Multifunctional cell-culture platform for aligned cell sheet monitoring, transfer printing, and therapy

ACS Nano

Volumn 9, Issue 3, 2015, Pages 2677-2688

  Kim, Seok Joo ^a,b   Cho, Hye Rim ^a,c   Cho, Kyoung Won ^a,b   Qiao, Shutao ^d   Rhim, Jung Soo ^b   Soh, Min ^a,b   Kim, Taeho ^a,b   Choi, Moon Kee ^a,b   Choi, Changsoon ^a,b   Park, Inhyuk ^a,b   Hwang, Nathaniel S ^b   Hyeon, Taeghwan ^a,b   Choi, Seung Hong ^a,c   Lu, Nanshu ^d   Kim, Dae Hyeong ^a,b  

^a Korea Basic Science Institute (KBSI)   (South Korea)

^b Seoul National University   (South Korea)

^c Seoul National University College of Medicine   (South Korea)

^d The University of Texas at Austin   (United States)

Author keywords

cell alignment; ceria nanoparticle; flexible nanomembrane electronics; graphene nanoribbon; real time monitoring; regenerative medicine; transfer printing

Indexed keywords

CELL CULTURE; CERIUM OXIDE; FLEXIBLE ELECTRONICS; GRAPHENE; GRAPHENE NANORIBBON; MUSCLE; NANORIBBONS; PATIENT MONITORING; REGENERATIVE MEDICINE; SCAFFOLDS (BIOLOGY); STEM CELLS;

CELL ALIGNMENT; CERIA NANOPARTICLES; NANOMEMBRANES; REAL TIME MONITORING; TRANSFER PRINTING;

CELL ENGINEERING;

CARBON NANOTUBE; GRAPHITE;

ANIMAL; BIOLOGICAL THERAPY; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CHEMISTRY; CULTURE TECHNIQUE; CYTOLOGY; FEMALE; MOUSE; PRINTING; PROCEDURES; SKELETAL MUSCLE; TISSUE ENGINEERING;

ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CELL- AND TISSUE-BASED THERAPY; FEMALE; GRAPHITE; MICE; MUSCLE, SKELETAL; NANOTUBES, CARBON; PRINTING; TISSUE ENGINEERING;

EID: 84925652628     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn5064634     Document Type: Article

References (52)

1. Levenberg, S.; Huang, N. F.; Lavik, E.; Rogers, A. B.; Itskovitz-Eldor, J.; Langer, R. Differentiation of Human Embryonic Stem Cells on Three-Dimensional Polymer Scaffolds Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 12741-12746
2. Dvir, T.; Timko, B. P.; Kohane, D. S.; Langer, R. Nanotechnological Strategies for Engineering Complex Tissues Nat. Nanotechnol. 2011, 6, 13-22
3. Sun, J. Y.; Zhao, X.; Illeperuma, W. R.; Chaudhuri, O.; Oh, K. H.; Mooney, D. J.; Vlassak, J. J.; Suo, Z. Highly Stretchable and Tough Hydrogels Nature 2012, 489, 133-136
4. Tian, B.; Liu, J.; Dvir, T.; Jin, L.; Tsui, J. H.; Qing, Q.; Suo, Z.; Langer, R.; Kohane, D. S.; Lieber, C. M. Macroporous Nanowire Nanoelectronic Scaffolds for Synthetic Tissues Nat. Mater. 2012, 11, 986-994
5. Straub, B.; Meyer, E.; Fromherz, P. Recombinant Maxi-K Channels on Transistor, A Prototype of Iono-Electronic Interfacing Nat. Biotechnol. 2001, 19, 121-124
6. Sekitani, T.; Zschieschang, U.; Klauk, H.; Someya, T. Flexible Organic Transistors and Circuits with Extreme Bending Stability Nat. Mater. 2010, 9, 1015-1022
7. Viventi, J.; Kim, D. H.; Vigeland, L.; Frechette, E. S.; Blanco, J. A.; Kim, Y. S.; Avrin, A. E.; Tiruvadi, V. R.; Hwang, S. W.; Vanleer, A. C. et al. Flexible, Foldable, Actively Multiplexed, High-Density Electrode Array for Mapping Brain Activity in Vivo Nat. Neurosci. 2011, 14, 1599-1605
8. Sekitani, T.; Noguchi, Y.; Hata, K.; Fukushima, T.; Aida, T.; Someya, T. A Rubberlike Stretchable Active Matrix Using Elastic Conductors Science 2008, 321, 1468-1472
9. Kim, D. H.; Lu, N.; Ma, R.; Kim, Y. S.; Kim, R. H.; Wang, S.; Wu, J.; Won, S. M.; Tao, H.; Islam, A. et al. Epidermal Electronics Science 2011, 333, 838-843
10. Keplinger, C.; Sun, J. Y.; Foo, C. C.; Rothemund, P.; Whitesides, G. M.; Suo, Z. Stretchable, Transparent, Ionic Conductors Science 2013, 341, 984-987
11. Son, D.; Lee, J.; Qiao, S.; Ghaffari, R.; Kim, J.; Lee, J. E.; Song, C.; Kim, S. J.; Lee, D. J.; Jun, S. W. et al. Multifunctional Wearable Devices for Diagnosis and Therapy of Movement Disorders Nat. Nanotechnol. 2014, 9, 397-404
12. Park, Y. J.; Lee, S. K.; Kim, M. S.; Kim, H.; Ahn, J. H. Graphene-Based Conformal Devices ACS Nano 2014, 8, 7655-7662
13. Nishida, K.; Yamato, M.; Hayashida, Y.; Watanabe, K.; Yamamoto, K.; Adachi, E.; Nagai, S.; Kikuchi, A.; Maeda, N.; Watanabe, H. et al. Corneal Reconstruction with Tissue-Engineered Cell Sheets Composed of Autologous Oral Mucosal Epithelium N. Engl. J. Med. 2004, 351, 1187-1196
14. Iwata, T.; Yamato, M.; Tsuchioka, H.; Takagi, R.; Mukobata, S.; Washio, K.; Okano, T.; Ishikawa, I. Periodontal Regeneration with Multi-Layered Periodontal Ligament-Derived Cell Sheets in a Canine Model Biomaterials 2009, 30, 2716-2723
15. Miyahara, Y.; Nagaya, N.; Kataoka, M.; Yanagawa, B.; Tanaka, K.; Hao, H.; Ishino, K.; Ishida, H.; Shimizu, T.; Kangawa, K. et al. Monolayered Mesenchymal Stem Cells Repair Scarred Myocardium after Myocardial Infarction Nat. Med. 2006, 12, 459-465
16. Akiyama, Y.; Kikuchi, A.; Yamato, M.; Okano, T. Ultrathin Poly(N-isopropylacrylamide) Grafted Layer on Polystyrene Surfaces for Cell Adhesion/Detachment Control Langmuir 2004, 20, 5506-5511
17. Engler, A. J.; Sen, S.; Sweeney, H. L.; Discher, D. E. Matrix Elasticity Directs Stem Cell Lineage Specification Cell 2006, 126, 677-689
18. Kim, D. H.; Song, J.; Choi, W. M.; Kim, H. S.; Kim, R. H.; Liu, Z.; Huang, Y. Y.; Hwang, K. C.; Zhang, Y.; Rogers, J. A. Materials and Noncoplanar Mesh Designs for Integrated Circuits with Linear Elastic Responses to Extreme Mechanical Deformations Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 18675-18680
19. Bowden, N.; Brittain, S.; Evans, A. G.; Hutchinson, J. W.; Whitesides, G. M. Spontaneous Formation of Odered Structures in Thin Films of Metals Supported on an Elastomeric Polymer Nature 1998, 393, 146-149
20. Khang, D. Y.; Jiang, H.; Huang, Y.; Rogers, J. A. A Stretchable Form of Single-Crystal Silicon for High-Performance Electronics on Rubber Substrates Science 2006, 311, 208-212
21. Jiang, H.; Khang, D. Y.; Song, J.; Sun, Y.; Huang, Y.; Rogers, J. A. Finite Deformation Mechanics in Buckled Thin Films on Compliant Supports Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 15607-15612
22. Park, S. Y.; Park, J.; Sim, S. H.; Sung, M. G.; Kim, K. S.; Hong, B. H.; Hong, S. Enhanced Differentiation of Human Neural Stem Cells into Neurons on Graphene Adv. Mater. 2011, 23, H263-H267
23. Hong, S. W.; Lee, J. H.; Kang, S. H.; Hwang, E. Y.; Hwang, Y. S.; Lee, M. H.; Han, D. W.; Park, J. C. Enhanced Neural Cell Adhesion and Neurite Outgrowth on Graphene-Based Biomimetic Substrates BioMed. Res. Int. 2014, 2014, 212149
24. Bajaj, P.; Rivera, J. A.; Marchwiany, D.; Solovyeva, V.; Bashir, R. Graphene-Based Patterning and Differentiation of C2C12 Myoblasts Adv. Healthcare Mater. 2014, 3, 995-1000
25. Park, J.; Park, S.; Ryu, S.; Bhang, S. H.; Kim, J.; Yoon, J. K.; Park, Y. H.; Cho, S. P.; Lee, S.; Hong, B. H. et al. Graphene-Regulated Cardiomyogenic Differentiation Process of Mesenchymal Stem Cells by Enhancing the Expression of Extracellular Matrix Proteins and Cell Signaling Molecules Adv. Healthcare Mater. 2014, 3, 176-181
26. Kim, K. S.; Zhao, Y.; Jang, H.; Lee, S. Y.; Kim, J. M.; Kim, K. S.; Ahn, J. H.; Kim, P.; Choi, J. Y.; Hong, B. H. Large-Scale Pattern Growth of Graphene Films for Stretchable Transparent Electrodes Nature 2009, 457, 706-710
27. Huh, D.; Matthews, B. D.; Mammoto, A.; Montoya-Zavala, M.; Hsin, H. Y.; Ingber, D. E. Reconstituting Organ-Level Lung Functions on a Chip Science 2010, 328, 1662-1668
28. Huh, D.; Hamilton, G. A.; Ingber, D. E. From 3D Cell Culture to Organs-on-Chips Trends Cell Biol. 2011, 21, 745-754
29. Huh, D.; Leslie, D. C.; Matthews, B. D.; Fraser, J. P.; Jurek, S.; Hamilton, G. A.; Thorneloe, K. S.; McAlexander, M. A.; Ingber, D. E. A Human Disease Model of Drug Toxicity-Induced Pulmonary Edema in a Lung-on-A-Chip Microdevice Sci. Transl. Med. 2012, 4, 159ra147
30. Guo, J. J.; Yao, X. J.; Ning, L. L.; Wang, Q. Q.; Liu, H. X. The Adsorption Mechanism and Induced Conformational Changes of Three Typical Proteins with Different Secondary Structural Features on Graphene RSC Adv. 2014, 4, 9953-9962
31. Sawyer, A. A.; Hennessy, K. M.; Bellis, S. L. Regulation of Mesenchymal Stem Cell Attachment and Spreading on Hydroxyapatite by RGD Peptides and Adsorbed Serum Proteins Biomaterials 2005, 26, 1467-1475
32. Boontheekul, T.; Hill, E. E.; Kong, H. J.; Mooney, D. J. Regulating Myoblast Phenotype through Controlled Gel Stiffness and Degradation Tissue Eng. 2007, 13, 1431-1442
33. Bagnaninchi, P. O.; Drummond, N. Real-Time Label-Free Monitoring of Adipose-Derived Stem Cell Differentiation with Electric Cell-Substrate Impedance Sensing Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 6462-6467
34. Kim, D. H.; Ghaffari, R.; Lu, N.; Wang, S.; Lee, S. P.; Keum, H.; DAngelo, R.; Klinker, L.; Su, Y.; Lu, C. et al. Electronic Sensor and Actuator Webs for Large-Area Complex Geometry Cardiac Mapping and Therapy Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 19910-19915
35. Wegener, J.; Keese, C. R.; Giaever, I. Electric Cell-Substrate Impedance Sensing (ECIS) as a Noninvasive Means to Monitor the Kinetics of Cell Spreading to Artificial Surfaces Exp. Cell Res. 2000, 259, 158-166
36. Rakhilin, S.; Turner, G.; Katz, M.; Warden, R.; Irelan, J.; Abassi, Y. A.; Glass, D. J. Electrical Impedance as a Novel Biomarker of Myotube Atrophy and Hypertrophy J. Biomol. Screen. 2011, 16, 565-574
37. Eltzschig, H. K.; Eckle, T. Ischemia and Reperfusion - from Mechanism to Translation Nat. Med. 2011, 17, 1391-1401
38. Karakoti, A.; Singh, S.; Dowding, J. M.; Seal, S.; Self, W. T. Redox-Active Radical Scavenging Nanomaterials Chem. Soc. Rev. 2010, 39, 4422-4432
39. Kim, C. K.; Kim, T.; Choi, I. Y.; Soh, M.; Kim, D.; Kim, Y. J.; Jang, H.; Yang, H. S.; Kim, J. Y.; Park, H. K. et al. Ceria Nanoparticles That Can Protect against Ischemic Stroke Angew. Chem., Int. Ed. 2012, 51, 11039-11043
40. Carlson, A.; Bowen, A. M.; Huang, Y.; Nuzzo, R. G.; Rogers, J. A. Transfer Printing Techniques for Materials Assembly and Micro/Nanodevice Fabrication Adv. Mater. 2012, 24, 5284-5318
41. Feng, X.; Meitl, M. A.; Bowen, A. M.; Huang, Y.; Nuzzo, R. G.; Rogers, J. A. Competing Fracture in Kinetically Controlled Transfer Printing Langmuir 2007, 23, 12555-12560
42. Nayak, T. R.; Andersen, H.; Makam, V. S.; Khaw, C.; Bae, S.; Xu, X.; Ee, P. L.; Ahn, J. H.; Hong, B. H.; Pastorin, G. et al. Graphene for Controlled and Accelerated Osteogenic Differentiation of Human Mesenchymal Stem Cells ACS Nano 2011, 5, 4670-4678
43. Wang, L.; Sun, B.; Ziemer, K. S.; Barabino, G. A.; Carrier, R. L. Chemical and Physical Modifications to Poly(dimethylsiloxane) Surfaces Affect Adhesion of Caco-2 Cells J. Biomed. Mater. Res., Part A 2010, 93A, 1260-1271
44. Webb, R. C. Smooth Muscle Contraction and Relaxation Adv. Physiol. Ed. 2003, 27, 201-206
45. Kim, S. J.; Jun, I.; Kim, D. W.; Lee, Y. B.; Lee, Y. J.; Lee, J. H.; Park, K. D.; Park, H.; Shin, H. Rapid Transfer of Endothelial Cell Sheet Using a Thermosensitive Hydrogel and Its Effect on Therapeutic Angiogenesis Biomacromolecules 2013, 14, 4309-4319
46. Kim, D. W.; Jun, I.; Lee, T. J.; Lee, J. H.; Lee, Y. J.; Jang, H. K.; Kang, S.; Park, K. D.; Cho, S. W.; Kim, B. S. et al. Therapeutic Angiogenesis by a Myoblast Layer Harvested by Tissue Transfer Printing from Cell-Adhesive, Thermosensitive Hydrogels Biomaterials 2013, 34, 8258-8268
47. Juhasa, M.; Engelmayr, C. G.; Fontanella, N. A.; Palmerb, M. G.; Bursac, N. Biomimetic Engineered Muscle with Capacity for Vascular Integration and Functional Maturation in Vivo Proc. Natl. Acad. Sci. U.S.A. 2014, 15, 5508-5513
48. Sekine, H.; Shimizu, T.; Sakaguchi, K.; Dobashi, I.; Wada, M.; Yamato, M.; Kobayashi, E.; Umezu, M.; Okano, T. In Vitro Fabrication of Functional Three-Dimensional Tissues with Perfusable Blood Vessels Nat. Commun. 2013, 4, 1399
49. Shweiki, D.; Itin, A.; Soffer, D.; Keshet, E. Vascular Endothelial Growth-Factor Induced by Hypoxia May Mediate Hypoxia-Initiated Angiogenesis Nature 1992, 359, 843-845
50. Levenberg, S.; Rouwkema, J.; Macdonald, M.; Garfein, E. S.; Kohane, D. S.; Darland, D. C.; Marini, R.; van Blitterswijk, C. A.; Mulligan, R. C.; DAmore, P. A. et al. Engineering Vascularized Skeletal Muscle Tissue Nat. Biotechnol. 2005, 23, 879-884
51. van Velthoven, C. T.; Kavelaars, A.; van Bel, F.; Heijnen, C. J. Mesenchymal Stem Cell Treatment after Neonatal Hypoxic-Ischemic Brain Injury Improves Behavioral Outcome and Induces Neuronal and Oligodendrocyte Regeneration Brain Behav. Immun. 2010, 24, 387-393
52. Bae, S.; Kim, H.; Lee, Y.; Xu, X.; Park, J. S.; Zheng, Y.; Balakrishnan, J.; Lei, T.; Kim, H. R.; Song, Y. I. et al. Roll-to-Roll Production of 30-inch Graphene Films for Transparent Electrodes Nat. Nanotechnol. 2010, 5, 574-578