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Reviews in the Neurosciences

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Volume 27, Issue 7 (Oct 2016)

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Use of electrospinning to construct biomaterials for peripheral nerve regeneration

Qi Quan
  • Department of Orthopedic Surgery, Key Laboratory of Musculoskeletal Trauma and War Injuries PLA, Beijing Key Laboratory of Regenerative Medicine in Orthopedics, Chinese PLA General Hospital, Beijing 100853, People’s Republic of China
/ Biao Chang
  • Department of Orthopedic Surgery, Key Laboratory of Musculoskeletal Trauma and War Injuries PLA, Beijing Key Laboratory of Regenerative Medicine in Orthopedics, Chinese PLA General Hospital, Beijing 100853, People’s Republic of China
/ Hao Ye Meng
  • Department of Orthopedic Surgery, Key Laboratory of Musculoskeletal Trauma and War Injuries PLA, Beijing Key Laboratory of Regenerative Medicine in Orthopedics, Chinese PLA General Hospital, Beijing 100853, People’s Republic of China
/ Ruo Xi Liu
  • Department of Orthopedic Surgery, Key Laboratory of Musculoskeletal Trauma and War Injuries PLA, Beijing Key Laboratory of Regenerative Medicine in Orthopedics, Chinese PLA General Hospital, Beijing 100853, People’s Republic of China
/ Yu Wang
  • Department of Orthopedic Surgery, Key Laboratory of Musculoskeletal Trauma and War Injuries PLA, Beijing Key Laboratory of Regenerative Medicine in Orthopedics, Chinese PLA General Hospital, Beijing 100853, People’s Republic of China
/ Shi Bi Lu
  • Department of Orthopedic Surgery, Key Laboratory of Musculoskeletal Trauma and War Injuries PLA, Beijing Key Laboratory of Regenerative Medicine in Orthopedics, Chinese PLA General Hospital, Beijing 100853, People’s Republic of China
/ Jiang Peng
  • Corresponding author
  • Department of Orthopedic Surgery, Key Laboratory of Musculoskeletal Trauma and War Injuries PLA, Beijing Key Laboratory of Regenerative Medicine in Orthopedics, Chinese PLA General Hospital, 28 FuXing Road, Beijing 100853, People’s Republic of China
  • Email:
/ Qing Zhao
  • Corresponding author
  • Department of Orthopedic Surgery, First Affiliated Hospital of PLA General Hospital, 51 FuCheng Road, Beijing 100048, People’s Republic of China
  • Email:
Published Online: 2016-07-18 | DOI: https://doi.org/10.1515/revneuro-2016-0032

Abstract

A number of limitations associated with the use of hollow nerve guidance conduits (NGCs) require further discussion. Most importantly, the functional recovery outcomes after the placement of hollow NGCs are poor even after the successful bridging of peripheral nerve injuries. However, nerve regeneration scaffolds built using electric spinning have several advantages that may improve functional recovery. Thus, the present study summarizes recent developments in this area, including the key cells that are combined with the scaffold and associated with nerve regeneration, the structure and configuration of the electrospinning design (which determines the performance of the electrospinning scaffold), the materials the electrospinning fibers are composed of, and the methods used to control the morphology of a single fiber. Additionally, this study also discusses the processes underlying peripheral nerve regeneration. The primary goals of the present review were to evaluate and consolidate the findings of studies that used scaffolding biomaterials built by electrospinning used for peripheral nerve regeneration support. It is amazing that the field of peripheral nerve regeneration continues to consistently produce such a wide variety of innovative techniques and novel types of equipment, because the introduction of every new process creates an opportunity for advances in materials for nerve repair.

Keywords: electrospinning; nanofiber scaffold; peripheral nerve regeneration

References

  • Araujo, J.V., Carvalho, P.P., and Best, S.M. (2015). Electrospinning of bioinspired polymer scaffolds. Adv. Exp. Med. Biol. 881, 33–53.

  • Arslantunali, D., Dursun, T., Yucel, D., Hasirci, N., and Hasirci, V. (2014). Peripheral nerve conduits: technology update. Med. Devices (Auckl.) 7, 405–424.

  • Arthur-Farraj, P.J., Latouche, M., Wilton, D.K., Quintes, S., Chabrol, E., Banerjee, A., Woodhoo, A., Jenkins, B., Rahman, M., Turmaine, M., et al. (2012). c-Jun reprograms Schwann cells of injured nerves to generate a repair cell essential for regeneration. Neuron 75, 633–647.

  • Avery, M.A., Sheehan, A.E., Kerr, K.S., Wang, J., and Freeman, M.R. (2009). Wld S requires Nmnat1 enzymatic activity and N16-VCP interactions to suppress Wallerian degeneration. J. Cell Biol. 184, 501–513.

  • Baleriola, J. and Hengst, U. (2015). Targeting axonal protein synthesis in neuroregeneration and degeneration. Neurotherapeutics 12, 57–65.

  • Bechara, S.L., Judson, A., and Popat, K.C. (2010). Template synthesized poly(epsilon-caprolactone) nanowire surfaces for neural tissue engineering. Biomaterials 31, 3492–3501.

  • Bellamkonda, R.V. (2006). Peripheral nerve regeneration: an opinion on channels, scaffolds and anisotropy. Biomaterials 27, 3515–3518.

  • Brown, R., Hynes-Allen, A., Swan, A.J., Dissanayake, K.N., Gillingwater, T.H., and Ribchester, R.R. (2015). Activity-dependent degeneration of axotomized neuromuscular synapses in Wld S mice. Neuroscience 290, 300–320.

  • Chen, H., Huang, J., Yu, J., Liu, S., and Gu, P. (2011). Electrospun chitosan-graft-poly (epsilon-caprolactone)/poly (epsilon-caprolactone) cationic nanofibrous mats as potential scaffolds for skin tissue engineering. Int. J. Biol. Macromol. 48, 13–19.

  • Chew, S.Y., Mi, R., Hoke, A., and Leong, K.W. (2007). Aligned protein–polymer composite fibers enhance nerve regeneration: a potential tissue-engineering platform. Adv. Funct. Mater. 17, 1288–1296.

  • Chew, S.Y., Mi, R., Hoke, A., and Leong, K.W. (2008). The effect of the alignment of electrospun fibrous scaffolds on Schwann cell maturation. Biomaterials 29, 653–661.

  • Coleman, M.P. and Freeman, M.R. (2010). Wallerian degeneration, wld(s), and nmnat. Annu. Rev. Neurosci. 33, 245–267.

  • Collyer, E., Catenaccio, A., Lemaitre, D., Diaz, P., Valenzuela, V., Bronfman, F., and Court, F.A. (2014). Sprouting of axonal collaterals after spinal cord injury is prevented by delayed axonal degeneration. Exp. Neurol. 261, 451–461.

  • Conforti, L., Gilley, J., and Coleman, M.P. (2014). Wallerian degeneration: an emerging axon death pathway linking injury and disease. Nat. Rev. Neurosci. 15, 394–409.

  • Daly, W., Yao, L., Zeugolis, D., Windebank, A., and Pandit, A. (2012). A biomaterials approach to peripheral nerve regeneration: bridging the peripheral nerve gap and enhancing functional recovery. J. R. Soc. Interface 9, 202–221.

  • Deng, H., Lin, L., Ji, M., Zhang, S., Yang, M., and Fu, Q. (2014). Progress on the morphological control of conductive network in conductive polymer composites and the use as electroactive multifunctional materials. Progr. Polymer Sci. 39, 627–655.

  • Deumens, R., Bozkurt, A., Meek, M.F., Marcus, M.A., Joosten, E.A., Weis, J., and Brook, G.A. (2010). Repairing injured peripheral nerves: bridging the gap. Prog. Neurobiol. 92, 245–276.

  • Dinis, T.M., Elia, R., Vidal, G., Dermigny, Q., Denoeud, C., Kaplan, D.L., Egles, C., and Marin, F. (2015). 3D multi-channel bi-functionalized silk electrospun conduits for peripheral nerve regeneration. J. Mech. Behav. Biomed. Mater. 41, 43–55.

  • Dinis, T.M., Vidal, G., Jose, R.R., Vigneron, P., Bresson, D., Fitzpatrick, V., Marin, F., Kaplan, D.L., and Egles, C. (2014). Complementary effects of two growth factors in multifunctionalized silk nanofibers for nerve reconstruction. PLoS One 9, e109770.

  • Faroni, A., Mobasseri, S.A., Kingham, P.J., and Reid, A.J. (2015). Peripheral nerve regeneration: experimental strategies and future perspectives. Adv. Drug Deliv. Rev. 82–83, 160–167.

  • Forciniti, L., Ybarra III, J., Zaman, M.H., and Schmidt, C.E. (2014). Schwann cell response on polypyrrole substrates upon electrical stimulation. Acta Biomaterialia 10, 2423–2433.

  • Franze, K., Janmey, P.A., and Guck, J. (2013). Mechanics in neuronal development and repair. Annu. Rev. Biomed. Eng. 15, 227–251.

  • Freeman, M.R. (2014). Signaling mechanisms regulating Wallerian degeneration. Curr. Opin. Neurobiol. 27, 224–231.

  • Gaudet, A.D., Popovich, P.G., and Ramer, M.S. (2011). Wallerian degeneration: gaining perspective on inflammatory events after peripheral nerve injury. J. Neuroinflamm. 8, 110.

  • George, P.M., Saigal, R., Lawlor, M.W., Moore, M.J., LaVan, D.A., Marini, R.P., Selig, M., Makhni, M., Burdick, J.A., Langer, R., et al. (2009). Three-dimensional conductive constructs for nerve regeneration. J. Biomed. Mater. Res. Part A 91A, 519–527.

  • Gerdts, J., Brace, E.J., Sasaki, Y., DiAntonio, A., and Milbrandt, J. (2015). SARM1 activation triggers axon degeneration locally via NAD+ destruction. Science 348, 453–457.

  • Ghasemi-Mobarakeh, L., Prabhakaran, M.P., Morshed, M., Nasr-Esfahani, M.H., and Ramakrishna, S. (2008). Electrospun poly(epsilon-caprolactone)/gelatin nanofibrous scaffolds for nerve tissue engineering. Biomaterials 29, 4532–4539.

  • Gilley, J. and Coleman, M.P. (2010). Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLoS Biol 8, e1000300.

  • Gu, X., Ding, F., Yang, Y., and Liu, J. (2011). Construction of tissue engineered nerve grafts and their application in peripheral nerve regeneration. Prog. Neurobiol. 93, 204–230.

  • Gu, Y., Zhu, J., Xue, C., Li, Z., Ding, F., Yang, Y., and Gu, X. (2014). Chitosan/silk fibroin-based, Schwann cell-derived extracellular matrix-modified scaffolds for bridging rat sciatic nerve gaps. Biomaterials 35, 2253–2263.

  • Guimard, N.K., Gomez, N., and Schmidt, C.E. (2007). Conducting polymers in biomedical engineering. Progr. Polymer Sci. 32, 876–921.

  • Ichihara, S., Inada, Y., and Nakamura, T. (2008). Artificial nerve tubes and their application for repair of peripheral nerve injury: an update of current concepts. Injury 39 (Suppl 4), 29–39.

  • Ikeda, M., Uemura, T., Takamatsu, K., Okada, M., Kazuki, K., Tabata, Y., Ikada, Y., and Nakamura, H. (2014). Acceleration of peripheral nerve regeneration using nerve conduits in combination with induced pluripotent stem cell technology and a basic fibroblast growth factor drug delivery system. J. Biomed. Mater. Res. A 102, 1370–1378.

  • Isaacs, J. (2010). Treatment of acute peripheral nerve injuries: current concepts. J. Hand Surg. Am. 35, 491–497; quiz 498.

  • Jha, B.S., Colello, R.J., Bowman, J.R., Sell, S.A., Lee, K.D., Bigbee, J.W., Bowlin, G.L., Chow, W.N., Mathern, B.E., and Simpson, D.G. (2011). Two pole air gap electrospinning: fabrication of highly aligned, three-dimensional scaffolds for nerve reconstruction. Acta Biomater. 7, 203–215.

  • Jiang, X., Lim, S.H., Mao, H.-Q., and Chew, S.Y. (2010). Current applications and future perspectives of artificial nerve conduits. Exper. Neurol. 223, 86–101.

  • Kabay, G., Kaleli, G., Sultanova, Z., Ölmez, T.T., Şeker, U.Ö.Ş., and Mutlu, M. (2016). Biocatalytic protein membranes fabricated by electrospinning. React. Funct. Polymers 103, 26–32.

  • Kim, Y.-T., Haftel, V.K., Kumar, S., and Bellamkonda, R.V. (2008). The role of aligned polymer fiber-based constructs in the bridging long peripheral nerve gaps. Biomaterials 29, 3117–3127.

  • Lee, J.Y., Bashur, C.A., Goldstein, A.S., and Schmidt, C.E. (2009). Polypyrrole-coated electrospun PLGA nanofibers for neural tissue applications. Biomaterials 30, 4325–4335.

  • Li, C., Vepari, C., Jin, H.J., Kim, H.J., and Kaplan, D.L. (2006). Electrospun silk-BMP-2 scaffolds for bone tissue engineering. Biomaterials 27, 3115–3124.

  • Liu, T., Teng, W.K., Chan, B.P., and Chew, S.Y. (2010). Photochemical crosslinked electrospun collagen nanofibers: synthesis, characterization and neural stem cell interactions. J. Biomed. Mater. Res. A 95, 276–282.

  • Malin, D., Sonnenberg-Riethmacher, E., Guseva, D., Wagener, R., Aszodi, A., Irintchev, A., and Riethmacher, D. (2009). The extracellular-matrix protein matrilin 2 participates in peripheral nerve regeneration. J. Cell Sci. 122, 1471–1471.

  • Marquardt, L.M. and Sakiyama-Elbert, S.E. (2013). Engineering peripheral nerve repair. Curr. Opin. Biotechnol. 24, 887–892.

  • Mosahebi, A., Fuller, P., Wiberg, M., and Terenghi, G. (2002). Effect of allogeneic Schwann cell transplantation on peripheral nerve regeneration. Exp. Neurol. 173, 213–223.

  • Nectow, A.R., Marra, K.G., and Kaplan, D.L. (2012). Biomaterials for the development of peripheral nerve guidance conduits. Tissue Eng. Part B Rev. 18, 40–50.

  • Nisbet, D.R., Forsythe, J.S., Shen, W., Finkelstein, D.I., and Horne, M.K. (2009). Review paper: a review of the cellular response on electrospun nanofibers for tissue engineering. J. Biomater. Appl. 24, 7–29.

  • Niu, Q., Zeng, L., Mu, X., Nie, J., and Ma, G. (2016). Preparation and characterization of core-shell nanofibers by electrospinning combined with in situ UV photopolymerization. J. Industrial Eng. Chem. 34, 337–343.

  • Pabari, A., Yang, S.Y., Seifalian, A.M., and Mosahebi, A. (2010). Modern surgical management of peripheral nerve gap. J. Plast. Reconstr. Aesthet. Surg. 63, 1941–1948.

  • Panseri, S., Cunha, C., Lowery, J., Del Carro, U., Taraballi, F., Amadio, S., Vescovi, A., and Gelain, F. (2008). Electrospun micro- and nanofiber tubes for functional nervous regeneration in sciatic nerve transections. BMC Biotechnol. 8, 39.

  • Pourbozorg, M., Li, T., and Law, A.W.K. (2016). Effect of turbulence on fouling control of submerged hollow fibre membrane filtration. Water Res. 99, 101–111.

  • Prabhakaran, M.P., Venugopal, J.R., Chyan, T.T., Hai, L.B., Chan, C.K., Lim, A.Y., and Ramakrishna, S. (2008). Electrospun biocomposite nanofibrous scaffolds for neural tissue engineering. Tissue Eng. Part A 14, 1787–1797.

  • Qazi, T.H., Rai, R., and Boccaccini, A.R. (2014). Tissue engineering of electrically responsive tissues using polyaniline based polymers: a review. Biomaterials 35, 9068–9086.

  • Ribeiro, J., Pereira, T., Caseiro, A.R., Armada-da-Silva, P., Pires, I., Prada, J., Amorim, I., Amado, S., França, M., Gonçalves, C., et al. (2015). Evaluation of biodegradable electric conductive tube-guides and mesenchymal stem cells. World J. Stem Cells 7, 956–975.

  • Ruckh, T.T., Kumar, K., Kipper, M.J., and Popat, K.C. (2010). Osteogenic differentiation of bone marrow stromal cells on poly(epsilon-caprolactone) nanofiber scaffolds. Acta Biomater. 6, 2949–2959.

  • Samadikuchaksaraei, A. (2007). An overview of tissue engineering approaches for management of spinal cord injuries. J. Neuroeng. Rehabil. 4, 15. [Crossref]

  • Schnell, E., Klinkhammer, K., Balzer, S., Brook, G., Klee, D., Dalton, P., and Mey, J. (2007). Guidance of glial cell migration and axonal growth on electrospun nanofibers of poly-epsilon-caprolactone and a collagen/poly-epsilon-caprolactone blend. Biomaterials 28, 3012–3025.

  • Stang, F., Fansa, H., Wolf, G., Reppin, M., and Keilhoff, G. (2005). Structural parameters of collagen nerve grafts influence peripheral nerve regeneration. Biomaterials 26, 3083–3091.

  • Subramanian, A., Krishnan, U.M., and Sethuraman, S. (2009). Development of biomaterial scaffold for nerve tissue engineering: Biomaterial mediated neural regeneration. J. Biomed. Sci. 16, 108.

  • Suwantong, O., Waleetorncheepsawat, S., Sanchavanakit, N., Pavasant, P., Cheepsunthorn, P., Bunaprasert, T., and Supaphol, P. (2007). In vitro biocompatibility of electrospun poly(3-hydroxybutyrate) and poly(3-hydroxybutyrate-co-3-hydroxyvalerate) fiber mats. Int. J. Biol. Macromol. 40, 217–223.

  • Tang, X., Xue, C., Wang, Y., Ding, F., Yang, Y., and Gu, X. (2012). Bridging peripheral nerve defects with a tissue engineered nerve graft composed of an in vitro cultured nerve equivalent and a silk fibroin-based scaffold. Biomaterials 33, 3860–3867.

  • Teuschl, A.H., Schuh, C., Halbweis, R., Pajer, K., Marton, G., Hopf, R., Mosia, S., Runzler, D., Redl, H., Nogradi, A., et al. (2015). A new preparation method for anisotropic silk fibroin nerve guidance conduits and its evaluation in vitro and in a rat sciatic nerve defect model. Tissue Eng. Part C Methods 21, 945–957.

  • Uemura, T., Takamatsu, K., Ikeda, M., Okada, M., Kazuki, K., Ikada, Y., and Nakamura, H. (2012). Transplantation of induced pluripotent stem cell-derived neurospheres for peripheral nerve repair. Biochem. Biophys. Res. Commun. 419, 130–135.

  • Valmikinathan, C.M., Hoffman, J., and Yu, X. (2011). Impact of scaffold micro and macro architecture on Schwann cell proliferation under dynamic conditions in a rotating wall vessel bioreactor. Mater. Sci. Eng. C Mater. Biol. Appl. 31, 22–29.

  • Verreck, G., Chun, I., Li, Y., Kataria, R., Zhang, Q., Rosenblatt, J., Decorte, A., Heymans, K., Adriaensen, J., Bruining, M., et al. (2005). Preparation and physicochemical characterization of biodegradable nerve guides containing the nerve growth agent sabeluzole. Biomaterials 26, 1307–1315.

  • Wang, J.T. and Barres, B.A. (2012). Axon degeneration: where the Wlds things are. Curr. Biol. 22, R221–R223. [Crossref]

  • Wang, X. and Xu, X.M. (2014). Long-term survival, axonal growth-promotion, and myelination of Schwann cells grafted into contused spinal cord in adult rats. Exp. Neurol. 261, 308–319.

  • Wang, W., Itoh, S., Matsuda, A., Aizawa, T., Demura, M., Ichinose, S., Shinomiya, K., and Tanaka, J. (2008). Enhanced nerve regeneration through a bilayered chitosan tube: the effect of introduction of glycine spacer into the CYIGSR sequence. J. Biomed. Mater. Res. A 85, 919–928.

  • Wang, W., Itoh, S., Konno, K., Kikkawa, T., Ichinose, S., Sakai, K., Ohkuma, T., and Watabe, K. (2009). Effects of Schwann cell alignment along the oriented electrospun chitosan nanofibers on nerve regeneration. J. Biomed. Mater. Res. A 91, 994–1005.

  • Wang, J.T., Medress, Z.A., and Barres, B.A. (2012). Axon degeneration: molecular mechanisms of a self-destruction pathway. J. Cell Biol. 196, 7–18.

  • Xia, D.L.Y. (2004). Direct fabrication of composite and ceramic hollow nanofibers by electrospinning. Nano Lett. 4, 933–938.

  • Yang, F., Murugan, R., Wang, S., and Ramakrishna, S. (2005). Electrospinning of nano/micro scale poly(l-lactic acid) aligned fibers and their potential in neural tissue engineering. Biomaterials 26, 2603–2610.

  • You, Y., Youk, J.H., Lee, S.W., Min, B.-M., Lee, S.J., and Park, W.H. (2006). Preparation of porous ultrafine PGA fibers via selective dissolution of electrospun PGA/PLA blend fibers. Mater. Lett. 60, 757–760.

  • Zhu, Y., Wang, A., Patel, S., Kurpinski, K., Diao, E., Bao, X., Kwong, G., Young, W.L., and Li, S. (2011). Engineering bi-layer nanofibrous conduits for peripheral nerve regeneration. Tissue Eng. Part C Methods 17, 705–715.

About the article

aQi Quan and Biao Chang: These authors contributed equally to this work.


Received: 2016-05-13

Accepted: 2016-05-26

Published Online: 2016-07-18

Published in Print: 2016-10-01


Funding Source: National Natural Science Foundation of China

Award identifier / Grant number: 51073024

Award identifier / Grant number: 51273021

The authors received funding from the National Natural Science Foundation of China (51073024, 51273021), 973 (2014CB542201 and 2012CB518106), the Special Project of the ‘Thirteenth Five-year Plan’ for medical Science Development of PLA (BWS13C029), and the Special Project of the ‘Twelfth–Five-year Plan’ for medical Science Development of PLA (BWS11J025).


Citation Information: Reviews in the Neurosciences, ISSN (Online) 2191-0200, ISSN (Print) 0334-1763, DOI: https://doi.org/10.1515/revneuro-2016-0032. Export Citation

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