Thermoresponsive nanofabricated substratum for the engineering of three-dimensional tissues with layer-by-layer architectural control

ACS Nano

Volumn 8, Issue 5, 2014, Pages 4430-4439

  Jiao, Alex ^a   Trosper, Nicole E ^a   Yang, Hee Seok ^a,b   Kim, Jinsung ^a   Tsui, Jonathan H ^a   Frankel, Samuel D ^a   Murry, Charles E ^a,c   Kim, Deok Ho ^a,c  

^a University of Washington   (United States)

^b Dankook University   (South Korea)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

thermoresponsive; three dimensional; tissue engineering

Indexed keywords

ANISOTROPY; CELLS; CYTOLOGY; HISTOLOGY; STRUCTURAL DYNAMICS; THREE DIMENSIONAL; TISSUE; TISSUE ENGINEERING;

ARCHITECTURAL CONTROL; CULTURE TEMPERATURE; ENGINEERING METHODS; HIERARCHICAL CONTROL; PHYSIOLOGICAL STRUCTURES; STRUCTURAL ANISOTROPY; STRUCTURAL CONTROL; THERMO-RESPONSIVE;

SCAFFOLDS (BIOLOGY);

GEL; NANOMATERIAL; POLYMER;

ANIMAL; ANISOTROPY; CELL LINE; CHEMISTRY; COMPUTER PROGRAM; FLUORESCENCE MICROSCOPY; GEL; HEAT; HUMAN; MOUSE; NANOTECHNOLOGY; NORMAL DISTRIBUTION; PROCEDURES; STRUCTURE ACTIVITY RELATION; SURFACE PROPERTY; THREE DIMENSIONAL IMAGING; TISSUE ENGINEERING; TISSUE SCAFFOLD;

ANIMALS; ANISOTROPY; CELL LINE; GELS; HOT TEMPERATURE; HUMANS; IMAGING, THREE-DIMENSIONAL; MICE; MICROSCOPY, FLUORESCENCE; NANOSTRUCTURES; NANOTECHNOLOGY; NORMAL DISTRIBUTION; POLYMERS; SOFTWARE; STRUCTURE-ACTIVITY RELATIONSHIP; SURFACE PROPERTIES; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84901650220     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn4063962     Document Type: Article

References (52)

1. Pampaloni, F.; Reynaud, E. G.; Stelzer, E. H. K. The Third Dimension Bridges the Gap between Cell Culture and Live Tissue Nat. Rev. Mol. Cell Biol. 2007, 8, 839-845
2. Griffith, L. G.; Swartz, M. A. Capturing Complex 3d Tissue Physiology in Vitro Nat. Rev. Mol. Cell Biol. 2006, 7, 211-224
3. Gauvin, R.; Khademhosseini, A. Microscale Technologies and Modular Approaches for Tissue Engineering: Moving toward the Fabrication of Complex Functional Structures ACS Nano 2011, 5, 4258-4264
4. Guerin, H. L.; Elliott, D. M. Quantifying the Contributions of Structure to Annulus Fibrosus Mechanical Function Using a Nonlinear, Anisotropic, Hyperelastic Model J. Orthop. Res. 2007, 25, 508-516
5. Lundon, K. Structure and Function of the Lumbar Intervertebral Disk in Health, Aging, and Pathologic Conditions J. Orthop. Sports Phys. Ther. 2001, 31, 291-306
6. Nikolaidou, T.; Aslanidi, O. V.; Zhang, H.; Efimov, I. R. Structure-Function Relationship in the Sinus and Atrioventricular Nodes Pediatr. Cardiol. 2012, 33, 890-899
7. Aagaard, P.; Andersen, J. L.; Dyhre-Poulsen, P.; Leffers, A.-M.; Wagner, A.; Magnusson, S. P.; Halkjær-Kristensen, J.; Simonsen, E. B. A Mechanism for Increased Contractile Strength of Human Pennate Muscle in Response to Strength Training: Changes in Muscle Architecture J. Physiol. 2001, 534, 613-623
8. Azizi, E.; Brainerd, E. L.; Roberts, T. J. Variable Gearing in Pennate Muscles Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 1745-1750
9. Kanzaki, Y.; Yamauchi, Y.; Okabe, M.; Terasaki, F.; Ishizaka, N. Three-Dimensional Architecture of Cardiomyocytes and Connective Tissues in Hypertrophic Cardiomyopathy: A Scanning Electron Microscopic Observation Circulation 2012, 125, 738-739
10. Fonseca, H.; Moreira-Gonçalves, D.; Coriolano, H.-J.; Duarte, J. Bone Quality: The Determinants of Bone Strength and Fragility Sports Med. 2014, 44, 37-53
11. McDevitt, T. C.; Angello, J. C.; Whitney, M. L.; Reinecke, H.; Hauschka, S. D.; Murry, C. E.; Stayton, P. S. In Vitro Generation of Differentiated Cardiac Myofibers on Micropatterned Laminin Surfaces J. Biomed. Mater. Res. 2002, 60, 472-479
12. Kuo, P.-L.; Lee, H.; Bray, M.-A.; Geisse, N. A.; Huang, Y.-T.; Adams, W. J.; Sheehy, S. P.; Parker, K. K. Myocyte Shape Regulates Lateral Registry of Sarcomeres and Contractility Am. J. Pathol. 2012, 181, 2030-2037
13. Kada, K.; Yasui, K.; Naruse, K.; Kamiya, K.; Kodama, I.; Toyama, J. Orientation Change of Cardiocytes Induced by Cyclic Stretch Stimulation: Time Dependency and Involvement of Protein Kinases J. Mol. Cell. Cardiol. 1999, 31, 247-259
14. Neidlinger-Wilke, C.; Grood, E. S.; Wang, J. H.-C.; Brand, R. A.; Claes, L. Cell Alignment Is Induced by Cyclic Changes in Cell Length: Studies of Cells Grown in Cyclically Stretched Substrates J. Orthop. Res. 2001, 19, 286-293
15. Salameh, A.; Wustmann, A.; Karl, S.; Blanke, K.; Apel, D.; Rojas-Gomez, D.; Franke, H.; Mohr, F. W.; Janousek, J.; Dhein, S. Cyclic Mechanical Stretch Induces Cardiomyocyte Orientation and Polarization of the Gap Junction Protein Connexin43 Circ. Res. 2010, 106, 1592-602
16. Sato, M.; Ito, A.; Akiyama, H.; Kawabe, Y.; Kamihira, M. Effects of B-Cell Lymphoma 2 Gene Transfer to Myoblast Cells on Skeletal Muscle Tissue Formation Using Magnetic Force-Based Tissue Engineering Tissue Eng., Part A 2012, 19, 307-315
17. Coletti, D.; Teodori, L.; Albertini, M. C.; Rocchi, M.; Pristerà, A.; Fini, M.; Molinaro, M.; Adamo, S. Static Magnetic Fields Enhance Skeletal Muscle Differentiation in Vitro by Improving Myoblast Alignment Cytometry, Part A 2007, 71A, 846-856
18. Radisic, M.; Park, H.; Shing, H.; Consi, T.; Schoen, F. J.; Langer, R.; Freed, L. E.; Vunjak-Novakovic, G. Functional Assembly of Engineered Myocardium by Electrical Stimulation of Cardiac Myocytes Cultured on Scaffolds Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 18129-18134
19. Tandon, N.; Cannizzaro, C.; Chao, P.-h. G.; Maidhof, R.; Ting, H.; Au, H.; Radisic, M.; Vunjak-Novakovic, G. Electrical Stimulation Systems for Cardiac Tissue Engineering Nat. Protoc. 2009, 4, 155-173
20. Gelain, F.; Silva, D.; Caprini, A.; Taraballi, F.; Natalello, A.; Villa, O.; Nam, K. T.; Zuckermann, R. N.; Doglia, S. M.; Vescovi, A. Bmhp1-Derived Self-Assembling Peptides: Hierarchically Assembled Structures with Self-Healing Propensity and Potential for Tissue Engineering Applications ACS Nano 2011, 5, 1845-1859
21. Caldwell, D. J.; Rao, R. R.; Stegemann, J. P. Assembly of Discrete Collagen-Chitosan Microenvironments into Multiphase Tissue Constructs Adv. Healthcare Mater. 2013, 2, 673-677
22. Haraguchi, Y.; Shimizu, T.; Sasagawa, T.; Sekine, H.; Sakaguchi, K.; Kikuchi, T.; Sekine, W.; Sekiya, S.; Yamato, M.; Umezu, M.; Okano, T. Fabrication of Functional Three-Dimensional Tissues by Stacking Cell Sheets in Vitro Nat. Protoc. 2012, 7, 850-858
23. Takahashi, H.; Shimizu, T.; Nakayama, M.; Yamato, M.; Okano, T. The Use of Anisotropic Cell Sheets To Control Orientation during the Self-Organization of 3D Muscle Tissue Biomaterials 2013, 34, 7372-7380
24. Williams, C.; Xie, A. W.; Yamato, M.; Okano, T.; Wong, J. Y. Stacking of Aligned Cell Sheets for Layer-by-Layer Control of Complex Tissue Structure Biomaterials 2011, 32, 5625-5632
25. Xia, Y.; He, X.; Cao, M.; Chen, C.; Xu, H.; Pan, F.; Lu, J. R. Thermoresponsive Microgel Films for Harvesting Cells and Cell Sheets Biomacromolecules 2013, 14, 3615-3625
26. Radisic, M.; Malda, J.; Epping, E.; Geng, W.; Langer, R.; Vunjak-Novakovic, G. Oxygen Gradients Correlate with Cell Density and Cell Viability in Engineered Cardiac Tissue Biotechnol. Bioeng. 2006, 93, 332-343
27. Vunjak-Novakovic, G.; Tandon, N.; Godier, A.; Maidhof, R.; Marsano, A.; Martens, T. P.; Radisic, M. Challenges in Cardiac Tissue Engineering Tissue Eng., Part B 2010, 16, 169-187
28. Tatkiewicz, W. I.; Seras-Franzoso, J.; García-Fruitós, E.; Vazquez, E.; Ventosa, N.; Peebo, K.; Ratera, I.; Villaverde, A.; Veciana, J. Two-Dimensional Microscale Engineering of Protein-Based Nanoparticles for Cell Guidance ACS Nano 2013, 7, 4774-4784
29. Zan, X.; Feng, S.; Balizan, E.; Lin, Y.; Wang, Q. Facile Method for Large Scale Alignment of One Dimensional Nanoparticles and Control over Myoblast Orientation and Differentiation ACS Nano 2013, 7, 8385-8396
30. Namgung, S.; Baik, K. Y.; Park, J.; Hong, S. Controlling the Growth and Differentiation of Human Mesenchymal Stem Cells by the Arrangement of Individual Carbon Nanotubes ACS Nano 2011, 5, 7383-7390
31. Kim, H. N.; Jiao, A.; Hwang, N. S.; Kim, M. S.; Kang, D. H.; Kim, D.-H.; Suh, K.-Y. Nanotopography-Guided Tissue Engineering and Regenerative Medicine Adv. Drug Delivery Rev. 2013, 64, 536-558
32. Kim, D.-H.; Seo, C.-H.; Han, K.; Kwon, K. W.; Levchenko, A.; Suh, K.-Y. Guided Cell Migration on Microtextured Substrates with Variable Local Density and Anisotropy Adv. Funct. Mater. 2009, 19, 1579-1586
33. Kim, D.-H.; Han, K.; Gupta, K.; Kwon, K. W.; Suh, K.-Y.; Levchenko, A. Mechanosensitivity of Fibroblast Cell Shape and Movement to Anisotropic Substratum Topography Gradients Biomaterials 2009, 30, 5433-5444
34. Kim, D.-H.; Lipke, E. A.; Kim, P.; Cheong, R.; Thompson, S.; Delannoy, M.; Suh, K.-Y.; Tung, L.; Levchenko, A. Nanoscale Cues Regulate the Structure and Function of Macroscopic Cardiac Tissue Constructs Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 565-570
35. Kim, P.; Kim, D. H.; Kim, B.; Choi, S. K.; Lee, S. H.; Khademhosseini, A.; Langer, R.; Suh, K. Y. Fabrication of Nanostructures of Polyethylene Glycol for Applications to Protein Adsorption and Cell Adhesion Nanotechnology 2005, 16, 2420-2426
36. Nagase, K.; Watanabe, M.; Kikuchi, A.; Yamato, M.; Okano, T. Thermo-Responsive Polymer Brushes as Intelligent Biointerfaces: Preparation via ATRP and Characterization Macromol. Biosci. 2011, 11, 400-409
37. Mudera, V. C.; Pleass, R.; Eastwood, M.; Tarnuzzer, R.; Schultz, G.; Khaw, P.; McGrouther, D. A.; Brown, R. A. Molecular Responses of Human Dermal Fibroblasts to Dual Cues: Contact Guidance and Mechanical Load Cell Motil. Cytoskeleton 2000, 45, 1-9
38. Au, H. T. H.; Cheng, I.; Chowdhury, M. F.; Radisic, M. Interactive Effects of Surface Topography and Pulsatile Electrical Field Stimulation on Orientation and Elongation of Fibroblasts and Cardiomyocytes Biomaterials 2007, 28, 4277-4293
39. Ramaglia, L.; Capece, G.; Di Spigna, G.; Bruno, M. P.; Buonocore, N.; Postiglione, L. Effects of Titanium Surface Topography on Morphology and in Vitro Activity of Human Gingival Fibroblasts Minerva Stomatol. 2013, 62, 267-280
40. Karamichos, D.; Funderburgh, M. L.; Hutcheon, A. E. K.; Zieske, J. D.; Du, Y.; Wu, J.; Funderburgh, J. L. A Role for Topographic Cues in the Organization of Collagenous Matrix by Corneal Fibroblasts and Stem Cells PLoS One 2014, 9, e86260
41. Lai, Y.; Chen, J.; Zhang, T.; Gu, D.; Zhang, C.; Li, Z.; Lin, S.; Fu, X.; Schultze-Mosgau, S. Effect of 3d Microgroove Surface Topography on Plasma and Cellular Fibronectin of Human Gingival Fibroblasts J. Dent. 2013, 41, 1109-1121
42. Wu, J.; Du, Y.; Watkins, S. C.; Funderburgh, J. L.; Wagner, W. R. The Engineering of Organized Human Corneal Tissue through the Spatial Guidance of Corneal Stromal Stem Cells Biomaterials 2012, 33, 1343-1352
43. Canavan, H. E.; Cheng, X.; Graham, D. J.; Ratner, B. D.; Castner, D. G. Surface Characterization of the Extracellular Matrix Remaining after Cell Detachment from a Thermoresponsive Polymer Langmuir 2004, 21, 1949-1955
44. Canavan, H. E.; Cheng, X.; Graham, D. J.; Ratner, B. D.; Castner, D. G. Cell Sheet Detachment Affects the Extracellular Matrix: A Surface Science Study Comparing Thermal Liftoff, Enzymatic, and Mechanical Methods J. Biomed. Mater. Res., Part A 2005, 75A, 1-13
45. Kushida, A.; Yamato, M.; Konno, C.; Kikuchi, A.; Sakurai, Y.; Okano, T. Decrease in Culture Temperature Releases Monolayer Endothelial Cell Sheets Together with Deposited Fibronectin Matrix from Temperature-Responsive Culture Surfaces J. Biomed. Mater. Res. 1999, 45, 355-362
46. Goetsch, K. P.; Myburgh, K. H.; Niesler, C. In Vitro Myoblast Motility Models: Investigating Migration Dynamics for the Study of Skeletal Muscle Repair J. Muscle Res. Cell Motil. 2013, 34, 333-347
47. Kino-oka, M.; Ngo, T. X.; Nagamori, E.; Takezawa, Y.; Miyake, Y.; Sawa, Y.; Saito, A.; Shimizu, T.; Okano, T.; Taya, M. Evaluation of Vertical Cell Fluidity in a Multilayered Sheet of Skeletal Myoblasts J. Biosci. Bioeng. 2012, 113, 128-131
48. Yang, H.-S.; Ieronimakis, N.; Tsui, J. H.; Kim, H. N.; Suh, K.-Y.; Reyes, M.; Kim, D.-H. Nanopatterned Muscle Cell Patches for Enhanced Myogenesis and Dystrophin Expression in a Mouse Model of Muscular Dystrophy Biomaterials 2014, 35, 1478-1486
49. Huang, N. F.; Patel, S.; Thakar, R. G.; Wu, J.; Hsiao, B. S.; Chu, B.; Lee, R. J.; Li, S. Myotube Assembly on Nanofibrous and Micropatterned Polymers Nano Lett. 2006, 6, 537-542
50. Ovsianikov, A.; Gruene, M.; Pflaum, M.; Koch, L.; Maiorana, F.; Wilhelmi, M.; Haverich, A.; Chichkov, B. Laser Printing of Cells into 3D Scaffolds Biofabrication 2010, 2, 014104
51. Hosseini, V.; Ahadian, S.; Ostrovidov, S.; Camci-Unal, G.; Chen, S.; Kaji, H.; Ramalingam, M.; Khademhosseini, A. Engineered Contractile Skeletal Muscle Tissue on a Microgrooved Methacrylated Gelatin Substrate Tissue Eng., Part A 2012, 18, 2453-2465
52. Cho, H.; Jönsson, H.; Campbell, K.; Melke, P.; Williams, J. W.; Jedynak, B.; Stevens, A. M.; Groisman, A.; Levchenko, A. Self-Organization in High-Density Bacterial Colonies: Efficient Crowd Control PLoS Biol. 2007, 5, e302