. 46.
    Han D, Steckl AJ. Triaxial electrospun nanofiber membranes for controlled dual release of functional molecules. ACS Appl Mater Interfaces. 2013;5:8241–5.PubMedCrossRefGoogle Scholar
  47. 47.
    Yu DG, Li XY, Wang X, Yang JH, Bligh SA, Williams GR. Nanofibers fabricated using triaxial electrospinning as zero order drug delivery systems. ACS Appl Mater Interfaces. 2015;7:18891–7.PubMedCrossRefGoogle Scholar
  48. 48.
    Li D, Xia Y. Direct fabrication of composite and ceramic hollow nanofibers by electrospinning. Nano Lett. 2004;4:933–8.CrossRefGoogle Scholar
  49. 49.
    Pakravan M, Heuzey M-C, Ajji A. Core–shell structured PEO-chitosan nanofibers by coaxial electrospinning. Biomacromolecules. 2012;13:412–21.PubMedCrossRefGoogle Scholar
  50. 50.
    Zhang X, Aravindan V, Kumar PS, Liu H, Sundaramurthy J, Ramakrishna S, et al. Synthesis of TiO2 hollow nanofibers by co-axial electrospinning and its superior lithium storage capability in full-cell assembly with olivine phosphate. Nanoscale. 2013;5:5973–80.PubMedCrossRefGoogle Scholar
  51. 51.
    Mccann JT, Li D, Xia Y. Electrospinning of nanofibers with core–sheath, hollow, or porous structures. J Mater Chem. 2005;15:735–8.CrossRefGoogle Scholar
  52. 52.
    Yu JH, Fridrikh SV, Rutledge GC. Production of submicrometer diameter fibers by two-fluid electrospinning. Adv Mater. 2004;16:1562–6.CrossRefGoogle Scholar
  53. 53.
    Zhang Y, Huang ZM, Xu X, Lim CT, Ramakrishna S. Preparation of core–shell structured PCL-r-gelatin bi-component nanofibers by coaxial electrospinning. Chem Mater. 2004;16:3406–9.CrossRefGoogle Scholar
  54. 54.
    Sun B, Duan B, Yuan X. Preparation of core/shell PVP/PLA ultrafine fibers by coaxial electrospinning. J Appl Polym Sci. 2006;102:39–45.CrossRefGoogle Scholar
  55. 55.
    Mickova A, Buzgo M, Benada O, Rampichova M, Fisar Z, Filova E, et al. Core/shell nanofibers with embedded liposomes as a drug delivery system. Biomacromolecules. 2012;13:952–62.PubMedCrossRefGoogle Scholar
  56. 56.
    Maleki M, Latifi M, Amani-Tehran M, Mathur S. Electrospun core–shell nanofibers for drug encapsulation and sustained release. Polym Eng Sci. 2013;53:1770–9.CrossRefGoogle Scholar
  57. 57.
    Lee GH, Song JC, Yoon KB. Controlled wall thickness and porosity of polymeric hollow nanofibers by coaxial electrospinning. Macromol Res. 2010;18:571–6.CrossRefGoogle Scholar
  58. 58.
    Megelski S, Stephens JS, Chase DB, Rabolt JF. Micro-and nanostructured surface morphology on electrospun polymer fibers. Macromolecules. 2002;35:8456–66.CrossRefGoogle Scholar
  59. 59.
    Casper CL, Stephens JS, Tassi NG, Chase DB, Rabolt JF. Controlling surface morphology of electrospun polystyrene fibers: effect of humidity and molecular weight in the electrospinning process. Macromolecules. 2004;37:573–8.CrossRefGoogle Scholar
  60. 60.
    Vaz C, Van Tuijl S, Bouten C, Baaijens F. Design of scaffolds for blood vessel tissue engineering using a multi-layering electrospinning technique. Acta Biomater. 2005;1:575–82.PubMedCrossRefGoogle Scholar
  61. 61.
    Zeugolis D, Li B, Lareu RR, Chan C, Raghunath M. Collagen solubility testing, a quality assurance step for reproducible electro-spun nano-fibre fabrication. A technical note. J Biomater Sci Polym Ed. 2008;19:1307–17.PubMedCrossRefGoogle Scholar
  62. 62.
    Shoulders MD, Raines RT. Collagen structure and stability. Annu Rev Biochem. 2009;78:929–58.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Gorgieva S, Kokol V, editors Collagen-vs. gelatine-based biomaterials and their biocompatibility: review and perspectives. InTech; 2011.Google Scholar
  64. 64.
    Kadler K, Holmes D, Trotter J, Chapman J. Collagen fibril formation. Biochem J. 1996;316:1–11.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Myllyharju J, Kivirikko KI. Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 2004;20:33–43.PubMedCrossRefGoogle Scholar
  66. 66.
    Pamela C, Richard A, Denise R, editors. Lippincotts illustrated reviews biochemistry. Philadelphia: Lippincott Williams and Wilkins; 2005.Google Scholar
  67. 67.
    Welgus HG, Jeffrey JJ, Eisen AZ. The collagen substrate specificity of human skin fibroblast collagenase. J Biol Chem. 1981;256:9511–5.PubMedGoogle Scholar
  68. 68.
    Lamers E, Van Horssen R, Te Riet J, Van Delft F, Luttge R, Walboomers X, et al. The influence of nanoscale topographical cues on initial osteoblast morphology and migration. Eur Cell Mater. 2010;20:329–43.PubMedCrossRefGoogle Scholar
  69. 69.
    Angele P, Abke J, Kujat R, Faltermeier H, Schumann D, Nerlich M, et al. Influence of different collagen species on physico-chemical properties of crosslinked collagen matrices. Biomaterials. 2004;25:2831–41.PubMedCrossRefGoogle Scholar
  70. 70.
    Lin YK, Liu DC. Comparison of physical-chemical properties of type I collagen from different species. Food Chem. 2006;99:244–51.CrossRefGoogle Scholar
  71. 71.
    An B, Kaplan DL, Brodsky B. Engineered recombinant bacterial collagen as an alternative collagen-based biomaterial for tissue engineering. Front Chem. 2014;2:40.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Wahl D, Czernuszka J. Collagen–hydroxyapatite composites for hard tissue repair. Eur Cell Mater. 2006;11:43–56.PubMedCrossRefGoogle Scholar
  73. 73.
    Nair LS, Laurencin CT. Biodegradable polymers as biomaterials. Prog Polym Sci. 2007;32:762–98.CrossRefGoogle Scholar
  74. 74.
    Powell HM, Supp DM, Boyce ST. Influence of electrospun collagen on wound contraction of engineered skin substitutes. Biomaterials. 2008;29:834–43.PubMedCrossRefGoogle Scholar
  75. 75.
    Hofman K, Tucker N, Stanger J, Staiger M, Marshall S, Hall B. Effects of the molecular format of collagen on characteristics of electrospun fibres. J Mater Sci. 2012;47:1148–55.CrossRefGoogle Scholar
  76. 76.
    Zhou G, Zhang G, Wu Z, Hou Y, Yan M, Liu H, et al. Research on the structure of fish collagen nanofibers influenced cell growth. J Nanomater. 2013. doi:10.1155/2013/764239.Google Scholar
  77. 77.
    Elamparithi A, Punnoose AM, Kuruvilla S. Electrospun type 1 collagen matrices preserving native ultrastructure using benign binary solvent for cardiac tissue engineering. Artif Cells Nanomed Biotechnol. 2016;44:1318–25.PubMedGoogle Scholar
  78. 78.
    Choi SM, Kang HY, Min HJ, Lee R, Ikram M, Subhan F, et al. Bioactive fish collagen/polycaprolactone composite nanofibrous scaffolds fabricated by electrospinning for 3D cell culture. J Biotechnol. 2015;205:47–58.PubMedCrossRefGoogle Scholar
  79. 79.
    Willard JJ, Drexler JW, Das A, Roy S, Shilo S, Shoseyov O, et al. Plant-derived human collagen scaffolds for skin tissue engineering. Tissue Eng Part A. 2013;19:1507–18.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Matthews JA, Wnek GE, Simpson DG, Bowlin GL. Electrospinning of collagen nanofibers. Biomacromolecules. 2002;3:232–8.PubMedCrossRefGoogle Scholar
  81. 81.
    Zeugolis DI, Khew ST, Yew ES, Ekaputra AK, Tong YW, Yung L-YL, et al. Electro-spinning of pure collagen nano-fibres—just an expensive way to make gelatin? Biomaterials. 2008;29:2293–305.PubMedCrossRefGoogle Scholar
  82. 82.
    Yang L, Fitie CF, Van Der Werf KO, Bennink ML, Dijkstra PJ, Feijen J. Mechanical properties of single electrospun collagen type I fibers. Biomaterials. 2008;29:955–62.PubMedCrossRefGoogle Scholar
  83. 83.
    Liu T, Teng WK, Chan BP, Chew SY. Photochemical crosslinked electrospun collagen nanofibers: synthesis, characterization and neural stem cell interactions. J Biomed Mater Res A. 2010;95:276–82.PubMedCrossRefGoogle Scholar
  84. 84.
    Telemeco T, Ayres C, Bowlin G, Wnek G, Boland E, Cohen N, et al. Regulation of cellular infiltration into tissue engineering scaffolds composed of submicron diameter fibrils produced by electrospinning. Acta Biomater. 2005;1:377–85.PubMedCrossRefGoogle Scholar
  85. 85.
    Jha BS, Ayres CE, Bowman JR, Telemeco TA, Sell SA, Bowlin GL, et al. Electrospun collagen: a tissue engineering scaffold with unique functional properties in a wide variety of applications. J Nanomater. 2011. doi:10.1155/2011/348268.Google Scholar
  86. 86.
    Dong B, Arnoult O, Smith ME, Wnek GE. Electrospinning of collagen nanofiber scaffolds from benign solvents. Macromol Rapid Commun. 2009;30:539–42.PubMedCrossRefGoogle Scholar
  87. 87.
    Baek J, Sovani S, Glembotski NE, Du J, Jin S, Grogan SP, et al. Repair of avascular meniscus tears with electrospun collagen scaffolds seeded with human cells. Tissue Eng Part A. 2016;22:436–48.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Rho KS, Jeong L, Lee G, Seo BM, Park YJ, Hong SD, et al. Electrospinning of collagen nanofibers: effects on the behavior of normal human keratinocytes and early-stage wound healing. Biomaterials. 2006;27:1452–61.PubMedCrossRefGoogle Scholar
  89. 89.
    Buttafoco L, Kolkman N, Engbers-Buijtenhuijs P, Poot A, Dijkstra P, Vermes I, et al. Electrospinning of collagen and elastin for tissue engineering applications. Biomaterials. 2006;27:724–34.PubMedCrossRefGoogle Scholar
  90. 90.
    Olde Damink L, Dijkstra P, Van Luyn M, Van Wachem P, Nieuwenhuis P, Feijen J. Cross-linking of dermal sheep collagen using a water-soluble carbodiimide. Biomaterials. 1996;17:765–73.PubMedCrossRefGoogle Scholar
  91. 91.
    Sundararaghavan HG, Monteiro GA, Lapin NA, Chabal YJ, Miksan JR, Shreiber DI. Genipin-induced changes in collagen gels: correlation of mechanical properties to fluorescence. J Biomed Mater Res A. 2008;87:308–20.PubMedCrossRefGoogle Scholar
  92. 92.
    Tian Z, Wu K, Liu W, Shen L, Li G. Two-dimensional infrared spectroscopic study on the thermally induced structural changes of glutaraldehyde-crosslinked collagen. Spectrochim Acta A Mol Biomol Spectrosc. 2015;140:356–63.PubMedCrossRefGoogle Scholar
  93. 93.
    Chau D, Collighan RJ, Verderio EA, Addy VL, Griffin M. The cellular response to transglutaminase-cross-linked collagen. Biomaterials. 2005;26:6518–29.PubMedCrossRefGoogle Scholar
  94. 94.
    Jus S, Stachel I, Schloegl W, Pretzler M, Friess W, Meyer M, et al. Cross-linking of collagen with laccases and tyrosinases. Mater Sci Eng C. 2011;31:1068–77.CrossRefGoogle Scholar
  95. 95.
    Weadock KS, Miller EJ, Bellincampi LD, Zawadsky JP, Dunn MG. Physical crosslinking of collagen fibers: comparison of ultraviolet irradiation and dehydrothermal treatment. J Biomed Mater Res. 1995;29:1373–9.PubMedCrossRefGoogle Scholar
  96. 96.
    Inoue N, Bessho M, Furuta M, Kojima T, Okuda S, Hara M. A novel collagen hydrogel cross-linked by gamma-ray irradiation in acidic pH conditions. J Biomater Sci Polym Ed. 2006;17:837–58.PubMedCrossRefGoogle Scholar
  97. 97.
    Charulatha V, Rajaram A. Influence of different crosslinking treatments on the physical properties of collagen membranes. Biomaterials. 2003;24:759–67.PubMedCrossRefGoogle Scholar
  98. 98.
    Ratanavaraporn J, Rangkupan R, Jeeratawatchai H, Kanokpanont S, Damrongsakkul S. Influences of physical and chemical crosslinking techniques on electrospun type A and B gelatin fiber mats. Int J Biol Macromol. 2010;47:431–8.PubMedCrossRefGoogle Scholar
  99. 99.
    Heck T, Faccio G, Richter M, Thöny-Meyer L. Enzyme-catalyzed protein crosslinking. Appl Microbiol Biotechnol. 2013;97:461–75.PubMedCrossRefGoogle Scholar
  100. 100.
    Jayakrishnan A, Jameela S. Glutaraldehyde as a fixative in bioprostheses and drug delivery matrices. Biomaterials. 1996;17:471–84.PubMedCrossRefGoogle Scholar
  101. 101.
    Yang LJ, Ou YC. The micro patterning of glutaraldehyde (GA)-crosslinked gelatin and its application to cell-culture. Lab Chip. 2005;5:979–84.PubMedCrossRefGoogle Scholar
  102. 102.
    Umashankar P, Mohanan P, Kumari T. Glutaraldehyde treatment elicits toxic response compared to decellularization in bovine pericardium. Toxicol Int. 2012;19:51–8.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Levy RJ, Schoen F, Sherman F, Nichols J, Hawley M, Lund S. Calcification of subcutaneously implanted type I collagen sponges. Effects of formaldehyde and glutaraldehyde pretreatments. Am J Pathol. 1986;122:71–82.PubMedPubMedCentralGoogle Scholar
  104. 104.
    Zhong SP, Teo WE, Zhu X, Beuerman R, Ramakrishna S, Yung LYL. Development of a novel collagen-GAG nanofibrous scaffold via electrospinning. Mater Sci Eng C. 2007;27:262–6.CrossRefGoogle Scholar
  105. 105.
    Hafemann B, Ghofrani K, Gattner HG, Stieve H, Pallua N. Cross-linking by 1-ethyl-3-(3-dimethylaminopropyl)-carbodiimide (EDC) of a collagen/elastin membrane meant to be used as a dermal substitute: effects on physical, biochemical and biological features in vitro. J Mater Sci Mater Med. 2001;12:437–46.PubMedCrossRefGoogle Scholar
  106. 106.
    Fiorani A, Gualandi C, Panseri S, Montesi M, Marcacci M, Focarete ML, et al. Comparative performance of collagen nanofibers electrospun from different solvents and stabilized by different crosslinkers. J Mater Sci Mater Med. 2014;25:2313–21.PubMedCrossRefGoogle Scholar
  107. 107.
    Kidoaki S, Kwon IK, Matsuda T. Mesoscopic spatial designs of nano-and microfiber meshes for tissue-engineering matrix and scaffold based on newly devised multilayering and mixing electrospinning techniques. Biomaterials. 2005;26:37–46.PubMedCrossRefGoogle Scholar
  108. 108.
    Huang GP, Shanmugasundaram S, Masih P, Pandya D, Amara S, Collins G, et al. An investigation of common crosslinking agents on the stability of electrospun collagen scaffolds. J Biomed Mater Res A. 2015;103:762–71.PubMedCrossRefGoogle Scholar
  109. 109.
    Torres-Giner S, Gimeno-Alcaniz JV, Ocio MJ, Lagaron JM. Comparative performance of electrospun collagen nanofibers cross-linked by means of different methods. ACS Appl Mater Interfaces. 2008;1:218–23.CrossRefGoogle Scholar
  110. 110.
    Subbiah R, Hwang MP, Du P, Suhaeri M, Hwang J-H, Hong J-H, et al. Tunable crosslinked cell-derived extracellular matrix guides cell fate. Macromol Biosci. 2016;16:1723–34.PubMedCrossRefGoogle Scholar
  111. 111.
    Zhou Y, Yao H, Wang J, Wang D, Liu Q, Li Z. Greener synthesis of electrospun collagen/hydroxyapatite composite fibers with an excellent microstructure for bone tissue engineering. Int J Nanomed. 2015;10:3203–15.CrossRefGoogle Scholar
  112. 112.
    Prabhakaran MP, Vatankhah E, Ramakrishna S. Electrospun aligned PHBV/collagen nanofibers as substrates for nerve tissue engineering. Biotechnol Bioeng. 2013;110:2775–84.PubMedCrossRefGoogle Scholar
  113. 113.
    Sekiya N, Ichioka S, Terada D, Tsuchiya S, Kobayashi H. Efficacy of a poly glycolic acid (PGA)/collagen composite nanofibre scaffold on cell migration and neovascularisation in vivo skin defect model. J Plast Surg Hand Surg. 2013;47:498–502.PubMedGoogle Scholar
  114. 114.
    Suganya S, Venugopal J, Mary SA, Ramakrishna S, Lakshmi B, Dev VG. Aloe vera incorporated biomimetic nanofibrous scaffold: a regenerative approach for skin tissue engineering. Iran Polym J. 2014;3:237–48.CrossRefGoogle Scholar
  115. 115.
    Chen Z, Wang P, Wei B, Mo X, Cui F. Electrospun collagen–chitosan nanofiber: a biomimetic extracellular matrix for endothelial cell and smooth muscle cell. Acta Biomater. 2010;6:372–82.PubMedCrossRefGoogle Scholar
  116. 116.
    Rnjak-Kovacina J, Wise SG, Li Z, Maitz PK, Young CJ, Wang Y, et al. Electrospun synthetic human elastin: collagen composite scaffolds for dermal tissue engineering. Acta Biomater. 2012;8:3714–22.PubMedCrossRefGoogle Scholar
  117. 117.
    Duan N, Geng X, Ye L, Zhang A, Feng Z, Guo L, et al. A vascular tissue engineering scaffold with core–shell structured nano-fibers formed by coaxial electrospinning and its biocompatibility evaluation. Biomed Mater. 2016;11:035007.PubMedCrossRefGoogle Scholar
  118. 118.
    Chen R, Huang C, Ke Q, He C, Wang H, Mo X. Preparation and characterization of coaxial electrospun thermoplastic polyurethane/collagen compound nanofibers for tissue engineering applications. Colloids Surf B Biointerfaces. 2010;79:315–25.PubMedCrossRefGoogle Scholar
  119. 119.
    Tang Y, Chen L, Zhao K, Wu Z, Wang Y, Tan Q. Fabrication of PLGA/HA (core)-collagen/amoxicillin (shell) nanofiber membranes through coaxial electrospinning for guided tissue regeneration. Compos Sci Technol. 2016;125:100–7.CrossRefGoogle Scholar
  120. 120.
    Lee K, Silva EA, Mooney DJ. Growth factor delivery-based tissue engineering: general approaches and a review of recent developments. J R Soc Interface. 2011;8:153–70.PubMedCrossRefGoogle Scholar
  121. 121.
    Townsend-Nicholson A, Jayasinghe SN. Cell electrospinning: a unique biotechnique for encapsulating living organisms for generating active biological microthreads/scaffolds. Biomacromolecules. 2006;7:3364–9.PubMedCrossRefGoogle Scholar
  122. 122.
    Stankus JJ, Guan J, Fujimoto K, Wagner WR. Microintegrating smooth muscle cells into a biodegradable, elastomeric fiber matrix. Biomaterials. 2006;27:735–44.PubMedCrossRefGoogle Scholar
  123. 123.
    Yang X, Shah JD, Wang H. Nanofiber enabled layer-by-layer approach toward three-dimensional tissue formation. Tissue Eng Part A. 2008;15:945–56.CrossRefGoogle Scholar
  124. 124.
    Bonvallet PP, Schultz MJ, Mitchell EH, Bain JL, Culpepper BK, Thomas SJ, et al. Microporous dermal-mimetic electrospun scaffolds pre-seeded with fibroblasts promote tissue regeneration in full-thickness skin wounds. PLoS One. 2015;10:e0122359.PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Bonvallet PP, Culpepper BK, Bain JL, Schultz MJ, Thomas SJ, Bellis SL. Microporous dermal-like electrospun scaffolds promote accelerated skin regeneration. Tissue Eng Part A. 2014;20:2434–45.PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Martins A, Araújo JV, Reis RL, Neves NM. Electrospun nanostructured scaffolds for tissue engineering applications. Nanomedicine. 2007;2:929–42.PubMedCrossRefGoogle Scholar
  127. 127.
    Shih YRV, Chen CN, Tsai SW, Wang YJ, Lee OK. Growth of mesenchymal stem cells on electrospun type I collagen nanofibers. Stem Cells. 2006;24:2391–7.PubMedCrossRefGoogle Scholar
  128. 128.
    Powell HM, Boyce ST. Engineered human skin fabricated using electrospun collagen-PCL blends: morphogenesis and mechanical properties. Tissue Eng Part A. 2009;15:2177–87.PubMedCrossRefGoogle Scholar
  129. 129.
    Fu X, Wang H. Spatial arrangement of polycaprolactone/collagen nanofiber scaffolds regulates the wound healing related behaviors of human adipose stromal cells. Tissue Eng Part A. 2011;18:631–42.PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Chong C, Wang Y, Maitz PK, Simanainen U, Li Z. An electrospun scaffold loaded with anti-androgen receptor compound for accelerating wound healing. Burns Trauma. 2013;1:95–101.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Gümüşderelioğlu M, Dalkıranoğlu S, Aydın R, Çakmak S. A novel dermal substitute based on biofunctionalized electrospun PCL nanofibrous matrix. J Biomed Mater Res A. 2011;98:461–72.PubMedCrossRefGoogle Scholar
  132. 132.
    Lai HJ, Kuan CH, Wu HC, Tsai JC, Chen TM, Hsieh DJ, et al. Tailored design of electrospun composite nanofibers with staged release of multiple angiogenic growth factors for chronic wound healing. Acta Biomater. 2014;10:4156–66.PubMedCrossRefGoogle Scholar
  133. 133.
    Lin J, Li C, Zhao Y, Hu J, Zhang L-M. Co-electrospun nanofibrous membranes of collagen and zein for wound healing. ACS Appl Mater Interfaces. 2012;4:1050–7.PubMedCrossRefGoogle Scholar
  134. 134.
    Uzunalan G, Ozturk MT, Dincer S, Tuzlakoglu K. A newly designed collagen-based bilayered scaffold for skin tissue regeneration. J Compos Biodegrad Polym. 2013;1:8–15.CrossRefGoogle Scholar
  135. 135.
    Lee CH, Chang SH, Chen WJ, Hung KC, Lin YH, Liu SJ, et al. Augmentation of diabetic wound healing and enhancement of collagen content using nanofibrous glucophage-loaded collagen/PLGA scaffold membranes. J Colloid Interface Sci. 2015;439:88–97.PubMedCrossRefGoogle Scholar
  136. 136.
    Wei Q, Xu F, Xu X, Geng X, Ye L, Zhang A, et al. The multifunctional wound dressing with core–shell structured fibers prepared by coaxial electrospinning. Front Mater Sci. 2016;10:113–21.CrossRefGoogle Scholar
  137. 137.
    Ki CS, Baek DH, Gang KD, Lee KH, Um IC, Park YH. Characterization of gelatin nanofiber prepared from gelatin–formic acid solution. Polymer. 2005;46:5094–102.CrossRefGoogle Scholar
  138. 138.
    Homayoni H, Ravandi SAH, Valizadeh M. Electrospinning of chitosan nanofibers: processing optimization. Carbohydr Polym. 2009;77:656–61.CrossRefGoogle Scholar
  139. 139.
    Liu F, Guo R, Shen M, Wang S, Shi X. Effect of processing variables on the morphology of electrospun poly [(lactic acid)-co-(glycolic acid)] nanofibers. Macromol Mater Eng. 2009;294:666–72.CrossRefGoogle Scholar
  140. 140.
    Zhang C, Yuan X, Wu L, Han Y, Sheng J. Study on morphology of electrospun poly(vinyl alcohol) mats. Eur Polym J. 2005;41:423–32.CrossRefGoogle Scholar
  141. 141.
    Gu S, Ren J, Vancso G. Process optimization and empirical modeling for electrospun polyacrylonitrile (PAN) nanofiber precursor of carbon nanofibers. Eur Polym J. 2005;41:2559–68.CrossRefGoogle Scholar
  142. 142.
    Şener AG, Altay AS, Altay F. Effect of voltage on morphology of electrospun nanofibers. Presented at: 2011 7th International Conference on Electrical and Electronics Engineering (ELECO). Bursa, Turkey; 2011.Google Scholar
  143. 143.
    Liu Y, Dong L, Fan J, Wang R, Yu JY. Effect of applied voltage on diameter and morphology of ultrafine fibers in bubble electrospinning. J Appl Polym Sci. 2011;120:592–8.CrossRefGoogle Scholar
  144. 144.
    Beachley V, Wen X. Effect of electrospinning parameters on the nanofiber diameter and length. Mater Sci Eng C. 2009;29:663–8.CrossRefGoogle Scholar
  145. 145.
    Rodoplu D, Mutlu M. Effects of electrospinning setup and process parameters on nanofiber morphology intended for the modification of quartz crystal microbalance surfaces. J Eng Fiber Fabr. 2012;7:118–23.Google Scholar
  146. 146.
    Fong H, Chun I, Reneker D. Beaded nanofibers formed during electrospinning. Polymer. 1999;40:4585–92.CrossRefGoogle Scholar
  147. 147.
    Yang Q, Li Z, Hong Y, Zhao Y, Qiu S, Wang C, et al. Influence of solvents on the formation of ultrathin uniform poly(vinyl pyrrolidone) nanofibers with electrospinning. J Polym Sci Part B Polym Phys. 2004;42:3721–6.CrossRefGoogle Scholar
  148. 148.
    Zheng J, He A, Li J, Xu J, Han CC. Studies on the controlled morphology and wettability of polystyrene surfaces by electrospinning or electrospraying. Polymer. 2006;47:7095–102.CrossRefGoogle Scholar
  149. 149.
    Huang C, Chen S, Lai C, Reneker DH, Qiu H, Ye Y, et al. Electrospun polymer nanofibres with small diameters. Nanotechnology. 2006;17:1558–63.PubMedCrossRefGoogle Scholar
  150. 150.
    Lin T, Wang H, Wang H, Wang X. The charge effect of cationic surfactants on the elimination of fibre beads in the electrospinning of polystyrene. Nanotechnology. 2004;15:1375–81.CrossRefGoogle Scholar
  151. 151.
    Koski A, Yim K, Shivkumar S. Effect of molecular weight on fibrous PVA produced by electrospinning. Mater Lett. 2004;58:493–7.CrossRefGoogle Scholar
  152. 152.
    Tao J, Shivkumar S. Molecular weight dependent structural regimes during the electrospinning of PVA. Mater Lett. 2007;61:2325–8.CrossRefGoogle Scholar
  153. 153.
    Kim KW, Lee KH, Khil MS, Ho YS, Kim HY. The effect of molecular weight and the linear velocity of drum surface on the properties of electrospun poly(ethylene terephthalate) nonwovens. Fiber Polym. 2004;5:122–7.CrossRefGoogle Scholar
  154. 154.
    Mo X, Xu C, Kotaki MEA, Ramakrishna S. Electrospun P (LLA-CL) nanofiber: a biomimetic extracellular matrix for smooth muscle cell and endothelial cell proliferation. Biomaterials. 2004;25:1883–90.PubMedCrossRefGoogle Scholar
  155. 155.
    Sukigara S, Gandhi M, Ayutsede J, Micklus M, Ko F. Regeneration of Bombyx mori silk by electrospinning-part 1: processing parameters and geometric properties. Polymer. 2003;44:5721–7.CrossRefGoogle Scholar
  156. 156.
    Veleirinho B, Rei MF, Lopes-Da-Silva J. Solvent and concentration effects on the properties of electrospun poly(ethylene terephthalate) nanofiber mats. J Polym Sci Part B Polym Phys. 2008;46:460–71.CrossRefGoogle Scholar
  157. 157.
    Wannatong L, Sirivat A, Supaphol P. Effects of solvents on electrospun polymeric fibers: preliminary study on polystyrene. Polym Int. 2004;53:1851–9.CrossRefGoogle Scholar
  158. 158.
    Pattamaprom C, Hongrojjanawiwat W, Koombhongse P, Supaphol P, Jarusuwannapoo T, Rangkupan R. The influence of solvent properties and functionality on the electrospinnability of polystyrene nanofibers. Macromol Mater Eng. 2006;291:840–7.CrossRefGoogle Scholar
  159. 159.
    Luo C, Stride E, Edirisinghe M. Mapping the influence of solubility and dielectric constant on electrospinning polycaprolactone solutions. Macromolecules. 2012;45:4669–80.CrossRefGoogle Scholar
  160. 160.
    Gu X, Song X, Shao C, Zeng P, Lu X, Shen X, et al. Electrospinning of poly(butylene-carbonate): effect of solvents on the properties of the nanofibers film. Int J Electrochem Sci. 2014;9:8045–56.Google Scholar
  161. 161.
    Du L, Xu H, Zhang Y, Zou F. Electrospinning of polycaprolatone nanofibers with DMF additive: the effect of solution proprieties on jet perturbation and fiber morphologies. Fiber Polym. 2016;17:751–9.CrossRefGoogle Scholar
  162. 162.
    Zhou H, Green TB, Joo YL. The thermal effects on electrospinning of polylactic acid melts. Polymer. 2006;47:7497–505.CrossRefGoogle Scholar
  163. 163.
    Wang C, Chien HS, Hsu CH, Wang YC, Wang CT, Lu HA. Electrospinning of polyacrylonitrile solutions at elevated temperatures. Macromolecules. 2007;40:7973–83.CrossRefGoogle Scholar
  164. 164.
    Mit-Uppatham C, Nithitanakul M, Supaphol P. Ultrafine electrospun polyamide-6 fibers: effect of solution conditions on morphology and average fiber diameter. Macromol Chem Phys. 2004;205:2327–38.CrossRefGoogle Scholar
  165. 165.
    Kim GT, Lee JS, Shin JH, Ahn YC, Hwang YJ, Shin HS, et al. Investigation of pore formation for polystyrene electrospun fiber: effect of relative humidity. Korean J Chem Eng. 2005;22:783–8.CrossRefGoogle Scholar
  166. 166.
    Medeiros ES, Mattoso LH, Offeman RD, Wood DF, Orts WJ. Effect of relative humidity on the morphology of electrospun polymer fibers. Can J Chem. 2008;86:590–9.CrossRefGoogle Scholar
  167. 167.
    Nezarati RM, Eifert MB, Cosgriff-Hernandez E. Effects of humidity and solution viscosity on electrospun fiber morphology. Tissue Eng Part C Methods. 2013;19:810–9.PubMedPubMedCentralCrossRefGoogle Scholar
  168. 168.
    Francis L, Giunco F, Balakrishnan A, Marsano E. Synthesis, characterization and mechanical properties of nylon–silver composite nanofibers prepared by electrospinning. Curr Appl Phys. 2010;10:1005–8.CrossRefGoogle Scholar
  169. 169.
    Lee CH, Singla A, Lee Y. Biomedical applications of collagen. Int J Pharm. 2001;221:1–22.PubMedCrossRefGoogle Scholar
  170. 170.
    Qian W, Yu DG, Li Y, Liao YZ, Wang X, Wang L. Dual drug release electrospun core–shell nanofibers with tunable dose in the second phase. Int J Mol Sci. 2014;15:774–86.PubMedPubMedCentralCrossRefGoogle Scholar
  171. 171.
    Li D, Xia Y. Direct fabrication of composite and ceramic hollow nanofibers by electrospinning. Nano Lett. 2004;4:933–8.CrossRefGoogle Scholar
  172. 172.
    Li Y, Lim CT, Kotaki M. Study on structural and mechanical properties of porous PLA nanofibers electrospun by channel-based electrospinning system. Polymer. 2015;56:572–80.CrossRefGoogle Scholar
  173. 173.
    Han SO, Son WK, Youk JH, Lee TS, Park WH. Ultrafine porous fibers electrospun from cellulose triacetate. Mater Lett. 2005;59:2998–3001.CrossRefGoogle Scholar
  174. 174.
    Englert C, Blunk T, Müller R, von Glasser SS, Baumer J, Fierlbeck J, et al. Bonding of articular cartilage using a combination of biochemical degradation and surface cross-linking. Arthritis Res Ther. 2007;9:R47.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© The Korean Tissue Engineering and Regenerative Medicine Society and Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Jia Xian Law
    • 1
  • Ling Ling Liau
    • 2
  • Aminuddin Saim
    • 3
  • Ying Yang
    • 4
  • Ruszymah Idrus
    • 2
  1. 1.Tissue Engineering CentreUniversiti Kebangsaan Malaysia Medical CentreKuala LumpurMalaysia
  2. 2.Department of Physiology, Faculty of MedicineUniversiti Kebangsaan Malaysia Medical CentreKuala LumpurMalaysia
  3. 3.Ear, Nose and Throat Consultant ClinicAmpang Puteri Specialist HospitalAmpangMalaysia
  4. 4.Institute for Science and Technology in Medicine, School of MedicineKeele UniversityStoke-on-TrentUK

Personalised recommendations