[en] For tissue engineering of skeletal muscles, there is a need for biomaterials which do not only allow cell attachment, proliferation, and differentiation, but also support the physiological conditions of the tissue. Next to the chemical nature and structure of the biomaterial, its response to the application of biophysical stimuli, such as mechanical deformation or application of electrical pulses, can impact in vitro tissue culture. In this study, gelatin methacryloyl (GelMA) is modified with hydrophilic 2-acryloxyethyltrimethylammonium chloride (AETA) and 3-sulfopropyl acrylate potassium (SPA) ionic comonomers to obtain a piezoionic hydrogel. Rheology, mass swelling, gel fraction, and mechanical characteristics are determined. The piezoionic properties of the SPA and AETA-modified GelMA are confirmed by a significant increase in ionic conductivity and an electrical response as a function of mechanical stress. Murine myoblasts display a viability of >95% after 1 week on the piezoionic hydrogels, confirming their biocompatibility. The GelMA modifications do not influence the fusion capacity of the seeded myoblasts or myotube width after myotube formation. These results describe a novel functionalization providing new possibilities to exploit piezo-effects in the tissue engineering field.
Disciplines :
Materials science & engineering
Author, co-author :
Burattini, Margherita ; Tissue Engineering Lab, Dep. Development and Regeneration, KU Leuven Kulak, Kortrijk, 8500, Belgium ; Dep. Of Surgical Sciences, Dentistry and Maternity, University of Verona, Verona, 37129, Italy
Lippens, Robrecht; Polymer Chemistry & Biomaterials Group, Center of Macromolecular Chemistry (CMaC), Dep. Of Organic and Macromolecular Chemistry, Ghent University (UGent), Ghent, 9000, Belgium
Baleine, Nicolas ; Université de Mons - UMONS > Faculté des Science > Service des Matériaux Polymères et Composit
Gerard, Melanie; Tissue Engineering Lab, Dep. Development and Regeneration, KU Leuven Kulak, Kortrijk, 8500, Belgium
Van Meerssche, Joeri ; Polymer Chemistry & Biomaterials Group, Center of Macromolecular Chemistry (CMaC), Dep. Of Organic and Macromolecular Chemistry, Ghent University (UGent), Ghent, 9000, Belgium
Geeroms, Chloë ; Polymer Chemistry & Biomaterials Group, Center of Macromolecular Chemistry (CMaC), Dep. Of Organic and Macromolecular Chemistry, Ghent University (UGent), Ghent, 9000, Belgium
ODENT, Jérémy ; Université de Mons - UMONS > Faculté des Sciences > Service des Matériaux Polymères et Composites
Raquez, Jean-Marie ; Université de Mons - UMONS > Faculté des Sciences > Service des Matériaux Polymères et Composites
Van Vlierberghe, Sandra; Polymer Chemistry & Biomaterials Group, Center of Macromolecular Chemistry (CMaC), Dep. Of Organic and Macromolecular Chemistry, Ghent University (UGent), Ghent, 9000, Belgium
Thorrez, Lieven ; Tissue Engineering Lab, Dep. Development and Regeneration, KU Leuven Kulak, Kortrijk, 8500, Belgium
R400 - Institut de Recherche en Science et Ingénierie des Matériaux
Funding text :
This work was funded by Interreg 3D4Med, co‐financed by the European Regional Development Fund, the provinces of East‐ and West‐Flanders and the Hermes fund, and KU Leuven C24E/20/067. J.‐M.R. is a senior research associate at F.R.S.‐F.N.R.S. (Belgium).This work was funded by Interreg 3D4Med, co-financed by the European Regional Development Fund, the provinces of East- and West-Flanders and the Hermes fund, and KU Leuven C24E/20/067. J.-M.R. is a senior research associate at F.R.S.-F.N.R.S. (Belgium).
J. M. Grasman, M. J. Zayas, R. Page, G. D. Pins, Acta Biomater. 2016, 25, 2.
J. Liu, D. Saul, K. O. Böker, J. Ernst, W. Lehman, A. F. Schilling, Biomed. Res. Int. 2018, 2018, 1984879.
B. E. Pollot, B. T. Corona, Methods Mol. Biol. 2016, 1460, 19.
N. J. Turner, S. F. Badylak, Cell Tissue Res. 2012, 347, 759.
S. Ostrovidov, V. Hosseini, S. Ahadian, T. Fujie, S. P. Parthiban, M. Ramalingam, H. Bae, H. Kaji, A. Khademhosseini, Tissue Eng., Part B 2014, 20, 403.
D. W. J. Van Der Schaft, A. C. C. Van Spreeuwel, K. J. M. Boonen, M. L. P. Langelaan, C. V. C. Bouten, F. P. T. Baaijens, J. Vis. Exp. 2013, 73, e4267.
H. H. Vandenburgh, Ann. N. Y. Acad. Sci. 2002, 961, 201.
D. Gholobova, L. Decroix, V. Van Muylder, L. Desender, M. Gerard, G. Carpentier, H. Vandenburgh, L. Thorrez, Tissue Eng., Part A 2015, 21, 2548.
D. Gholobova, M. Gerard, L. Decroix, L. Desender, N. Callewaert, P. Annaert, L. Thorrez, Sci. Rep. 2018, 8, 1.
D. Gholobova, L. Terrie, K. Mackova, L. Desender, G. Carpentier, M. Gerard, L. Hympanova, J. Deprest, L. Thorrez, Biofabrication 2020, 12, 035021.
P. H. U. Lee, H. H. Vandenburgh, Tissue Eng., Part A 2013, 19, 2147.
L. Thorrez, K. Disano, J. Shansky, H. Vandenburgh, Front. Physiol. 2018, 9, 1076.
L. Tytgat, L. Van Damme, J. Van Hoorick, H. Declercq, H. Thienpont, H. Ottevaere, P. Blondeel, P. Dubruel, S. van Vlierberghe, Acta Biomater. 2019, 94, 340.
K. Yue, G. Trujillo-De Santiago, M. M. Alvarez, A. Tamayol, N. Annabi, A. Khademhosseini, Biomaterials 2015, 73, 254.
J. Van Hoorick, L. Tytgat, A. Dobos, H. Ottevaere, J. Van Erps, H. Thienpont, A. Ovsianikov, P. Dubruel, S. van Vlierberghe, Acta Biomater. 2019, 97, 46.
M. Zhu, Y. Wang, G. Ferracci, J. Zheng, N.-J. Cho, B. H. Lee, Sci. Rep. 2019, 9, 1.
A.n I. Van Den Bulcke, B. Bogdanov, N. De Rooze, E. H. Schacht, M. Cornelissen, H. Berghmans, Biomacromolecules 2000, 1, 31.
A. Ito, Y. Yamamoto, M. Sato, K. Ikeda, M. Yamamoto, H. Fujita, E. Nagamori, Y. Kawabe, M. Kamihira, Sci. Rep. 2014, 4, 1.
R. D. Breukers, K. J. Gilmore, M. Kita, K. K. Wagner, M. J. Higgins, S. E. Moulton, G. M. Clark, D. L. Officer, R. M. I. Kapsa, G. G. Wallace, J. Biomed. Mater. Res. A 2010, 95A, 256.
R. Dong, P. X. Ma, B. Guo, Biomaterials 2020, 229, 119584.
J. Odent, T. J. Wallin, W. Pan, K. Kruemplestaedter, R. F. Shepherd, E. P. Giannelis, Adv. Funct. Mater. 2017, 27, 1701807.
Y. Dobashi, D. Yao, Y. Petel, T. N. Nguyen, M. S. Sarwar, Y. Thabet, C. L. W. Ng, E. Scabeni Glitz, G. T. M. Nguyen, C. Plesse, F. Vidal, C. A. Michal, J. D. W. Madden, Science (1979) 2022, 376, 502.
J. Heikenfeld, A. Jajack, J. Rogers, P. Gutruf, L. Tian, T. Pan, R. Li, M. Khine, J. Kim, J. Wang, J. Kim, Lab Chip 2018, 18, 217.
T. Iwazumi, M. Noble, Int. J. Cardiol. 1989, 24, 267.
A. Zaszczynska, P. Sajkiewicz, A. Gradys, Polymers (Basel) 2020, 12, 161.
D.-M. Shin, S. W. Hong, Y.-H. Hwang, Nanomaterials 2020, 10, 123.
C. Ribeiro, V. Sencadas, D. M. Correia, S. Lanceros-Méndez, Colloids Surf., B 2015, 136, 46.
N. A. Kamel, Biophys. Rev. 2022, 14, 717.
J. Odent, N. Baleine, V. Biard, Y. Dobashi, C. Vancaeyzeele, G. T. M. Nguyen, J. D. W. Madden, C. Plesse, J.-M. Raquez, Adv. Funct. Mater. 2022, 33, 2210485.
A. I. van Den Bulcke, B. Bogdanov, N. De Rooze, E. H. Schacht, M. Cornelissen, H. Berghmans, Biomacromolecules 2000, 1, 31.
L. Tytgat, M. Markovic, T. H. Qazi, M. Vagenende, F. Bray, J. C. Martins, C. Rolando, H. Thienpont, H. Ottevaere, A. Ovsianikov, P. Dubruel, S. Van Vlierberghe, J. Mater. Chem. B 2019, 7, 3100.
K. J. M. Boonen, M. L. P. Langelaan, R. B. Polak, D. W. J. Van Der Schaft, F. P. T. Baaijens, M. J. Post, J. Biomech. 2010, 43, 1514.
M. L. P. Langelaan, K. J. M. Boonen, K. Y. Rosaria-Chak, D. W. J. van derSchaft, M. J. Post, F. P. T. Baaijens, Ann. Am. Thorac. Soc. 2010, 12, 181.
Y. Wu, Y. X. Chen, J. Yan, D. Quinn, P. Dong, S. W. Sawyer, P. Soman, Acta Biomater. 2016, 33, 122.
S. W. Sawyer, P. Dong, S. Venn, A. Ramos, D. Quinn, J. A. Horton, P. Soman, Biomed. Phys. Eng. Express 2018, 4,015005.
I. Van Nieuwenhove, A. Salamon, K. Peters, G.-J. Graulus, J. C. Martins, D. Frankel, K. Kersemans, F. De Vos, S. Van Vlierberghe, P. Dubruel, Carbohydr. Polym. 2016, 152, 129.
R. Luo, H. Li, Acta Biomater. 2009, 5, 2920.
P. Li, N. H. Kim, D. Hui, K. Y. Rhee, J. H. Lee, Appl. Clay Sci. 2009, 46, 414.
F. Tan, X. Xu, T. Deng, M. Yin, X. Zhang, J. Wang, Biomed. Mater. 2012, 7,055009.
Q. Xing, K. Yates, C. Vogt, Z. Qian, M. C. Frost, F. Zhao, Sci. Rep. 2014, 4, 4706.
G.-J. Graulus, A. Mignon, S. Van Vlierberghe, H. Declercq, K. Fehér, M. Cornelissen, J. C. Martins, P. Dubruel, Eur. Polym. J. 2015, 72, 494.
J. Van Hoorick, P. Gruber, M. Markovic, M. Tromayer, J. Van Erps, H. Thienpont, R. Liska, A. Ovsianikov, P. Dubruel, S. Van Vlierberghe, Biomacromolecules 2017, 18, 3260.
J. Van Hoorick, H. Declercq, A. De Muynck, A. Houben, L. Van Hoorebeke, R. Cornelissen, J. Van Erps, H. Thienpont, P. Dubruel, S. Van Vlierberghe, J. Mater. Sci.: Mater. Med. 2015, 26, 247.
S. Van Vlierberghe, B. Fritzinger, J. C. Martins, P. Dubruel, Appl. Spectrosc. 2010, 64, 1176.
N. Rajabi, M. Kharaziha, R. Emadi, A. Zarrabi, H. Mokhtari, S. Salehi, J. Colloid Interface Sci. 2020, 564, 155.
Q. Huang, Y. Zou, M. C. Arno, S. Chen, T. Wang, J. Gao, A. P. Dove, J. Du, Chem. Soc. Rev. 2017, 46, 6255.
X. Chen, W. Du, Z. Cai, S. Ji, M. Dwivedi, J. Chen, G. Zhao, J. Chu, ACS Appl. Mater. Interfaces 2020, 12, 2162.
W. Kim, H. Lee, J. Lee, A. Atala, J. J. Yoo, S. J. Lee, G. H. Kim, Biomaterials 2020, 230, 119632.
L. Tytgat, L. Van Damme, J. Van Hoorick, H. Declercq, H. Thienpont, H. Ottevaere, P. Blondeel, P. Dubruel, S. Van Vlierberghe, Acta Biomater. 2019, 94, 340.
N. Atale, S. Gupta, U. C. S. Yadav, V. Rani, J. Microsc. 2014, 255, 7.
P. Bajaj, B. Reddy, L. Millet, C. Wei, P. Zorlutuna, G. Bao, R. Bashir, Integr. Biol. 2011, 3, 897.
R. Mccoll, M. Nkosi, C. Snyman, C. Niesler, BioTechniques 2016, 61, 323.