Reverse engineering of an anatomically equivalent nerve conduit
Preethy Amruthavarshini Ramesh
Tissue Engineering and Additive Manufacturing (TEAM) Lab, Centre for Nanotechnology & Advanced Biomaterials, ABCDE Innovation Centre, School of Chemical & Biotechnology, SASTRA Deemed University, Thanjavur, India
Contribution: Formal analysis, Investigation, Writing - original draft
Search for more papers by this authorRamya Dhandapani
Tissue Engineering and Additive Manufacturing (TEAM) Lab, Centre for Nanotechnology & Advanced Biomaterials, ABCDE Innovation Centre, School of Chemical & Biotechnology, SASTRA Deemed University, Thanjavur, India
Contribution: Formal analysis, Investigation, Writing - review & editing
Search for more papers by this authorShambhavi Bagewadi
Tissue Engineering and Additive Manufacturing (TEAM) Lab, Centre for Nanotechnology & Advanced Biomaterials, ABCDE Innovation Centre, School of Chemical & Biotechnology, SASTRA Deemed University, Thanjavur, India
Contribution: Formal analysis, Investigation
Search for more papers by this authorAllen Zennifer
Tissue Engineering and Additive Manufacturing (TEAM) Lab, Centre for Nanotechnology & Advanced Biomaterials, ABCDE Innovation Centre, School of Chemical & Biotechnology, SASTRA Deemed University, Thanjavur, India
Contribution: Formal analysis
Search for more papers by this authorJanani Radhakrishnan
Tissue Engineering and Additive Manufacturing (TEAM) Lab, Centre for Nanotechnology & Advanced Biomaterials, ABCDE Innovation Centre, School of Chemical & Biotechnology, SASTRA Deemed University, Thanjavur, India
Contribution: Formal analysis
Search for more papers by this authorSwaminathan Sethuraman
Tissue Engineering and Additive Manufacturing (TEAM) Lab, Centre for Nanotechnology & Advanced Biomaterials, ABCDE Innovation Centre, School of Chemical & Biotechnology, SASTRA Deemed University, Thanjavur, India
Contribution: Conceptualization, Writing - review & editing
Search for more papers by this authorCorresponding Author
Anuradha Subramanian
Tissue Engineering and Additive Manufacturing (TEAM) Lab, Centre for Nanotechnology & Advanced Biomaterials, ABCDE Innovation Centre, School of Chemical & Biotechnology, SASTRA Deemed University, Thanjavur, India
Correspondence
Anuradha Subramanian, Tissue Engineering and Additive Manufacturing (TEAM) Lab, Centre for Nanotechnology & Advanced Biomaterials, ABCDE Innovation Centre, School of Chemical & Biotechnology, SASTRA Deemed University, Thanjavur 613 401, Tamil Nadu, India.
Email: [email protected]
Contribution: Conceptualization, Methodology, Validation, Writing - review & editing
Search for more papers by this authorPreethy Amruthavarshini Ramesh
Tissue Engineering and Additive Manufacturing (TEAM) Lab, Centre for Nanotechnology & Advanced Biomaterials, ABCDE Innovation Centre, School of Chemical & Biotechnology, SASTRA Deemed University, Thanjavur, India
Contribution: Formal analysis, Investigation, Writing - original draft
Search for more papers by this authorRamya Dhandapani
Tissue Engineering and Additive Manufacturing (TEAM) Lab, Centre for Nanotechnology & Advanced Biomaterials, ABCDE Innovation Centre, School of Chemical & Biotechnology, SASTRA Deemed University, Thanjavur, India
Contribution: Formal analysis, Investigation, Writing - review & editing
Search for more papers by this authorShambhavi Bagewadi
Tissue Engineering and Additive Manufacturing (TEAM) Lab, Centre for Nanotechnology & Advanced Biomaterials, ABCDE Innovation Centre, School of Chemical & Biotechnology, SASTRA Deemed University, Thanjavur, India
Contribution: Formal analysis, Investigation
Search for more papers by this authorAllen Zennifer
Tissue Engineering and Additive Manufacturing (TEAM) Lab, Centre for Nanotechnology & Advanced Biomaterials, ABCDE Innovation Centre, School of Chemical & Biotechnology, SASTRA Deemed University, Thanjavur, India
Contribution: Formal analysis
Search for more papers by this authorJanani Radhakrishnan
Tissue Engineering and Additive Manufacturing (TEAM) Lab, Centre for Nanotechnology & Advanced Biomaterials, ABCDE Innovation Centre, School of Chemical & Biotechnology, SASTRA Deemed University, Thanjavur, India
Contribution: Formal analysis
Search for more papers by this authorSwaminathan Sethuraman
Tissue Engineering and Additive Manufacturing (TEAM) Lab, Centre for Nanotechnology & Advanced Biomaterials, ABCDE Innovation Centre, School of Chemical & Biotechnology, SASTRA Deemed University, Thanjavur, India
Contribution: Conceptualization, Writing - review & editing
Search for more papers by this authorCorresponding Author
Anuradha Subramanian
Tissue Engineering and Additive Manufacturing (TEAM) Lab, Centre for Nanotechnology & Advanced Biomaterials, ABCDE Innovation Centre, School of Chemical & Biotechnology, SASTRA Deemed University, Thanjavur, India
Correspondence
Anuradha Subramanian, Tissue Engineering and Additive Manufacturing (TEAM) Lab, Centre for Nanotechnology & Advanced Biomaterials, ABCDE Innovation Centre, School of Chemical & Biotechnology, SASTRA Deemed University, Thanjavur 613 401, Tamil Nadu, India.
Email: [email protected]
Contribution: Conceptualization, Methodology, Validation, Writing - review & editing
Search for more papers by this authorAbstract
Reconstruction of peripheral nervous tissue remains challenging in critical-sized defects due to the lack of Büngner bands from the proximal to the distal nerve ends. Conventional nerve guides fail to bridge the large-sized defect owing to the formation of a thin fibrin cable. Hence, in the present study, an attempt was made to reverse engineer the intricate epi-, peri- and endo-neurial tissues using Fused Deposition Modeling based 3D printing. Bovine serum albumin protein nanoflowers (NF) exhibiting Viburnum opulus ‘Roseum’ morphology were ingrained into 3D printed constructs without affecting its secondary structure to enhance the axonal guidance from proximal to distal ends of denuded nerve ends. Scanning electron micrographs confirmed the uniform distribution of protein NF in 3D printed constructs. The PC-12 cells cultured on protein ingrained 3D printed scaffolds demonstrated cytocompatibility, improved cell adhesion and extended neuronal projections with significantly higher intensities of NF-200 and tubulin expressions. Further suture-free fixation designed in the current 3D printed construct aids facile implantation of printed conduits to the transected nerve ends. Hence the protein ingrained 3D printed construct would be a promising substitute to treat longer peripheral nerve defects as its structural equivalence of endo- and perineurial organization along with the ingrained protein NF promote the neuronal extension towards the distal ends by minimizing axonal dispersion.
CONFLICT OF INTEREST
The authors do not have any conflict of interest.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Supporting Information
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| term3245-sup-0001-fig_s1.docx173.1 KB | Supplementary Material |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Bronze-Uhle, E., Costa, B. C., Ximenes, V. F., & Lisboa-Filho, P. N. (2016). Synthetic nanoparticles of bovine serum albumin with entrapped salicylic acid. Nanotechnology, Science and Applications, 10, 11–21. https://doi.org/10.2147/NSA.S117018
- Çalımlı, M. H., Demirbaş, Ö., Aygün, A., Alma, M. H., Nas, M. S., & Şen, F. (2018). Immobilization kinetics and mechanism of bovine serum albumin on diatomite clay from aqueous solutions. Applied Water Science, 8(7), 1–12. https://doi.org/10.1007/s13201-018-0858-8
- Chen, W., Zhang, P., Xue, F., Yin, X., Qi, C., Ma, J., Chen, B., Yu, Y. L., Deng, J. X., & Jiang, B. (2015). Large animal models of human cauda equina injury and repair: Evaluation of a novel goat model. Neural Regeneration Research, 10(1), 60.
- Csach, K., Juríková, A., Miškuf, J., Koneracká, M., Závišová, V., Kubov£íková, M., & Kop£anský, P. (2012). Thermogravimetric study of the decomposition of BSA-coated magnetic nanoparticles. Acta Physica Polonica Series A, 121(5–6), 1293–1295.
- Dhandapani, R., Krishnan, P. D., Zennifer, A., Kannan, V., Manigandan, A., Arul, M. R., Jaiswal, D., Subramanian, A., Kumbar, S. G., & Sethuraman, S. (2020). Bioactive materials additive manufacturing of biodegradable porous orthopaedic screw. Bioactive Materials, 5(3), 458–467. https://doi.org/10.1016/j.bioactmat.2020.03.009
- Dinis, T. M., Elia, R., Vidal, G., Dermigny, Q., Denoeud, C., Kaplan, D. L., Egles, C., & Marin, F. (2015). 3D multi-channel bi-functionalized silk electrospun conduits for peripheral nerve regeneration. Journal of the Mechanical Behavior of Biomedical Materials, 41, 43–55. https://doi.org/10.1016/j.jmbbm.2014.09.029
- Du, J., Chen, H., Qing, L., Yang, X., & Jia, X. (2018). Biomimetic neural scaffolds: A crucial step towards optimal peripheral nerve regeneration. Biomaterials Science, 6(6), 1299–1311. https://doi.org/10.1039/c8bm00260f
- Flynn, K. C. (2013). The cytoskeleton and neurite initiation. BioArchitecture, 3(4), 86–109. https://doi.org/10.4161/bioa.26259
- Gao, X., Zhou, P., Yang, R., Yang, D., & Zhang, N. (2013). Protein-loaded comb-shape copolymer-based pH-responsive nanoparticles to improve the stability of proteins. Journal of Materials Chemistry B, 1(38), 4992–5002. https://doi.org/10.1039/c3tb20500b
- Ge, J., Lei, J., & Zare, R. N. (2012). Protein-inorganic hybrid nanoflowers. Nature Nanotechnology, 7(7), 428–432. https://doi.org/10.1038/nnano.2012.80
- Hsiang, S. W., Tsai, C. C., Tsai, F. J., Ho, T. Y., Yao, C. H., & Chen, Y. S. (2011). Novel use of biodegradable casein conduits for guided peripheral nerve regeneration. Journal of the Royal Society Interface, 8(64), 1622–1634. https://doi.org/10.1098/rsif.2011.0009
- Hu, Y., Wu, Y., Gou, Z., Tao, J., Zhang, J., Liu, Q., Kang, T., Jiang, S., Huang, S., He, J., Chen, S., Du, Y., & Gou, M. (2016). 3D-engineering of cellularized conduits for peripheral nerve regeneration. Scientific Reports, 6(August), 1–12. https://doi.org/10.1038/srep32184
- Huang, Y., Ran, X., Lin, Y., Ren, J., & Qu, X. (2015). Self-assembly of an organic-inorganic hybrid nanoflower as an efficient biomimetic catalyst for self-activated tandem reactions. Chemical Communications, 51(21), 4386–4389. https://doi.org/10.1039/c5cc00040h
- Karami, K., Jamshidian, N., Hajiaghasi, A., & Amirghofran, Z. (2020). BSA nanoparticles as controlled release carriers for isophethalaldoxime palladacycle complex; synthesis, characterization: In vitro evaluation, cytotoxicity and release kinetics analysis. New Journal of Chemistry, 44(11), 4394–4405. https://doi.org/10.1039/c9nj05847h
- Kochhar, J. S., Zou, S., Chan, S. Y., & Kang, L. (2012). Protein encapsulation in polymeric microneedles by photolithography. International Journal of Nanomedicine, 7(June), 3143–3154. https://doi.org/10.2147/IJN.S32000
- Krekoski, C. A., Neubauer, D., Graham, J. B., & Muir, D. (2002). Metalloproteinase-dependent predegeneration in vitro enhances axonal regeneration within acellular peripheral nerve grafts. Journal of Neuroscience, 22(23), 10408–10415.
- Lee, S. J., Asheghali, D., Blevins, B., Timsina, R., Esworthy, T., Zhou, X., Cui, H., Hann, S. Y., Qiu, X., Tokarev, A., Minko, S., & Zhang, L. G. (2020). Touch-spun nanofibers for nerve regeneration. ACS Applied Materials & Interfaces, 12(2), 2067–2075. https://doi.org/10.1021/acsami.9b18614
- Liu, Q., Wang, X., & Yi, S. (2018). Pathophysiological changes of physical barriers of peripheral nerves after injury. Frontiers in Neuroscience, 12(AUG), 1–8. https://doi.org/10.3389/fnins.2018.00597
- Magaz, A., Faroni, A., Gough, J. E., Reid, A. J., Li, X., & Blaker, J. J. (2018). Bioactive silk-based nerve guidance conduits for augmenting peripheral nerve repair. Advanced Healthcare Materials, 7(23), 1800308. https://doi.org/10.1002/adhm.201800308
- Majorek, K. A., Porebski, P. J., Dayal, A., Zimmerman, M. D., Jablonska, K., Stewart, A. J., Chruszcz, M., & Minor, W. (2012). Structural and immunologic characterization of bovine, horse, and rabbit serum albumins. Molecular Immunology, 52(3–4), 174–182. https://doi.org/10.1016/j.molimm.2012.05.011
- Manigandan, A., Vimalanadhan, M., Dhandapani, R., Bagewadi, S., Kannan, V., Sethuraman, S., & Subramanian, A. (2020). Marigold-like tyrosinase-embedded nanostructures–A nano-in-micro system. Dalton Transactions, 49(32), 11329–11335. https://doi.org/10.1039/d0dt02358b
- Ornelas, L., Padilla, L., Di Silvio, M., Schalch, P., Esperante, S., Infante, R. L., Bustamante, J. C., Avalos, P., Varela, D., & López, M. (2006). Fibrin glue: An alternative technique for nerve coaptation–Part I. Wave amplitude, conduction velocity, and plantar-length factors. Journal of Reconstructive Microsurgery, 22(2), 119–122. https://doi.org/10.1055/s-2006-932506
- Pfister, L. A., Papaloïzos, M., Merkle, H. P., & Gander, B. (2007). Nerve conduits and growth factor delivery in peripheral nerve repair. Journal of the Peripheral Nervous System, 12(2), 65–82. https://doi.org/10.1111/j.1529-8027.2007.00125.x
- Ray, W. Z., & Mackinnon, S. E. (2010). Management of nerve gaps: Autografts, allografts, nerve transfers, and end-to-side neurorrhaphy. Experimental Neurology, 223(1), 77–85. https://doi.org/10.1016/j.expneurol.2009.03.031
- Richner, M., Ferreira, N., Dudele, A., Jensen, T. S., Vaegter, C. B., & Gonçalves, N. P. (2019). Functional and structural changes of the blood-nerve-barrier in diabetic neuropathy. Frontiers in Neuroscience, 13(JAN), 1–9. https://doi.org/10.3389/fnins.2018.01038
- Shende, P., Kasture, P., & Gaud, R. S. (2018). Nanoflowers: The future trend of nanotechnology for multi-applications. Artificial Cells, Nanomedicine and Biotechnology, 46, 413–422. https://doi.org/10.1080/21691401.2018.1428812
- Sierpinski, P., Garrett, J., Ma, J., Apel, P., Klorig, D., Smith, T., Koman, L. A., Atala, A., & Van Dyke, M. (2008). The use of keratin biomaterials derived from human hair for the promotion of rapid regeneration of peripheral nerves. Biomaterials, 29(1), 118–128. https://doi.org/10.1016/j.biomaterials.2007.08.023
- Subramanian, A., Krishnan, U. M., & Sethuraman, S. (2009). Development of biomaterial scaffold for nerve tissue engineering: Biomaterial mediated neural regeneration. Journal of Biomedical Science, 16, 108. https://doi.org/10.1186/1423-0127-16-108
- Sun, W., Liu, Y., Miao, L., Wang, Y., Ren, S., Yang, X., Hu, Y., & Chen, X. (2016). Controlled release of recombinant human cementum protein 1 from electrospun multiphasic scaffold for cementum regeneration. International Journal of Nanomedicine, 11, 3145–3158. https://doi.org/10.2147/IJN.S104324
- Tao, J., Hu, Y., Wang, S., Zhang, J., Liu, X., Gou, Z., Cheng, H., Liu, Q., Zhang, Q., You, S., & Gou, M. (2017). A 3D-engineered porous conduit for peripheral nerve repair. Scientific Reports, 7(April), 1–13. https://doi.org/10.1038/srep46038
- Tse, R., & Ko, J. H. (2012). Nerve glue for upper extremity reconstruction. Hand Clinics, 28(4), 529–540. https://doi.org/10.1016/j.hcl.2012.08.006
- Vijayavenkataraman, S., Kannan, S., Cao, T., Fuh, J. Y. H., Sriram, G., & Lu, W. F. (2019). 3D-Printed PCL/PPy conductive scaffolds as three-dimensional porous nerve guide conduits (NGCs) for peripheral nerve injury repair. Frontiers in Bioengineering and Biotechnology, 7(October), 1–14. https://doi.org/10.3389/fbioe.2019.00266
- Vo, T. N., Kasper, F. K., & Mikos, A. G. (2013). Strategies for controlled delivery of growth factors and cells for bone regeneration. Advanced Drug Delivery Reviews, 64(12), 1292–1309. https://doi.org/10.1016/j.addr.2012.01.016.Strategies
- Wang, J., Cheng, Y., Chen, L., Zhu, T., Ye, K., Jia, C., Wang, H., Zhu, M., Fan, C., & Mo, X. (2019). In vitro and in vivo studies of electroactive reduced graphene oxide-modified nanofiber scaffolds for peripheral nerve regeneration. Acta Biomaterialia, 84, 98–113. https://doi.org/10.1016/j.actbio.2018.11.032
- Yan, J., Wang, F., Chen, J., Liu, T., & Zhang, T. (2016). Preparation and characterization of irinotecan loaded cross-linked bovine serum albumin beads for liver cancer chemoembolization therapy. International Journal of Polymer Science, 2016, 1–8. https://doi.org/10.1155/2016/9651486
- Yilmaz, E., Ocsoy, I., Ozdemir, N., & Soylak, M. (2016). Bovine serum albumin-Cu(II) hybrid nanoflowers: An effective adsorbent for solid-phase extraction and slurry sampling flame atomic absorption spectrometric analysis of cadmium and lead in water, hair, food, and cigarette samples. Analytica Chimica Acta, 906, 110–117. https://doi.org/10.1016/j.aca.2015.12.001
- Zhang, W., Xu, B., Zhang, Y., & Luo, Y. (2014). Evaluation of extracellular matrix-based nerve conduits for long-gap peripheral nerve repair in a goat model. Journal of Biomaterials and Tissue Engineering, 4(12), 1063–1072. https://doi.org/10.1166/jbt.2014.1252
- Zhang, Z., Zhang, Y., He, L., Yang, Y., Liu, S., Wang, M., Fang, S., & Fu, G. (2015). A feasible synthesis of Mn3(PO4)2@BSA nanoflowers and its application as the support nanomaterial for Pt catalyst. Journal of Power Sources, 284, 170–177. https://doi.org/10.1016/j.jpowsour.2015.03.011
- Zhao, Y., Zhang, Q., Zhao, L., Gan, L., Yi, L., Zhao, Y., Jingling, X., Luo, L., Du, Q., Geng, R., Sun, Z., Benkirane-Jessel, N., Chen, P., Li, Y., & Chen, Y. (2017). Enhanced peripheral nerve regeneration by a high surface area to volume ratio of nerve conduits fabricated from hydroxyethyl cellulose/soy protein composite sponges. ACS Omega, 2(11), 7471–7481. https://doi.org/10.1021/acsomega.7b01003
- Zhu, S., Zhu, Q., Liu, X., Yang, W., Jian, Y., Zhou, X., He, B., Gu, L., Yan, L., Lin, T., Xiang, J., & Qi, J. (2016). Three-dimensional reconstruction of the microstructure of human acellular nerve allograft. Scientific Reports, 6(August), 30694. https://doi.org/10.1038/srep30694
