Dielectrophoretically Aligned Carbon Nanotubes to Control Electrical and Mechanical Properties of Hydrogels to Fabricate Contractile Muscle Myofibers

Advanced MaterialsVolume 25, Issue 29 p. 4028-4034 Communication Dielectrophoretically Aligned Carbon Nanotubes to Control Electrical and Mechanical Properties of Hydrogels to Fabricate Contractile Muscle Myofibers Javier Ramón-Azcón, Javier Ramón-Azcón WPI-Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, JapanSearch for more papers by this authorSamad Ahadian, Samad Ahadian WPI-Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, JapanSearch for more papers by this authorMehdi Estili, Mehdi Estili Materials Processing Unit, National Institute for Materials Science (NIMS), Tsukuba 305-0047, JapanSearch for more papers by this authorXiaobin Liang, Xiaobin Liang WPI-Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, JapanSearch for more papers by this authorSerge Ostrovidov, Serge Ostrovidov WPI-Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, JapanSearch for more papers by this authorHirokazu Kaji, Hirokazu Kaji Department of Bioengineering and Robotics, Graduate School of Engineering, Tohoku University, Sendai 980-8579, JapanSearch for more papers by this authorHitoshi Shiku, Hitoshi Shiku Graduate School of Environmental Studies, Tohoku University, Sendai 980-8579, JapanSearch for more papers by this authorMurugan Ramalingam, Murugan Ramalingam WPI-Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, Japan Centre for Stem Cell Research, A unit of the Institute for Stem Cell Biology and Regenerative Medicine, Christian Medical College Campus, Vellore 632002, India, Institut National de la Santé Et de la Recherche Médicale U977, Faculté de Chirurgie Dentaire, Université de Strasbourg, Strasbourg 67085, FranceSearch for more papers by this authorKen Nakajima, Ken Nakajima WPI-Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, JapanSearch for more papers by this authorYoshio Sakka, Yoshio Sakka Materials Processing Unit, National Institute for Materials Science (NIMS), Tsukuba 305-0047, JapanSearch for more papers by this authorAli Khademhosseini, Corresponding Author Ali Khademhosseini [email protected] Department of Medicine, Center for Biomedical Engineering, Brigham and Women's Hospital, Harvard Medical School, Cambridge, Massachusetts 02139, USA, Harvard–MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA, Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, Massachusetts 02115, USA and Department of Maxillofacial Biomedical Engineering and Institute of Oral Biology, School of Dentistry, Kyung Hee University, Seoul 130-701, Republic of Korea WPI-Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, Japan Ali Khademhosseini, Department of Medicine, Center for Biomedical Engineering, Brigham and Women's Hospital, Harvard Medical School, Cambridge, Massachusetts 02139, USA, Harvard–MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA, Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, Massachusetts 02115, USA and Department of Maxillofacial Biomedical Engineering and Institute of Oral Biology, School of Dentistry, Kyung Hee University, Seoul 130-701, Republic of Korea Tomokazu Matsue, Graduate School of Environmental Studies, Tohoku University, Sendai 980-8579, Japan.Search for more papers by this authorTomokazu Matsue, Corresponding Author Tomokazu Matsue [email protected] Graduate School of Environmental Studies, Tohoku University, Sendai 980-8579, Japan WPI-Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, Japan Ali Khademhosseini, Department of Medicine, Center for Biomedical Engineering, Brigham and Women's Hospital, Harvard Medical School, Cambridge, Massachusetts 02139, USA, Harvard–MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA, Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, Massachusetts 02115, USA and Department of Maxillofacial Biomedical Engineering and Institute of Oral Biology, School of Dentistry, Kyung Hee University, Seoul 130-701, Republic of Korea Tomokazu Matsue, Graduate School of Environmental Studies, Tohoku University, Sendai 980-8579, Japan.Search for more papers by this author Javier Ramón-Azcón, Javier Ramón-Azcón WPI-Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, JapanSearch for more papers by this authorSamad Ahadian, Samad Ahadian WPI-Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, JapanSearch for more papers by this authorMehdi Estili, Mehdi Estili Materials Processing Unit, National Institute for Materials Science (NIMS), Tsukuba 305-0047, JapanSearch for more papers by this authorXiaobin Liang, Xiaobin Liang WPI-Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, JapanSearch for more papers by this authorSerge Ostrovidov, Serge Ostrovidov WPI-Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, JapanSearch for more papers by this authorHirokazu Kaji, Hirokazu Kaji Department of Bioengineering and Robotics, Graduate School of Engineering, Tohoku University, Sendai 980-8579, JapanSearch for more papers by this authorHitoshi Shiku, Hitoshi Shiku Graduate School of Environmental Studies, Tohoku University, Sendai 980-8579, JapanSearch for more papers by this authorMurugan Ramalingam, Murugan Ramalingam WPI-Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, Japan Centre for Stem Cell Research, A unit of the Institute for Stem Cell Biology and Regenerative Medicine, Christian Medical College Campus, Vellore 632002, India, Institut National de la Santé Et de la Recherche Médicale U977, Faculté de Chirurgie Dentaire, Université de Strasbourg, Strasbourg 67085, FranceSearch for more papers by this authorKen Nakajima, Ken Nakajima WPI-Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, JapanSearch for more papers by this authorYoshio Sakka, Yoshio Sakka Materials Processing Unit, National Institute for Materials Science (NIMS), Tsukuba 305-0047, JapanSearch for more papers by this authorAli Khademhosseini, Corresponding Author Ali Khademhosseini [email protected] Department of Medicine, Center for Biomedical Engineering, Brigham and Women's Hospital, Harvard Medical School, Cambridge, Massachusetts 02139, USA, Harvard–MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA, Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, Massachusetts 02115, USA and Department of Maxillofacial Biomedical Engineering and Institute of Oral Biology, School of Dentistry, Kyung Hee University, Seoul 130-701, Republic of Korea WPI-Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, Japan Ali Khademhosseini, Department of Medicine, Center for Biomedical Engineering, Brigham and Women's Hospital, Harvard Medical School, Cambridge, Massachusetts 02139, USA, Harvard–MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA, Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, Massachusetts 02115, USA and Department of Maxillofacial Biomedical Engineering and Institute of Oral Biology, School of Dentistry, Kyung Hee University, Seoul 130-701, Republic of Korea Tomokazu Matsue, Graduate School of Environmental Studies, Tohoku University, Sendai 980-8579, Japan.Search for more papers by this authorTomokazu Matsue, Corresponding Author Tomokazu Matsue [email protected] Graduate School of Environmental Studies, Tohoku University, Sendai 980-8579, Japan WPI-Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, Japan Ali Khademhosseini, Department of Medicine, Center for Biomedical Engineering, Brigham and Women's Hospital, Harvard Medical School, Cambridge, Massachusetts 02139, USA, Harvard–MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA, Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, Massachusetts 02115, USA and Department of Maxillofacial Biomedical Engineering and Institute of Oral Biology, School of Dentistry, Kyung Hee University, Seoul 130-701, Republic of Korea Tomokazu Matsue, Graduate School of Environmental Studies, Tohoku University, Sendai 980-8579, Japan.Search for more papers by this author First published: 25 June 2013 https://doi.org/10.1002/adma.201301300Citations: 234Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation 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Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Graphical Abstract Dielectrophoresis is used to align carbon nanotubes (CNTs) within gelatin methacrylate (GelMA) hydrogels in a facile and rapid manner. Aligned GelMA-CNT hydrogels show higher electrical properties compared with pristine and randomly distributed CNTs in GelMA hydrogels. The muscle cells cultured on these materials demonstrate higher maturation compared with cells cultured on pristine and randomly distributed CNTs in GelMA hydrogels. Supporting Information As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer reviewed and may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors. 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Nanotechnol. 2011, 6, 720. 10.1038/nnano.2011.160 CASPubMedWeb of Science®Google Scholar 4 L. Xu, Z. Jiang, Q. Qing, L. Mai, Q. Zhang, C. M. Lieber, Nano Lett. 2012, 13, 746. 10.1021/nl304435z CASWeb of Science®Google Scholar 5 B. Tian, J. Liu, T. Dvir, L. Jin, J. H. Tsui, Q. Qing, Z. Suo, R. Langer, D. S. Kohane, C. M. Lieber, Nat. Mater. 2012, 11, 986. 10.1038/nmat3404 CASPubMedWeb of Science®Google Scholar 6 P. Schwille, Science. 2011, 333, 1252. 10.1126/science.1211701 CASPubMedWeb of Science®Google Scholar 7 K. T. Sapra, H. Bayley, Sci. Rep. 2012, 2, 848. 10.1038/srep00848 CASPubMedWeb of Science®Google Scholar 8 S. R. Shin, S. M. Jung, M. Zalabany, K. Kim, P. Zorlutuna, S. Kim, M. Nikkhah, M. Khabiry, M. Azize, J. Kong, K. Wan, T. Palacios, M. R. Dokmeci, H. Bae, X. Tang, A. Khademhosseini, ACS Nano 2013, 7, 2369. 10.1021/nn305559j CASPubMedWeb of Science®Google Scholar 9 T. Dvir, B. P. Timko, D. S. Kohane, R. Langer, Nat. Nanotechnol. 2011, 6, 13. 10.1038/nnano.2010.246 CASPubMedWeb of Science®Google Scholar 10 J.-O. You, M. Rafat, G. J. C. Ye, D. T. Auguste, Nano Lett. 2011, 11, 3643. 10.1021/nl201514a CASPubMedWeb of Science®Google Scholar 11 T. Cohen-Karni, R. Langer, D. S. Kohane, ACS Nano 2012, 6, 6541. 10.1021/nn302915s CASPubMedWeb of Science®Google Scholar 12 F. J. Rawson, C. L. Yeung, S. K. Jackson, P. M. Mendes, Nano Lett. 2012, 13, 1. 10.1021/nl203780d CASPubMedWeb of Science®Google Scholar 13 A. K. Shalek, J. T. Gaublomme, L. Wang, N. Yosef, N. Chevrier, M. S. Andersen, J. T. Robinson, N. Pochet, D. Neuberg, R. S. Gertner, I. Amit, J. R. Brown, N. Hacohen, A. Regev, C. J. Wu, H. Park, Nano Lett. 2012, 12, 6498. 10.1021/nl3042917 CASPubMedWeb of Science®Google Scholar 14 J. W. Nichol, S. T. Koshy, H. Bae, C. M. Hwang, S. Yamanlar, A. Khademhosseini, Biomaterials 2010, 31, 5536. 10.1016/j.biomaterials.2010.03.064 CASPubMedWeb of Science®Google Scholar 15 S. R. Shin, H. Bae, J. M. Cha, J. Y. Mun, Y.-C. Chen, H. Tekin, H. Shin, S. Farshchi, M. R. Dokmeci, S. Tang, A. Khademhosseini, ACS Nano 2012, 6, 362. 10.1021/nn203711s CASPubMedWeb of Science®Google Scholar 16 J. Ramón-Azcón, T. Yasukawa, H. J. Lee, T. Matsue, F. Sánchez-Baeza, M.-P. Marco, F. Mizutani, Biosens. Bioelectron. 2010, 25, 1928. 10.1016/j.bios.2010.01.006 CASPubMedWeb of Science®Google Scholar 17 J. Ramón-Azcón, R. Kunikata, F.-J. Sanchez, M.-P. Marco, H. Shiku, T. Yasukawa, T. Matsue, Biosens. Bioelectron. 2009, 24, 1592. 10.1016/j.bios.2008.08.035 CASPubMedWeb of Science®Google Scholar 18 J. H. Sung, H. S. Kim, H.-J. Jin, H. J. Choi, I.-J. Chin, Macromolecules 2004, 37, 9899. 10.1021/ma048355g CASWeb of Science®Google Scholar 19 J. Ayutsede, M. Gandhi, S. Sukigara, H. Ye, C. Hsu, Y. Gogotsi, F. Ko, Biomacromolecules 2005, 7, 208. 10.1021/bm0505888 CASWeb of Science®Google Scholar 20 R. Sen, B. Zhao, D. Perea, M. E. Itkis, H. Hu, J. Love, E. Bekyarova, R. C. Haddon, Nano Lett. 2004, 4, 459. 10.1021/nl035135s CASWeb of Science®Google Scholar 21 Y. Dror, W. Salalha, R. L. Khalfin, Y. Cohen, A. L. Yarin, E. Zussman, Langmuir 2003, 19, 7012. 10.1021/la034234i CASWeb of Science®Google Scholar 22 F. Ko, Y. Gogotsi, A. Ali, N. Naguib, H. Ye, G. L. Yang, C. Li, P. Willis, Adv. Mater. 2003, 15, 1161. 10.1002/adma.200304955 CASWeb of Science®Google Scholar 23 C. M. Voge, M. Kariolis, R. A. MacDonald, J. P. Stegemann, J. Biomed. Mater. Res. Part A. 2008, 86A, 269. 10.1002/jbm.a.32029 CASWeb of Science®Google Scholar 24 S. Namgung, K. Y. Baik, J. Park, S. Hong, ACS Nano 2011, 5, 7383. 10.1021/nn2023057 CASPubMedWeb of Science®Google Scholar 25 B. V. Derjaguin, V. M. Muller, Y. Toporov, J. Coll. Interf. Sci. 1975, 53, 314. 10.1016/0021-9797(75)90018-1 CASWeb of Science®Google Scholar 26 G. C. Reilly, A. J. Engler, J. Biomech. 2010, 43, 55. 10.1016/j.jbiomech.2009.09.009 PubMedWeb of Science®Google Scholar 27 M. P. Lutolf, P. M. Gilbert, H. M. Blau, Nature 2009, 462, 433. 10.1038/nature08602 CASPubMedWeb of Science®Google Scholar 28 H. Aubin, J. W. Nichol, C. B. Hutson, H. Bae, A. L. Sieminski, D. M. Cropek, P. Akhyari, A. Khademhosseini, Biomaterials 2010, 31, 6941. 10.1016/j.biomaterials.2010.05.056 CASPubMedWeb of Science®Google Scholar 29 J. Suhr, N. Koratkar, P. Keblinski, P. Ajayan, Nat. Mater. 2005, 4, 134. 10.1038/nmat1293 CASPubMedWeb of Science®Google Scholar 30 a) V. Hosseini, S. Ahadian, S. Ostrovidov, G. Camci-Unal, S. Chen, H. Kaji, M. Ramalingam, A. Khademhosseini, Tissue Eng. Pt. A. 2012, 18, 2453; 10.1089/ten.tea.2012.0181 CASPubMedWeb of Science®Google Scholarb) S. Ahadian, J. Ramon-Azcon, S. Ostrovidov, G. Camci-Unal, H. Kaji, K. Ino, H. Shiku, A. Khademhosseini, T. Matsue, Lab Chip 2012, 12, 3491; 10.1039/c2lc40479f CASPubMedWeb of Science®Google Scholarc) S. Ahadian, S. Ostrovidov, V. Hosseini, H. Kaji, M. Ramalingam, H. Bae, A. Khademhosseini, Organogenesis 2013, 9, April/May/June 2013. 10.4161/org.25121 Web of Science®Google Scholar 31 J. Ramon-Azcon, S. Ahadian, R. Obregon, G. Camci-Unal, S. Ostrovidov, V. Hosseini, H. Kaji, K. Ino, H. Shiku, A. Khademhosseini, T. Matsue, Lab Chip 2012, 12, 2959. 10.1039/c2lc40213k CASPubMedWeb of Science®Google Scholar 32 S. Ahadian, J. Ramon-Azcon, S. Ostrovidov, G. Camci-Unal, V. Hosseini, H. Kaji, K. Ino, H. Shiku, A. Khademhosseini, T. Matsue, Lab Chip 2012, 12, 3491. 10.1039/c2lc40479f CASPubMedWeb of Science®Google Scholar 33 S. Arber, G. Halder, P. Caroni, Cell 1994, 79, 221. 10.1016/0092-8674(94)90192-9 CASPubMedWeb of Science®Google Scholar 34 S. Sirivisoot, B. Harrison, Int. J. Nanomed. 2011, 6, 2483. 10.2147/IJN.S24073 CASPubMedWeb of Science®Google Scholar Citing Literature Volume25, Issue29August 7, 2013Pages 4028-4034 ReferencesRelatedInformation