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Multifunctional Cell-Culture Platform for Aligned Cell Sheet Monitoring, Transfer Printing, and Therapy

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Center for Nanoparticle Research, Institute for Basic Science (IBS), Seoul 151-742, Republic of Korea
School of Chemical and Biological Engineering, Institute of Chemical Processes, Seoul National University, Seoul 151-742, Republic of Korea
§ Department of Radiology, Seoul National University College of Medicine, Seoul 110-744, Republic of Korea
Center for Mechanics of Solids, Structures, and Materials, Department of Aerospace Engineering and Engineering Mechanics, Texas Materials Institute, University of Texas at Austin, 210 E. 24th Street, Austin, Texas 78712, United States
School of Mechanical and Aerospace Engineering, Seoul National University, Seoul 151-742, Republic of Korea
*Address correspondence to D.-H. Kim ([email protected]), N. Lu ([email protected]), S. H. Choi ([email protected]).
Cite this: ACS Nano 2015, 9, 3, 2677–2688
Publication Date (Web):February 16, 2015
https://doi.org/10.1021/nn5064634
Copyright © 2015 American Chemical Society
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Abstract

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While several functional platforms for cell culturing have been proposed for cell sheet engineering, a soft integrated system enabling in vitro physiological monitoring of aligned cells prior to their in vivo applications in tissue regeneration has not been reported. Here, we present a multifunctional, soft cell-culture platform equipped with ultrathin stretchable nanomembrane sensors and graphene-nanoribbon cell aligners, whose system modulus is matched with target tissues. This multifunctional platform is capable of aligning plated cells and in situ monitoring of cellular physiological characteristics during proliferation and differentiation. In addition, it is successfully applied as an in vitro muscle-on-a-chip testing platform. Finally, a simple but high-yield transfer printing mechanism is proposed to deliver cell sheets for scaffold-free, localized cell therapy in vivo. The muscle-mimicking stiffness of the platform allows the high-yield transfer printing of multiple cell sheets and results in successful therapies in diseased animal models. Expansion of current results to stem cells will provide unique opportunities for emerging classes of tissue engineering and cell therapy technologies.

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  6. Chong Cheng, Shuang Li, Arne Thomas, Nicholas A. Kotov, and Rainer Haag . Functional Graphene Nanomaterials Based Architectures: Biointeractions, Fabrications, and Emerging Biological Applications. Chemical Reviews 2017, 117 (3) , 1826-1914. https://doi.org/10.1021/acs.chemrev.6b00520
  7. Ling Wang, Yaobin Wu, Baolin Guo, and Peter X. Ma . Nanofiber Yarn/Hydrogel Core–Shell Scaffolds Mimicking Native Skeletal Muscle Tissue for Guiding 3D Myoblast Alignment, Elongation, and Differentiation. ACS Nano 2015, 9 (9) , 9167-9179. https://doi.org/10.1021/acsnano.5b03644
  8. Hui Zhao, Yiqian Yang, Yu Chen, Jie Li, Lei Wang, Chunshan Li. A review of multiple Pickering emulsions: Solid stabilization, preparation, particle effect, and application. Chemical Engineering Science 2022, 248 , 117085. https://doi.org/10.1016/j.ces.2021.117085
  9. Min Chan Shin, Moon Sung Kang, Rowoon Park, Seon Yeong Chae, Dong-Wook Han, Suck Won Hong. Differential cellular interactions and responses to ultrathin micropatterned graphene oxide arrays with or without ordered in turn RGD peptide films. Applied Surface Science 2021, 561 , 150115. https://doi.org/10.1016/j.apsusc.2021.150115
  10. Pingqiang Cai, Changxian Wang, Huajian Gao, Xiaodong Chen. Mechanomaterials: A Rational Deployment of Forces and Geometries in Programming Functional Materials. Advanced Materials 2021, 92 , 2007977. https://doi.org/10.1002/adma.202007977
  11. Sung-Hyuk Sunwoo, Kyoung-Ho Ha, Sangkyu Lee, Nanshu Lu, Dae-Hyeong Kim. Wearable and Implantable Soft Bioelectronics: Device Designs and Material Strategies. Annual Review of Chemical and Biomolecular Engineering 2021, 12 (1) , 359-391. https://doi.org/10.1146/annurev-chembioeng-101420-024336
  12. Xiaoyu Sui, Julia R. Downing, Mark C. Hersam, Junhong Chen. Additive manufacturing and applications of nanomaterial-based sensors. Materials Today 2021, 9 https://doi.org/10.1016/j.mattod.2021.02.001
  13. Chih-Hui Yang, Shu-Ling Huang, Yi-Ting Wang, Chun-Ho Chang, Ya-Chi Tsai, Yu-Mei Lin, Yuan-Yi Lu, Yung-Sheng Lin, Keng-Shiang Huang. Applications of Advanced Nanotechnology in Stem Cell Research. Science of Advanced Materials 2021, 13 (2) , 188-198. https://doi.org/10.1166/sam.2021.3944
  14. Prashant Rawat, Deju Zhu. Fabrication and Application Prospective of Graphene Infused Polymeric Flexible, Stretchable and Transparent Devices. 2021,,, 35-63. https://doi.org/10.1007/978-3-030-75456-3_2
  15. Amy Corbin Farr, Katie J. Hogan, Antonios G. Mikos. Nanomaterial Additives for Fabrication of Stimuli‐Responsive Skeletal Muscle Tissue Engineering Constructs. Advanced Healthcare Materials 2020, 9 (23) , 2000730. https://doi.org/10.1002/adhm.202000730
  16. Sung-Hyuk Sunwoo, Sang Ihn Han, Hyunwoo Joo, Gi Doo Cha, Dokyoon Kim, Seung Hong Choi, Taeghwan Hyeon, Dae-Hyeong Kim. Advances in Soft Bioelectronics for Brain Research and Clinical Neuroengineering. Matter 2020, 3 (6) , 1923-1947. https://doi.org/10.1016/j.matt.2020.10.020
  17. Kyoung Won Cho, Wang Hee Lee, Byung-Soo Kim, Dae-Hyeong Kim. Sensors in heart-on-a-chip: A review on recent progress. Talanta 2020, 219 , 121269. https://doi.org/10.1016/j.talanta.2020.121269
  18. Ja Hoon Koo, Jun‐Kyul Song, Seungwon Yoo, Sung‐Hyuk Sunwoo, Donghee Son, Dae‐Hyeong Kim. Unconventional Device and Material Approaches for Monolithic Biointegration of Implantable Sensors and Wearable Electronics. Advanced Materials Technologies 2020, 5 (10) , 2000407. https://doi.org/10.1002/admt.202000407
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  28. Hironobu Takahashi, Tatsuya Shimizu, Teruo Okano. Intelligent Surfaces for Cell Sheet Engineering. 2019,,, 469-484. https://doi.org/10.1016/B978-0-12-809880-6.00028-X
  29. Hironobu Takahashi, Teruo Okano. Thermally-triggered fabrication of cell sheets for tissue engineering and regenerative medicine. Advanced Drug Delivery Reviews 2019, 138 , 276-292. https://doi.org/10.1016/j.addr.2019.01.004
  30. Changhong Linghu, Shun Zhang, Chengjun Wang, Jizhou Song. Transfer printing techniques for flexible and stretchable inorganic electronics. npj Flexible Electronics 2018, 2 (1) https://doi.org/10.1038/s41528-018-0037-x
  31. Qinming Yu, Furong Chen, Honglei Zhou, Xudong Yu, Huanyu Cheng, Huaping Wu. Design and Analysis of Magnetic-Assisted Transfer Printing. Journal of Applied Mechanics 2018, 85 (10) https://doi.org/10.1115/1.4040599
  32. Youngsik Lee, Jaemin Kim, Ja Hoon Koo, Tae-Ho Kim, Dae-Hyeong Kim. Nanomaterials for bioelectronics and integrated medical systems. Korean Journal of Chemical Engineering 2018, 35 (1) , 1-11. https://doi.org/10.1007/s11814-017-0236-5
  33. Brittany L. Rodriguez, Lisa M. Larkin. Functional three-dimensional scaffolds for skeletal muscle tissue engineering. 2018,,, 279-304. https://doi.org/10.1016/B978-0-08-100979-6.00012-4
  34. Zhikai Tan, Tong Liu, Juchang Zhong, Yikun Yang, Weihong Tan. Control of cell growth on 3D-printed cell culture platforms for tissue engineering. Journal of Biomedical Materials Research Part A 2017, 105 (12) , 3281-3292. https://doi.org/10.1002/jbm.a.36188
  35. Ishan D. Joshipura, Mickey Finn, Siew Ting Melissa Tan, Michael D. Dickey, Darren J. Lipomi. Stretchable bioelectronics—Current and future. MRS Bulletin 2017, 42 (12) , 960-967. https://doi.org/10.1557/mrs.2017.270
  36. Yong Shin, Su-Jin Song, Suck Hong, Seung Jeong, Wojciech Chrzanowski, Jae-Chang Lee, Dong-Wook Han. Multifaceted Biomedical Applications of Functional Graphene Nanomaterials to Coated Substrates, Patterned Arrays and Hybrid Scaffolds. Nanomaterials 2017, 7 (11) , 369. https://doi.org/10.3390/nano7110369
  37. Youngsik Lee, Jaemin Kim, Hyunwoo Joo, Milan S. Raj, Roozbeh Ghaffari, Dae-Hyeong Kim. Wearable Sensing Systems with Mechanically Soft Assemblies of Nanoscale Materials. Advanced Materials Technologies 2017, 2 (9) , 1700053. https://doi.org/10.1002/admt.201700053
  38. Pingqiang Cai, Wan Ru Leow, Xiaoyuan Wang, Yun-Long Wu, Xiaodong Chen. Programmable Nano-Bio Interfaces for Functional Biointegrated Devices. Advanced Materials 2017, 29 (26) , 1605529. https://doi.org/10.1002/adma.201605529
  39. Deji Akinwande, Christopher J. Brennan, J. Scott Bunch, Philip Egberts, Jonathan R. Felts, Huajian Gao, Rui Huang, Joon-Seok Kim, Teng Li, Yao Li, Kenneth M. Liechti, Nanshu Lu, Harold S. Park, Evan J. Reed, Peng Wang, Boris I. Yakobson, Teng Zhang, Yong-Wei Zhang, Yao Zhou, Yong Zhu. A review on mechanics and mechanical properties of 2D materials—Graphene and beyond. Extreme Mechanics Letters 2017, 13 , 42-77. https://doi.org/10.1016/j.eml.2017.01.008
  40. Yanlong Tai, Tushar Kanti Bera, Zhenguo Yang, Gilles Lubineau. Leveraging a temperature-tunable, scale-like microstructure to produce multimodal, supersensitive sensors. Nanoscale 2017, 9 (23) , 7888-7894. https://doi.org/10.1039/C7NR01662J
  41. Jaemin Kim, Jongsu Lee, Donghee Son, Moon Kee Choi, Dae-Hyeong Kim. Deformable devices with integrated functional nanomaterials for wearable electronics. Nano Convergence 2016, 3 (1) https://doi.org/10.1186/s40580-016-0062-1
  42. Changsoon Choi, Moon Kee Choi, Taeghwan Hyeon, Dae-Hyeong Kim. Nanomaterial-Based Soft Electronics for Healthcare Applications. ChemNanoMat 2016, 2 (11) , 1006-1017. https://doi.org/10.1002/cnma.201600191
  43. Puay Yong Neo, Thomas Kok Hiong Teh, Alex Sheng Ru Tay, Maria Christine Tankeh Asuncion, Si Ning Png, Siew Lok Toh, James Cho-Hong Goh. Stem cell-derived cell-sheets for connective tissue engineering. Connective Tissue Research 2016, 57 (6) , 428-442. https://doi.org/10.3109/03008207.2016.1173035
  44. Xiaozhao Wang, Kui Cheng, Wenjian Weng, Huiming Wang, Jun Lin. Light‐Induced Cell‐Sheet Harvest on TiO 2 Films Sensitized with Carbon Quantum Dots. ChemPlusChem 2016, 81 (11) , 1166-1173. https://doi.org/10.1002/cplu.201600202
  45. , Hyunjae Lee, Dae-Hyeong Kim. Soft bioelectronics using nanomaterials. 2016,,, 994502. https://doi.org/10.1117/12.2235267
  46. Suji Choi, Hyunjae Lee, Roozbeh Ghaffari, Taeghwan Hyeon, Dae-Hyeong Kim. Recent Advances in Flexible and Stretchable Bio-Electronic Devices Integrated with Nanomaterials. Advanced Materials 2016, 28 (22) , 4203-4218. https://doi.org/10.1002/adma.201504150
  47. Jangsoo Lim, Indong Jun, Yu Bin Lee, Eun Mi Kim, Dongsuk Shin, Hojeong Jeon, Hansoo Park, Heungsoo Shin. Fabrication of cell sheets with anisotropically aligned myotubes using thermally expandable micropatterned hydrogels. Macromolecular Research 2016, 24 (6) , 562-572. https://doi.org/10.1007/s13233-016-4070-0
  48. Seok Joo Kim, Kyoung Won Cho, Hye Rim Cho, Liu Wang, Sung Young Park, Seung Eun Lee, Taeghwan Hyeon, Nanshu Lu, Seung Hong Choi, Dae-Hyeong Kim. Stretchable and Transparent Biointerface Using Cell-Sheet-Graphene Hybrid for Electrophysiology and Therapy of Skeletal Muscle. Advanced Functional Materials 2016, 26 (19) , 3207-3217. https://doi.org/10.1002/adfm.201504578
  49. Donghee Son, Ja Hoon Koo, Jongsu Lee, Dae-Hyeong Kim. High-Performance Wearable Bioelectronics Integrated with Functional Nanomaterials. 2016,,, 151-171. https://doi.org/10.1007/978-3-319-28694-5_8
  50. Moon Kee Choi, Inhyuk Park, Dong Chan Kim, Eehyung Joh, Ok Kyu Park, Jaemin Kim, Myungbin Kim, Changsoon Choi, Jiwoong Yang, Kyoung Won Cho, Jae-Ho Hwang, Jwa-Min Nam, Taeghwan Hyeon, Ji Hoon Kim, Dae-Hyeong Kim. Thermally Controlled, Patterned Graphene Transfer Printing for Transparent and Wearable Electronic/Optoelectronic System. Advanced Functional Materials 2015, 25 (46) , 7109-7118. https://doi.org/10.1002/adfm.201502956
  51. Jong Ho Lee, Yong Cheol Shin, Sang-Min Lee, Oh Seong Jin, Seok Hee Kang, Suck Won Hong, Chang-Mo Jeong, Jung Bo Huh, Dong-Wook Han. Enhanced Osteogenesis by Reduced Graphene Oxide/Hydroxyapatite Nanocomposites. Scientific Reports 2015, 5 (1) https://doi.org/10.1038/srep18833
  52. Runrun Wu, Jianming Pan, Xiaohui Dai, Dong Qiu, Hengjia Zhu, Yue Ma, Weidong Shi, Yongsheng Yan. A hierarchical rippled and crumpled PLA microstructure generated through double emulsion: the interesting roles of Pickering nanoparticles. Chemical Communications 2015, 51 (90) , 16251-16254. https://doi.org/10.1039/C5CC06516J

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