DOI QR코드

DOI QR Code

The effect of collagen/polycaprolactone fibrous scaffold decorated with graphene nanoplatelet and low-frequency electromagnetic field on neuronal gene expression by stem cells

  • Moraveji, Marzie (National Cell Bank of Iran, Pasteur Institute of Iran) ;
  • Keshvari, Hamid (Department of Biomedical Engineering, Amirkabir University of Technology) ;
  • Karkhaneh, Akbar (Department of Biomedical Engineering, Amirkabir University of Technology) ;
  • Bonakdar, Shahin (National Cell Bank of Iran, Pasteur Institute of Iran) ;
  • Hadi, Amin (Cellular and Molecular Research Center, Yasuj University of Medical Sciences) ;
  • Haghighipour, Nooshin (National Cell Bank of Iran, Pasteur Institute of Iran)
  • Received : 2020.09.29
  • Accepted : 2021.03.16
  • Published : 2021.06.25

Abstract

This study aimed to develop a collagen/polycaprolactone (CP) fibrous scaffold decorated with Graphene (Gr) nanoplatelets (Gr-CP). In previous studies, accessibility of cells to the surface of Gr nanoplatelet was missed. Nanofibers were prepared by electrospinning which sprayed Gr nanoplatelets (1 wt.%) to synthesize the Gr-CP scaffold. Fourier transform infrared spectroscopy (FTIR) was utilized for investigation of chemical structure. Tensile tests were performed to study the influence of Gr on the mechanical properties of scaffolds. Cell differentiation was analyzed based on MAP2 and TUJ1 expression levels using real-time PCR technique in 6 groups. The variables examined in this experiment was the neural differentiating chemical medium, low-frequency electromagnetic field (LFEMF; 50Hz, 1mT) and Gr. Based on the results, Young's modulus, tensile strength and work of fracture ratio of the Gr-CP were 1.68, 2.41 and 1.42 times higher than those of the CP scaffold, respectively. MTT assay outcomes were indicative of scaffold cytocompatibility. The group treated with all three factors exhibited the highest MAP2 expression level compared to other groups. Based on the obtained results, exposing stem cells to the combined treatment of Gr and LFEMF can be used as a promising method to induce neuronal differentiation.

Keywords

Acknowledgement

This work has been financially supported by Iran National Science Foundation (INSF, grant number: 92027763) and was approved by the Pasteur institute of Iran.

References

  1. Acar, H., Garifullin, R. and Guler, M.O. (2011), "Self-assembled template-directed synthesis of one-dimensional silica and titania nanostructures", Langmuir, 27(3), 1079-1084. https://doi.org/10.1021/la104518g.
  2. Alegret, N., Dominguez-Alfaro, A., Gonzalez-Dominguez, J.M., Arnaiz, B., Cossio, U., Bosi, S., Vazquez, E., Ramos-Cabrer, P., Mecerreyes, D. and Prato, M. (2018), "Three-Dimensional Conductive Scaffolds as Neural Prostheses Based on Carbon Nanotubes and Polypyrrole", ACS Appl. Mater. Interf., 10(50), 43904-43914. doi:https://doi.org/10.1021/acsami.8b16462.
  3. Barati, A., Adeli, M.M. and Hadi, A. (2020a), "Static torsion of bidirectional functionally graded microtube based on the couple stress theory under magnetic field", Int. J. Appl. Mech., 12(02), 2050021. https://doi.org/10.1142/S1758825120500210.
  4. Barati, A., Hadi, A., Nejad, M.Z. and Noroozi, R. (2020b), "On vibration of bi-directional functionally graded nanobeams under magnetic field", Mech. Based Des. Struct., 1-18. https://doi.org/10.1080/15397734.2020.1719507.
  5. Bedard, A. and Parent, A. (2004), "Evidence of newly generated neurons in the human olfactory bulb", Dev. Brain Res., 151(1), 159-168. https://doi.org/10.1016/j.devbrainres.2004.03.021.
  6. Binhi, V., Alipov, Y.D. and Belyaev, I.Y. (2001), "Effect of static magnetic field on E. coli cells and individual rotations of ion-protein complexes", Bioelectromagnetics, 22(2), 79-86. https://doi.org/10.1002/1521-186X(200102)22:2%3C79::AIDBEM1009%3E3.0.CO;2-7.
  7. Bojnordi, M.N., Azizi, H., Skutella, T., Movahedin, M., Pourabdolhossein, F., Shojaei, A. and Hamidabadi, H.G. (2016), "Differentiation of Spermatogonia Stem Cells into Functional Mature Neurons Characterized with Differential Gene Expression", Mole. Neurobiol., 1-7. https://doi.org/10.1007/s12035-016-0097-7.
  8. Buchachenko, A.L., Lukzen, N.N. and Pedersen, J.B. (2007), "On the magnetic field and isotope effects in enzymatic phosphorylation", Chem. Phys. Lett., 434(1-3), 139-143. https://doi.org/10.1016/j.cplett.2006.12.019.
  9. Callahan, L.A.S., Xie, S., Barker, I.A., Zheng, J., Reneker, D.H., Dove, A.P. and Becker, M.L. (2013), "Directed differentiation and neurite extension of mouse embryonic stem cell on aligned poly (lactide) nanofibers functionalized with YIGSR peptide", Biomaterials, 34(36), 9089-9095. https://doi.org/10.1016/j.biomaterials.2013.08.028.
  10. Capkin, M., Cakmak, S., Kurt, F.O., Gumusderelioglu, M., Sen, B.H., Turk, B.T. and Deliloglu-Gurhan, S.I. (2012), "Random/aligned electrospun PCL/PCL-collagen nanofibrous membranes: Comparison of neural differentiation of rat AdMSCs and BMSCs", Biomed. Mater., 7(4), 045013. https://doi.org/10.1088/1748-6041/7/4/045013.
  11. Cheng, K. and Zou, C. (2006), "Electromagnetic field effect on separation of nucleotide sequences and unwinding of a double helix during DNA replication", Med. Hypotheses, 66(1), 148-153. https://doi.org/10.1016/j.mehy.2005.07.007.
  12. Cho, H., Seo, Y.K., Yoon, H.H., Kim, S.C., Kim, S.M., Song, K.Y. and Park, J.K. (2012), "Neural stimulation on human bone marrow-derived mesenchymal stem cells by extremely low frequency electromagnetic fields", Biotechnol. Prog., 28(5), 1329-1335. https://doi.org/10.1002/btpr.1607.
  13. Coates, J. (2000), "Interpretation of infrared spectra, a practical approach", In: Encyclopedia of analytical chemistry: applications, theory and instrumentation. https://doi.org/10.1002/9780470027318.a5606.
  14. Damink, L.O., Dijkstra, P., Van Luyn, M., Van Wachem, P., Nieuwenhuis, P. and Feijen, J. (1995), "Glutaraldehyde as a crosslinking agent for collagen-based biomaterials", J. Mater. Sci.-Mater. M., 6(8), 460-472. https://doi.org/10.1007/BF00123371.
  15. Driscoll, N., Richardson, A.G., Maleski, K., Anasori, B., Adewole, O., Lelyukh, P., Escobedo, L., Cullen, D.K., Lucas, T.H., Gogotsi, Y. and Vitale, F. (2018), "Two-dimensional Ti3C2 MXene for high-resolution neural interfaces", ACS Nano, 12(10), 10419-10429. https://doi.org/10.1021/acsnano.8b06014.
  16. Festjens, N., Kalai, M., Smet, J., Meeus, A., Van Coster, R., Saelens, X. and Vandenabeele, P. (2006), "Butylated hydroxyanisole is more than a reactive oxygen species scavenger", Cell Death Differ., 13(1), 166-169. https://doi.org/10.1038/sj.cdd.4401746.
  17. Gaetani, R., Ledda, M., Barile, L., Chimenti, I., De Carlo, F., Forte, E., Ionta, V.,Giuliani, L., D'Emilia, E., Frati, G., Miraldi, F., Pozzi, D., Messina, E., Grimaldi, S., Giacomello, A. and Lisi, A. (2009), "Differentiation of human adult cardiac stem cells exposed to Extremely Low Frequency Electromagnetic Fields", Cardiovasc. Res., 82(3), 411-420. https://doi.org/10.1093/cvr/cvp067.
  18. Garrudo, F.F., Chapman, C.A., Hoffman, P.R., Udangawa, R.W., Silva, J.C., Mikael, P.E., Rodrigues, C.A.V., Cabral, J.M.S., Morgado, J.M.F., Ferreira, F.C. and Lindhardt, R.J. (2019), "Polyaniline-polycaprolactone blended nanofibers for neural cell culture", Eur. Polym. J., 117, 28-37. https://doi.org/10.1016/j.eurpolymj.2019.04.048.
  19. Ginestra, P. (2019), "Manufacturing of polycaprolactone-Graphene fibers for nerve tissue engineering", J. Mech. Behav. Biomed. Mater., 100, 103387. https://doi.org/10.1016/j.jmbbm.2019.103387.
  20. Golafshan, N., Kharaziha, M. and Fathi, M. (2017), "Tough and conductive hybrid graphene-PVA: Alginate fibrous scaffolds for engineering neural construct", Carbon, 111, 752-763. https://doi.org/10.1016/j.carbon.2016.10.042.
  21. Gupta, P., Agrawal, A., Murali, K., Varshney, R., Beniwal, S., Manhas, S., Roy, P. and Lahiri, D. (2019), "Differential neural cell adhesion and neurite outgrowth on carbon nanotube and graphene reinforced polymeric scaffolds", Mater. Sci. Eng. C, 97, 539-551. https://doi.org/10.1016/j.msec.2018.12.065.
  22. He, B., Yuan, X. and Jiang, D. (2014), "Molecular self-assembly guides the fabrication of peptide nanofiber scaffolds for nerve repair", RSC Adv., 4(45), 23610-23621. https://doi.org/10.1039/C4RA01826E.
  23. Huo, Y., Qiu, W.-Y., Pan, Q., Yao, Y.-F., Xing, K. and Lou, M.F. (2009), "Reactive oxygen species (ROS) are essential mediators in epidermal growth factor (EGF)-stimulated corneal epithelial cell proliferation, adhesion, migration, and wound healing", Exp. Eye Res., 89(6), 876-886. https://doi.org/10.1016/j.exer.2009.07.012.
  24. Jazayeri, M., Shokrgozar, M.A., Haghighipour, N., Bolouri, B., Mirahmadi, F. and Farokhi, M. (2016), "Effects of electromagnetic stimulation on gene expression of mesenchymal stem cells and repair of bone lesions", Cell. J. (Yakhteh), 19(1), 34. https://doi.org/10.22074%2Fcellj.2016.4870. https://doi.org/10.22074%2Fcellj.2016.4870
  25. Kavand, H., Haghighipour, N., Zeynali, B., Seyedjafari, E. and Abdemami, B. (2016), "Extremely low frequency electromagnetic field in mesenchymal stem cells gene regulation: chondrogenic markers evaluation", Artif. Organs., 40(10), 929-937. https://doi.org/10.1111/aor.12696.
  26. Kenry, L.W., Loh, K.P. and Lim, C.T. (2018), "When stem cells meet graphene: opportunities and challenges in regenerative medicine", Biomaterials, 155, 236-250. https://doi.org/10.1016/j.biomaterials.2017.10.004.
  27. Khoram, M.M., Hosseini, M., Hadi, A. and Shishehsaz, M. (2020), "Bending analysis of bidirectional FGM Timoshenko nanobeam subjected to mechanical and magnetic forces and resting on Winkler-Pasternak foundation", Int. J. Appl. Mech., 12(8), 2050093. https://doi.org/10.1142/S1758825120500933.
  28. Lanza, R., Langer, R. and Vacanti, J.P. (2013), Principles of Tissue Engineering (4th Edition ed.), Academic press, Massachusetts, U.S.A.
  29. Laurence, J.A., French, P.W., Lindner, R.A. and Mckenzie, D.R. (2000), "Biological effects of electromagnetic fields-Mechanisms for the effects of pulsed microwave radiation on protein conformation", J. Theoretic. Biol., 206(2), 291-298. https://doi.org/10.1006/jtbi.2000.2123
  30. Le Belle, J.E., Orozco, N.M., Paucar, A.A., Saxe, J.P., Mottahedeh, J., Pyle, A.D., Wu, H. and Kornblum, H.I. (2011), "Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner", Cell Stem Cell, 8(1), 59-71. https://doi.org/10.1016/j.stem.2010.11.028.
  31. Lee, Y.-J., Jang, W., Im, H. and Sung, J.-S. (2015), "Extremely low frequency electromagnetic fields enhance neuronal differentiation of human mesenchymal stem cells on graphenebased substrates", Curr. Appl. Phys., 15, S95-S102. https://doi.org/10.1016/j.cap.2015.04.017.
  32. Levin, M. (2009), "Bioelectric mechanisms in regeneration: unique aspects and future perspectives", In: Seminars in Cell & Developmental Biology (Vol. 20, No. 5, pp. 543-556), Academic Press. https://doi.org/10.1016/j.semcdb.2009.04.013
  33. Li, N., Zhang, X., Song, Q., Su, R., Zhang, Q., Kong, T., Liu, L., Jin, G., Tang, M. and Cheng, G. (2011), "The promotion of neurite sprouting and outgrowth of mouse hippocampal cells in culture by graphene substrates", Biomaterials, 32(35), 9374-9382. 10.1016/j.biomaterials.2011.08.065.
  34. Li, W., Guo, Y., Wang, H., Shi, D., Liang, C., Ye, Z., Qing, F. and Gong, J. (2008), "Electrospun nanofibers immobilized with collagen for neural stem cells culture", J. Mater. Sci. Mater. M., 19(2), 847-854. https://doi.org/10.1007/s10856-007-3087-5.
  35. Li, Z., Zhang, Y. and Wang, Y. (2003), "Synthesis and characterization of N-benzoyl-N'-carboxyalkyl substituted thiourea derivatives", Phosphorus Sulfur, 178(2), 293-297. https://doi.org/10.1080/10426500307952.
  36. Ma, Q., Chen, C., Deng, P., Zhu, G., Lin, M., Zhang, L., Xu, S., He, M., Lu, Y., Duan, W., Pi, H., Cao, Z., Pei, L., Li, M., Liu, C., Zhang, Y., Zhong, M., Zhou, Z. and Yu, Z. (2016), "Extremely low-frequency electromagnetic fields promote in vitro neuronal differentiation and neurite outgrowth of embryonic neural stem cells via up-regulating TRPC1", PloS one, 11(3), e0150923-e0150923. https://doi.org/10.1371/journal.pone.0150923.
  37. Madec, F., Billaudel, B., de Sauvage, R.C., Sartor, P. and Veyret, B. (2003), "Effects of ELF and static magnetic fields on calcium oscillations in islets of Langerhans", Bioelectrochemistry, 60(1-2), 73-80. https://doi.org/10.1016/S1567-5394(03)00049-5.
  38. Magaz, A., Spencer, B.F., Hardy, J.G., Li, X., Gough, J.E. and Blaker, J.J. (2020), "Modulation of neuronal cell affinity on PEDOT-PSS nonwoven silk scaffolds for neural tissue engineering", ACS Biomater. Sci. Eng., 6(12), 6906-6916. https://doi.org/10.1021/acsbiomaterials.0c01239.
  39. Markov, M. and Pilla, A. (1997), "Weak static magnetic field modulation of myosin phosphorylation in a cell-free preparation: calcium dependence", Bioelectrochem. Bioenergetic., 43(2), 233-238. https://doi.org/10.1016/S0302-4598(96)02226-X.
  40. Mohabatpour, F., Karkhaneh, A. and Sharifi, A.M. (2016), "A hydrogel/fiber composite scaffold for chondrocyte encapsulation in cartilage tissue regeneration", RSC Adv., 6(86), 83135-83145. https://doi.org/10.1039/C6RA15592H.
  41. Moraveji, M., Haghighipour, N., Keshvari, H., Abbariki, T.N., Shokrgozar, M.A. and Amanzadeh, A. (2016), "Effect of extremely low frequency electromagnetic field on MAP2 and Nestin gene expression of hair follicle dermal papilla cells", Int. J. Artificial Organs, 39(6), 294-299. https://doi.org/10.5301/ijao.5000512.
  42. Muyonga, J., Cole, C. and Duodu, K. (2004), "Fourier transform infrared (FTIR) spectroscopic study of acid soluble collagen and gelatin from skins and bones of young and adult Nile perch (Lates niloticus)", Food Chem., 86(3), 325-332. https://doi.org/10.1016/j.foodchem.2003.09.038.
  43. Najafzadeh, M., Adeli, M.M., Zarezadeh, E. and Hadi, A. (2020), "Torsional vibration of the porous nanotube with an arbitrary cross-section based on couple stress theory under magnetic field", Mech. Based Des. Struct., 1-15. https://doi.org/10.1080/15397734.2020.1733602.
  44. Norizadeh-Abbariki, T., Mashinchian, O., Shokrgozar, M.A., Haghighipour, N., Sen, T. and Mahmoudi, M. (2014), "Superparamagnetic nanoparticles direct differentiation of embryonic stem cells into skeletal muscle cells", J. Biomater. Tissue Eng., 4(7), 579-585. https://doi.org/10.1166/jbt.2014.1205.
  45. Ongaro, A., Pellati, A., Bagheri, L., Fortini, C., Setti, S. and De Mattei, M. (2014), "Pulsed electromagnetic fields stimulate osteogenic differentiation in human bone marrow and adipose tissue derived mesenchymal stem cells", Bioelectromagnetics, 35(6), 426-436. https://doi.org/10.1002/bem.21862.
  46. Ou, L., Song, B., Liang, H., Liu, J., Feng, X., Deng, B., Sun, T. and Shao, L. (2016), "Toxicity of graphene-family nanoparticles: a general review of the origins and mechanisms", Particle Fibre Toxicol., 13(1), 57. https://doi.org/10.1186/s12989-016-0168-y.
  47. Ouyang, Y., Huang, C., Zhu, Y., Fan, C. and Ke, Q. (2013), "Fabrication of seamless electrospun collagen/PLGA conduits whose walls comprise highly longitudinal aligned nanofibers for nerve regeneration", J. Biomed. Nanotechnol., 9(6), 931-943. https://doi.org/10.1166/jbn.2013.1605.
  48. O zgun, A., Marote, A., Behie, L.A., Salgado, A. and Garipcan, B. (2019), "Extremely low frequency magnetic field induces human neuronal differentiation through NMDA receptor activation", J. Neural Transm., 126(10), 1281-1290. https://doi.org/10.1007/s00702-019-02045-5.
  49. Park, J.-E., Seo, Y.-K., Yoon, H.-H., Kim, C.-W., Park, J.-K. and Jeon, S. (2013), "Electromagnetic fields induce neural differentiation of human bone marrow derived mesenchymal stem cells via ROS mediated EGFR activation", Neurochem. Int., 62(4), 418-424. https://doi.org/10.1016/j.neuint.2013.02.002.
  50. Park, S.Y., Park, J., Sim, S.H., Sung, M.G., Kim, K.S., Hong, B.H. and Hong, S. (2011), "Enhanced differentiation of human neural stem cells into neurons on graphene", Adv. Mater., 23(36), https://doi.org/10.1002/adma.201101503.
  51. Pereda, A.E. (2014), "Electrical synapses and their functional interactions with chemical synapses", Nat. Rev. Neurosci., 15(4), 250. https://doi.org/10.1038/nrn3708.
  52. Piacentini, R., Ripoli, C., Mezzogori, D., Azzena, G.B. and Grassi, C. (2008), "Extremely low-frequency electromagnetic fields promote in vitro neurogenesis via upregulation of Cav1-channel activity", J. Cell. Physiol., 215(1), 129-139. https://doi.org/10.1002/jcp.21293.
  53. Qin, X. and Wu, D. (2012), "Effect of different solvents on poly (caprolactone)(PCL) electrospun nonwoven membranes", J. Therm. Anal. Calorim., 107(3), 1007-1013. https://doi.org/10.1007/s10973-011-1640-4.
  54. Rajzer, I., Menaszek, E., Kwiatkowski, R., Planell, J.A. and Castano, O. (2014), "Electrospun gelatin/poly (ε-caprolactone) fibrous scaffold modified with calcium phosphate for bone tissue engineering", Mater. Sci. Eng. C, 44, 183-190. https://doi.org/10.1016/j.msec.2014.08.017.
  55. Raposio, E., Guida, C., Baldelli, I., Benvenuto, F., Curto, M., Paleari, L., Filippia, F., Fioccab, R., Robello. G. and Santi, P. (2007), "Characterization and induction of human preadipocytes", Toxicol. in Vitro, 21(2), 330-334. https://doi.org/10.1016/j.tiv.2006.09.022.
  56. Rastin, H., Zhang, B., Bi, J., Hassan, K., Tung, T.T. and Losic, D. (2020), "3D printing of cell-laden electroconductive bioinks for tissue engineering applications", J. Mater. Chem. B, 8(27), 5862-5876. https://doi.org/10.1039/D0TB00627K.
  57. Rastin, H., Zhang, B., Mazinani, A., Hassan, K., Bi, J., Tung, T.T. and Losic, D. (2020), "3D bioprinting of cell-laden electroconductive MXene nanocomposite bioinks", Nanoscale, 12(30), 16069-16080. https://doi.org/10.1039/D0NR02581J.
  58. Rohani Rad, E., Vahabi, H., Formela, K., Saeb, M.R. and Thomas, S. (2019), "Injectable poloxamer/graphene oxide hydrogels with well-controlled mechanical and rheological properties", Polym. Adv. Technol., 30(9), 2250-2260. https://doi.org/10.1002/pat.4654.
  59. Ryu, S. and Kim, B.-S. (2013), "Culture of neural cells and stem cells on graphene", Tissue Eng., 10(2), 39-46. https://doi.org/10.1007/s13770-013-0384-6.
  60. 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-εcaprolactone and a collagen/poly-ε-caprolactone blend", Biomaterials, 28(19), 3012-3025. https://doi.org/10.1016/j.biomaterials.2007.03.009.
  61. Sionkowska, A., Lewandowska, K. and Adamiak, K. (2020), "The influence of UV light on rheological properties of collagen extracted from silver carp skin", Materials, 13(19), 4453. https://doi.org/10.3390/ma13194453.
  62. Soleimani, A., Dastani, K., Hadi, A. and Naei, M.H. (2019), "Effect of out-of-plane defects on the postbuckling behavior of graphene sheets based on nonlocal elasticity theory", Steel Compos. Struct., Int. J., 30(6), 517-534. https://doi.org/10.12989/scs.2019.30.6.517.
  63. Szymanski, J.M., Jallerat, Q. and Feinberg, A.W. (2014), "ECM protein nanofibers and nanostructures engineered using surface-initiated assembly", J. Visual. Experiments: JoVE, (86), https://dx.doi.org/10.3791%2F51176. https://doi.org/10.3791%2F51176
  64. Teo, W.E. and Ramakrishna, S. (2006), "A review on electrospinning design and nanofibre assemblies", Nanotechnology, 17(14), R89. https://doi.org/10.1088/0957-4484/17/14/r01.
  65. Tonini, R., Baroni, M.D., Masala, E., Micheletti, M., Ferroni, A. and Mazzanti, M. (2001), "Calcium protects differentiating neuroblastoma cells during 50 Hz electromagnetic radiation", Biophys. J., 81(5), 2580-2589. https://doi.org/10.1016/S0006-3495(01)75902-4.
  66. Vasita, R. and Katti, D.S. (2006), "Nanofibers and their applications in tissue engineering", Int. J. Nanomed., 1(1), 15. https://dx.doi.org/10.2147%2Fnano.2006.1.1.15. https://doi.org/10.2147%2Fnano.2006.1.1.15
  67. Vijayavenkataraman, S., Thaharah, S., Zhang, S., Lu, W.F. and Fuh, J.Y.H. (2018), "3D-Printed PCL/rGO conductive scaffolds for peripheral nerve injury repair", Artif. Organs., 43(5), 515-523.https://doi.org/10.1111/aor.13360.
  68. Wang, Z., Sarje, A., Che, P.-L. and Yarema, K.J. (2009), "Moderate strength (0.23-0.28 T) static magnetic fields (SMF) modulate signaling and differentiation in human embryonic cells", BMC Genomics, 10(1), 356. https://doi.org/10.1186/1471-2164-10-356.
  69. Wychowaniec, J.K., Litowczenko, J., Tadyszak, K., Natu, V., Aparicio, C., Peplinska, B., Barsoumc, M.W., Otyepka, M. and Scheibe, B. (2020), "Unique cellular network formation guided by heterostructures based on reduced graphene oxide-Ti3C2Tx MXene hydrogels", Acta Biomater., 115, 104-115. https://doi.org/10.1016/j.actbio.2020.08.010.
  70. Xia, Y., Li, S., Nie, C., Zhang, J., Zhou, S., Yang, H., Li, M., Li, W., Cheng. C. and Haag, R. (2019), "A multivalent polyaniondispersed carbon nanotube toward highly bioactive nanostructured fibrous stem cell scaffolds", Appl. Mater. Today, 16, 518-528. https://doi.org/10.1016/j.apmt.2019.07.006.
  71. Xie, J., Willerth, S.M., Li,X., Macewan, M.R., Rader, A., Sakiyama-Elbert, S.E. and Xia, Y. (2009), "The differentiation of embryonic stem cells seeded on electrospun nanofibers into neural lineages", Biomaterials, 30(3), 354-362. https://doi.org/10.1016%2Fj.biomaterials.2008.09.046. https://doi.org/10.1016%2Fj.biomaterials.2008.09.046
  72. Yin, Y., Huang, P., Han, Z., Wei, G., Zhou, C., Wen, J., Su, B., Wang, X. and Wang, Y. (2014), "Collagen nanofibers facilitated presynaptic maturation in differentiated neurons from spinal-cord-derived neural stem cells through MAPK/ERK1/2-Synapsin I signaling pathway", Biomacromolecules, 15(7), 2449-2460. https://doi.org/10.1021/bm500321h.
  73. Yoshitani, M., Fukuda, S., Itoi, S.-i., Morino, S., Tao, H., Nakada, A., Inada, Y., Endo, K. and Nakamura, T. (2007), "Experimental repair of phrenic nerve using a polyglycolic acid and collagen tube", J. Thorac. Cardiov. Sur., 133(3), 726-732. e723. https://doi.org/10.1016/j.jtcvs.2006.08.089.
  74. Zhang, B., Wei, P., Zhou, Z. and Wei, T. (2016), "Interactions of graphene with mammalian cells: Molecular mechanisms and biomedical insights", Adv. Drug Deliver. Rev., 105, 145-162. https://doi.org/10.1016/j.addr.2016.08.009.
  75. Zhang, K., Zheng, H., Liang, S. and Gao, C. (2016), "Aligned PLLA nanofibrous scaffolds coated with graphene oxide for promoting neural cell growth", Acta Biomaterialia, 37, 131-142. https://doi.org/10.1016/j.actbio.2016.04.008.
  76. Zhang, Z., Klausen, L.H., Chen, M. and Dong, M. (2018), "Electroactive scaffolds for neurogenesis and myogenesis: Graphene-based nanomaterials", Small, 14(48), 1801983. https://doi.org/10.1002/smll.201801983.