Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-28T03:46:15.509Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of anisotropic silk fibroin topographies on dorsal root ganglion

Published online by Cambridge University Press:  03 June 2020

Yan Kong ,
Liling Zhang ,
Qi Han ,
Shiyu Chen ,
Yifan Liu ,
Hanshuo Mu ,
Yiheng Liu ,
Guicai Li Open the ORCID record for Guicai Li [Opens in a new window] ,
Xiaoyang Chen  and
Yumin Yang
Yan Kong
Affiliation:
Key Laboratory of Eco-Textiles, Ministry of Education, School of Textiles and Clothing, Jiangnan University, Wuxi, Jiangsu214122, P.R. China
Liling Zhang
Affiliation:
Key Laboratory of Neuroregeneration of Jiangsu and Ministry of Education, Nantong University, Nantong226001, P.R. China Co-innovation Center of Neuroregeneration, Nantong University, Nantong226001, P.R. China
Qi Han
Affiliation:
Key Laboratory of Neuroregeneration of Jiangsu and Ministry of Education, Nantong University, Nantong226001, P.R. China Co-innovation Center of Neuroregeneration, Nantong University, Nantong226001, P.R. China
Shiyu Chen
Affiliation:
Key Laboratory of Neuroregeneration of Jiangsu and Ministry of Education, Nantong University, Nantong226001, P.R. China Co-innovation Center of Neuroregeneration, Nantong University, Nantong226001, P.R. China
Yifan Liu
Affiliation:
School of Medicine, Nantong University, Nantong226001, P.R. China
Hanshuo Mu
Affiliation:
School of Medicine, Nantong University, Nantong226001, P.R. China
Yiheng Liu
Affiliation:
School of Medicine, Nantong University, Nantong226001, P.R. China
Guicai Li*
Affiliation:
Key Laboratory of Neuroregeneration of Jiangsu and Ministry of Education, Nantong University, Nantong226001, P.R. China Co-innovation Center of Neuroregeneration, Nantong University, Nantong226001, P.R. China
Xiaoyang Chen*
Affiliation:
Department of Ultrasound, Affiliated Hospital of Nantong University, Nantong226001, P.R. China
Yumin Yang*
Affiliation:
Key Laboratory of Eco-Textiles, Ministry of Education, School of Textiles and Clothing, Jiangnan University, Wuxi, Jiangsu214122, P.R. China Key Laboratory of Neuroregeneration of Jiangsu and Ministry of Education, Nantong University, Nantong226001, P.R. China Co-innovation Center of Neuroregeneration, Nantong University, Nantong226001, P.R. China
*
a)Address all correspondence to these authors. e-mail: gcli1981@ntu.edu.cn
b)e-mail: 110288664@qq.com
c)e-mail: yangym@ntu.edu.cn
Get access

Abstract

The surface topology of biomaterial has a definite effect on the growth behavior of nerve cells for peripheral nerve regeneration. In this study, the silk fibroin (SF) film with different anisotropic microgroove/ridge was constructed by micropatterning technology. The effects of topologies width on the directional growth of dorsal root ganglion (DRG) neurons were evaluated. The results showed that the topological structure of the SF film with higher SF concentration was more clear and complete. The microtopography of the SF film with a concentration of 15% and a groove width of around 30 μm could effectively guide the directional growth of the nerve fibers of DRG. And nerve fibers could obviously form nerve fiber bundles which may have a certain pavement effect on the recovery of nerve function. The study indicated that the SF film with a specific width of the topological structure may have potential applications in the field of directional nerve regeneration.

Type
Article
Information
Journal of Materials Research , Volume 35 , Issue 13: Focus Section: Interactions of Shear Transformation Bands , 14 July 2020 , pp. 1738 - 1748
Check for updates
Copyright
Copyright © Materials Research Society 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Robinson, L.R.: Traumatic injury to peripheral nerves. Muscle Nerve 23, 863 (2000).3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Gu, X., Ding, F., and Williams, D.F.: Neural tissue engineering options for peripheral nerve regeneration. Biomaterials 35, 6143 (2014).CrossRefGoogle ScholarPubMed
Gu, X.S., Ding, F., Yang, Y.M., and Liu, J.: Construction of tissue engineered nerve grafts and their application in peripheral nerve regeneration. Prog. Neurobiol. 93, 204 (2011).CrossRefGoogle ScholarPubMed
Gu, X.S., Ding, F., and Williams, D.F.: Neural tissue engineering options for peripheral nerve regeneration. Biomaterials 35, 6143 (2014).CrossRefGoogle ScholarPubMed
Belanger, K., Dinis, T.M., Taourirt, S., Vidal, G., Kaplan, D.L., and Egles, C.: Recent strategies in tissue engineering for guided peripheral nerve regeneration. Macromol. Biosci. 16, 472 (2016).CrossRefGoogle ScholarPubMed
Siemionow, M. and Brzezicki, G.: Chapter 8: Current techniques and concepts in peripheral nerve repair. Int. Rev. Neurobiol. 87, 141 (2009).CrossRefGoogle ScholarPubMed
Mackinnon, S.E. and Hudson, A.R.: Clinical application of peripheral nerve transplantation. Plast. Reconstr. Surg. 90, 695 (1992).CrossRefGoogle ScholarPubMed
Yang, Y., Ding, F., Wu, H., Hu, W., Liu, W., Liu, H., and Gu, X.: Development and evaluation of silk fibroin-based nerve grafts used for peripheral nerve regeneration. Biomaterials 28, 5526 (2007).CrossRefGoogle ScholarPubMed
Xu, Z.Q., Chen, Z.X., Feng, W.F., Huang, M.L., Yang, X.N., and Qi, Z.L.: Grafted muscle-derived stem cells promote the therapeutic efficiency of epimysium conduits in mice with peripheral nerve gap injury. Artif. Organs 44, E214 (2020).CrossRefGoogle ScholarPubMed
Houshyar, S., Bhattacharyya, A., and Shanks, R.: Peripheral nerve conduit: Materials and structures. ACS Chem. Neurosci. 10, 3349 (2019).CrossRefGoogle ScholarPubMed
Lee, C.H., Cheng, Y.W., and Huang, G.S.: Topographical control of cell-cell interaction in C6 glioma by nanodot arrays. Nanoscale Res. Lett. 9, 250 (2014).CrossRefGoogle ScholarPubMed
Leclech, C., Renner, M., Villard, C., and Metin, C.: Topographical cues control the morphology and dynamics of migrating cortical interneurons. Biomaterials 214 (2019).CrossRefGoogle ScholarPubMed
Bui, V.T., Thuy, L.T., Choi, J.S., and Choi, H.S.: Ordered cylindrical micropatterned Petri dishes used as scaffolds for cell growth. J. Colloid Interf. Sci. 513, 161 (2018).CrossRefGoogle ScholarPubMed
Viswanathan, P., Ondeck, M.G., Chirasatitsin, S., Ngamkham, K., Reilly, G.C., Engler, A.J., and Battaglia, G.: 3D surface topology guides stem cell adhesion and differentiation. Biomaterials 52, 140 (2015).CrossRefGoogle ScholarPubMed
Seo, H.R., Joo, H.J., Kim, D.H., Cui, L.H., Choi, S.C., Kim, J.H., Cho, S.W., Lee, K.B., and Lim, D.S.: Nanopillar surface topology promotes cardiomyocyte differentiation through cofilin-mediated cytoskeleton rearrangement. ACS Appl. Mater. Interfaces 9, 16804 (2017).CrossRefGoogle ScholarPubMed
Liliensiek, S.J., Wood, J.A., Yong, J.A., Auerbach, R., Nealey, P.F., and Murphy, C.J.: Modulation of human vascular endothelial cell behaviors by nanotopographic cues. Biomaterials 31, 5418 (2010).CrossRefGoogle ScholarPubMed
Abagnale, G., Sechi, A., Steger, M., Zhou, Q.H., Kuo, C.C., Aydin, G., Schalla, C., Muller-Newen, G., Zenke, M., Costa, I.G., Van Rijn, P., Gillner, A., and Wagner, W.: Surface topography guides morphology and spatial patterning of induced pluripotent stem cell colonies. Stem Cell Rep. 9, 654 (2017).CrossRefGoogle ScholarPubMed
Li, G.C., Chen, S.Y., Zeng, M., Yan, K., Fei, Z., Luzhong, Z., and Yumin, Y.: Hierarchically aligned gradient collagen micropatterns for rapidly screening Schwann cells behavior. Colloid Surf. B 176, 341 (2019).CrossRefGoogle ScholarPubMed
Li, G.C., Zhao, X.Y., Zhao, W.X., Zhang, L.Z., Wang, C.P., Jiang, M.R., Gu, X.S., and Yang, Y.M.: Porous chitosan scaffolds with surface micropatterning and inner porosity and their effects on Schwann cells. Biomaterials 35, 8503 (2014).CrossRefGoogle ScholarPubMed
Badea, A., Mccracken, J.M., Tillmaand, E.G., Kandel, M.E., Oraham, A.W., Mevis, M.B., Rubakhin, S.S., Popescu, G., Sweedler, J.V., and Nuzzo, R.G.: 3D-Printed pHEMA materials for topographical and biochemical modulation of dorsal root ganglion cell response. ACS Appl. Mater. Interfaces 9, 30318 (2017).CrossRefGoogle ScholarPubMed
Vepari, C. and Kaplan, D.L.: Silk as a biomaterial. Prog. Polym. Sci. 32, 991 (2007).CrossRefGoogle Scholar
Huemmerich, D., Slotta, U., and Scheibel, T.: Processing and modification of films made from recombinant spider silk proteins. Appl. Phys. A Mater. Sci. Process. 82, 219 (2006).CrossRefGoogle Scholar
Altman, G.H., Diaz, F., Jakuba, C., Calabro, T., Horan, R.L., Chen, J.S., Lu, H., Richmond, J., and Kaplan, D.L.: Silk-based biomaterials. Biomaterials 24, 401 (2003).CrossRefGoogle ScholarPubMed
Lawrence, B.D., Marchant, J.K., Pindrus, M.A., Omenetto, F.G., and Kaplan, D.L.: Silk film biomaterials for cornea tissue engineering. Biomaterials 30, 1299 (2009).CrossRefGoogle ScholarPubMed
Gil, E.S., Mandal, B.B., Park, S.H., Marchant, J.K., Omenetto, F.G., and Kaplan, D.L.: Helicoidal multi-lamellar features of RGD-functionalized silk biomaterials for corneal tissue engineering. Biomaterials 31, 8953 (2010).CrossRefGoogle ScholarPubMed
Yang, Y.M., Chen, X.M., Ding, F., Zhang, P.Y., Liu, J., and Go, X.S.: Biocompatibility evaluation of silk fibroin with peripheral nerve tissues and cells in vitro. Biomaterials 28, 1643 (2007).CrossRefGoogle ScholarPubMed
Li, G.F., Chen, K., You, D., Xia, M.Y., Li, W., Fan, S.N., Chai, R.J., Zhang, Y.P., Li, H.W., and Sun, S.: Laminin-coated electrospun regenerated silk fibroin mats promote neural progenitor cell proliferation, differentiation, and survival in vitro. Front. Bioeng. Biotech. 7, 190 (2019).CrossRefGoogle ScholarPubMed
Nune, M., Manchineella, S., Govindaraju, T., and Narayan, K.S.: Melanin incorporated electroactive and antioxidant silk fibroin nanofibrous scaffolds for nerve tissue engineering. Mat. Sci. Eng. C Mater. 94, 17 (2019).CrossRefGoogle ScholarPubMed
Wang, C.Y., Xia, K.L., Zhang, Y.Y., and Kaplan, D.L.: Silk-based advanced materials for soft electronics. Acc. Chem. Res. 52, 2916 (2019).CrossRefGoogle ScholarPubMed
Shrestha, S., Shrestha, B.K., Lee, J., Joong, O.K., Kim, B.S., Park, C.H., and Kim, C.S.: A conducting neural interface of polyurethane/silk-functionalized multiwall carbon nanotubes with enhanced mechanical strength for neuroregeneration. Mat. Sci. Eng. C Mater. 102, 511 (2019).CrossRefGoogle ScholarPubMed
Saftics, A., Turk, B., Sulyok, A., Nagy, N., Gerecsei, T., Szekacs, I., Kurunczi, S., and Horvath, R.: Biomimetic dextran-based hydrogel layers for cell micropatterning over large areas using the FluidFM BOT technology. Langmuir 35, 2412 (2019).CrossRefGoogle ScholarPubMed
Frank, A., Grunwald, J., Breitbach, B., and Scheu, C.: Facile and robust solvothermal synthesis of nanocrystalline CuInS2 thin films. Nanomaterials (Basel) 8, 405 (2018).CrossRefGoogle ScholarPubMed
Blum, A.P., Kammeyer, J.K., Rush, A.M., Callmann, C.E., Hahn, M.E., and Gianneschi, N.C.: Stimuli-responsive nanomaterials for biomedical applications. J. Am. Chem. Soc. 137, 2140 (2015).CrossRefGoogle ScholarPubMed
Zhang, Y., Chen, S.E., Shao, J.L., and Van Den Beucken, J.J.J.P.: Combinatorial surface roughness effects on osteoclastogenesis and osteogenesis. ACS Appl. Mater. Interfaces 10, 36652 (2018).CrossRefGoogle ScholarPubMed
Li, X.Z., Huang, Q.L., Elkhooly, T.A., Liu, Y., Wu, H., Feng, Q.L., Liu, L., Fang, Y., Zhu, W.H., and Hu, T.R.: Effects of titanium surface roughness on the mediation of osteogenesis via modulating the immune response of macrophages. Biomed. Mater. 13, 19 (2018).CrossRefGoogle ScholarPubMed
Gad, M.M., Rahoma, A., and Al-Thobity, A.M.: Effect of polymerization technique and glass fiber addition on the surface roughness and hardness of PMMA denture base material. Dent. Mater. J. 37, 746 (2018).CrossRefGoogle ScholarPubMed
Schoen, B., Avrahami, R., Baruch, L., Efraim, Y., Goldfracht, I., Elul, O., Davidov, T., Gepstein, L., Zussman, E., and Machluf, M.: Electrospun extracellular matrix: Paving the way to tailor-made natural scaffolds for cardiac tissue regeneration. Adv. Funct. Mater. 27, 1700427 (2017).CrossRefGoogle Scholar
Sethuraman, A., Han, M., Kane, R.S., and Belfort, G.: Effect of surface wettability on the adhesion of proteins. Langmuir 20, 7779 (2004).CrossRefGoogle ScholarPubMed
Cheng, M.Y., Deng, J.U., Yang, F., Gong, Y.D., Zhao, N.M., and Zhang, X.F.: Study on physical properties and nerve cell affinity of composite films from chitosan and gelatin solutions. Biomaterials 24, 2871 (2003).CrossRefGoogle Scholar
Chandran, V., Coppola, G., Nawabi, H., Omura, T., Versano, R., Huebner, E.A., Zhang, A., Costigan, M., Yekkirala, A., Barrett, L., Blesch, A., Michaelevski, I., Davis-Turak, J., Gao, F., Langfelder, P., Horvath, S., He, Z., Benowitz, L., Fainzilber, M., Tuszynski, M., Woolf, C.J., and Geschwind, D.H.: A systems-level analysis of the peripheral nerve intrinsic axonal growth program. Neuron 89, 956 (2016).CrossRefGoogle ScholarPubMed
Li, C.W., Davis, B., Shea, J., Sant, H., Gale, B.K., and Agarwal, J.: Optimization of micropatterned poly(lactic-co-glycolic acid) films for enhancing dorsal root ganglion cell orientation and extension. Neural Regen. Res. 13, 105 (2018).Google Scholar
Hu, A.J., Zuo, B.Q., Zhang, F., Lan, Q., and Zhang, H.X.: Electrospun silk fibroin nanofibers promote Schwann cell adhesion, growth and proliferation. Neural Regen. Res. 7, 1171 (2012).Google ScholarPubMed
Tang, X., Ding, F., Yang, Y.M., Hu, N., Wu, H., and Gu, X.S.: Evaluation on in vitro biocompatibility of silk fibroin-based biomaterials with primarily cultured hippocampal neurons. J. Biomed. Mater. Res. A 91a, 166 (2009).CrossRefGoogle Scholar
Li, X., Zhang, Q., Luo, Z., Yan, S., and You, R.: Biofunctionalized silk fibroin nanofibers for directional and long neurite outgrowth. Biointerphases 14, 061001 (2019).CrossRefGoogle ScholarPubMed
Ghaznavi, A.M., Kokai, L.E., Lovett, M.L., Kaplan, D.L., and Marra, K.G.: Silk fibroin conduits: a cellular and functional assessment of peripheral nerve repair. Ann. Plast. Surg. 66, 273 (2011).CrossRefGoogle ScholarPubMed
Nguyen, A.T., Sathe, S.R., and Yim, E.K.: From nano to micro: topographical scale and its impact on cell adhesion, morphology and contact guidance. J. Phys. Condens. Matter 28, 183001 (2016).CrossRefGoogle ScholarPubMed
White, J.D., Wang, S., Weiss, A.S., and Kaplan, D.L.: Silk-tropoelastin protein films for nerve guidance. Acta Biomater. 14, 1 (2015).CrossRefGoogle ScholarPubMed
Kaiser, J.P., Reinmann, A., and Bruinink, A.: The effect of topographic characteristics on cell migration velocity. Biomaterials 27, 5230 (2006).CrossRefGoogle ScholarPubMed
Melendez-Vasquez, C.V., Einheber, S., and Salzer, J.L.: Rho kinase regulates Schwann cell myelination and formation of associated axonal domains. J. Neurosci. 24, 3953 (2004).CrossRefGoogle ScholarPubMed
Lu, Q., Hu, X., Wang, X.Q., Kluge, J.A., Lu, S.Z., Cebe, P., and Kaplan, D.L.: Water-insoluble silk films with silk I structure. Acta Biomater. 6, 1380 (2010).CrossRefGoogle ScholarPubMed