Multiscale, hierarchically patterned topography for directing human neural stem cells into functional neurons

ACS Nano

Volumn 8, Issue 8, 2014, Pages 7809-7822

  Yang, Kisuk ^a   Jung, Hyunjung ^b   Lee, Hak Rae ^c   Lee, Jong Seung ^a   Kim, Su Ran ^a   Song, Ki Yeong ^a   Cheong, Eunji ^a   Bang, Joona ^b   Im, Sung Gap ^c   Cho, Seung Woo ^a  

^a Yonsei University   (South Korea)

^b Korea University   (South Korea)

^c Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

cytoskeleton alignment; differentiation; focal adhesion; hierarchically patterned substrate; human neural stem cell; topographical stimulation

Indexed keywords

ADHESION; ALIGNMENT; BLOCK COPOLYMERS; DIFFERENTIATION (CALCULUS); ELECTROPHYSIOLOGY; FILM PREPARATION; NANOPORES; NEURONS; PHOTOLITHOGRAPHY; PROTEINS; SCAFFOLDS (BIOLOGY); SUBSTRATES; TOPOGRAPHY;

CYTOSKELETONS; FOCAL ADHESIONS; NEURAL STEM CELL; PATTERNED SUBSTRATES; TOPOGRAPHICAL STIMULATION;

STEM CELLS;

CELL DIFFERENTIATION; CYTOLOGY; CYTOSKELETON; DEVICES; FOCAL ADHESION; HUMAN; MECHANOTRANSDUCTION; METABOLISM; MICROTECHNOLOGY; NANOTECHNOLOGY; NERVE CELL; NEURAL STEM CELL; PHENOTYPE; PROCEDURES;

CELL DIFFERENTIATION; CYTOSKELETON; FOCAL ADHESIONS; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MICROTECHNOLOGY; NANOTECHNOLOGY; NEURAL STEM CELLS; NEURONS; PHENOTYPE;

EID: 84906658964     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn501182f     Document Type: Article

References (51)

1. Schuldiner, M.; Eiges, R.; Eden, A.; Yanuka, O.; Itskovitz-Eldor, J.; Goldstein, R. S.; Benvenisty, N. Induced Neuronal Differentiation of Human Embryonic Stem Cells Brain Res. 2001, 913, 201-205
2. Blurton-Jones, M.; Kitazawa, M.; Martinez-Coria, H.; Castello, N. A.; Müller, F.-J.; Loring, J. F.; Yamasaki, T. R.; Poon, W. W.; Green, K. N.; LaFerla, F. M. Neural Stem Cells Improve Cognition via BDNF in a Transgenic Model of Alzheimer Disease Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 13594-13599
3. Discher, D. E.; Mooney, D. J.; Zandstra, P. W. Growth Factors, Matrices, and Forces Combine and Control Stem Cells Science 2009, 324, 1673-1677
4. Yang, K.; Lee, J. S.; Kim, J.; Lee, Y. B.; Shin, H.; Um, S. H.; Kim, J. B.; Park, K. I.; Lee, H.; Cho, S. W. Polydopamine-Mediated Surface Modification of Scaffold Materials for Human Neural Stem Cell Engineering Biomaterials 2012, 33, 6952-6964
5. Ko, E.; Yang, K.; Shin, J.; Cho, S. W. Polydopamine-Assisted Osteoinductive Peptide Immobilization of Polymer Scaffolds for Enhanced Bone Regeneration by Human Adipose-Derived Stem Cells Biomacromolecules 2013, 14, 3202-3213
6. Engler, A. J.; Sen, S.; Sweeney, H. L.; Discher, D. E. Matrix Elasticity Directs Stem Cell Lineage Specification Cell 2006, 126, 677-689
7. Cameron, A. R.; Frith, J. E.; Cooper-White, J. J. The Influence of Substrate Creep on Mesenchymal Stem Cell Behaviour and Phenotype Biomaterials 2011, 32, 5979-5993
8. Trappmann, B.; Gautrot, J. E.; Connelly, J. T.; Strange, D. G.; Li, Y.; Oyen, M. L.; Stuart, M. A. C.; Boehm, H.; Li, B.; Vogel, V. Extracellular-Matrix Tethering Regulates Stem-Cell Fate Nat. Mater. 2012, 11, 642-649
9. Yamamoto, K.; Takahashi, T.; Asahara, T.; Ohura, N.; Sokabe, T.; Kamiya, A.; Ando, J. Proliferation, Differentiation, and Tube Formation by Endothelial Progenitor Cells in Response to Shear Stress J. Appl. Phys. 2003, 95, 2081-2088
10. Swift, J.; Ivanovska, I. L.; Buxboim, A.; Harada, T.; Dingal, P. C.; Pinter, J.; Pajerowski, J. D.; Spinler, K. R.; Shin, J. W.; Tewari, M. et al. Nuclear Lamin-a Scales with Tissue Stiffness and Enhances Matrix-Directed Differentiation Science 2013, 341, 1240104
11. Dalby, M. J.; Gadegaard, N.; Tare, R.; Andar, A.; Riehle, M. O.; Herzyk, P.; Wilkinson, C. D.; Oreffo, R. O. The Control of Human Mesenchymal Cell Differentiation Using Nanoscale Symmetry and Disorder Nat. Mater. 2007, 6, 997-1003
12. Yao, X.; Peng, R.; Ding, J. Effects of Aspect Ratios of Stem Cells on Lineage Commitments with and without Induction Media Biomaterials 2013, 34, 930-939
13. Aizawa, Y.; Shoichet, M. S. The Role of Endothelial Cells in the Retinal Stem and Progenitor Cell Niche within a 3d Engineered Hydrogel Matrix Biomaterials 2012, 33, 5198-5205
14. Guerrero, J.; Catros, S.; Derkaoui, S. M.; Lalande, C.; Siadous, R.; Bareille, R.; Thebaud, N.; Bordenave, L.; Chassande, O.; Le Visage, C. et al. Cell Interactions between Human Progenitor-Derived Endothelial Cells and Human Mesenchymal Stem Cells in a Three-Dimensional Macroporous Polysaccharide-Based Scaffold Promote Osteogenesis Acta Biomater. 2013, 9, 8200-8213
15. Guvendiren, M.; Burdick, J. A. Stem Cell Response to Spatially and Temporally Displayed and Reversible Surface Topography Adv. Healthcare Mater. 2013, 2, 155-164
16. Yim, E. K.; Darling, E. M.; Kulangara, K.; Guilak, F.; Leong, K. W. Nanotopography-Induced Changes in Focal Adhesions, Cytoskeletal Organization, and Mechanical Properties of Human Mesenchymal Stem Cells Biomaterials 2010, 31, 1299-1306
17. Teo, B. K.; Wong, S. T.; Lim, C. K.; Kung, T. Y.; Yap, C. H.; Ramagopal, Y.; Romer, L. H.; Yim, E. K. Nanotopography Modulates Mechanotransduction of Stem Cells and Induces Differentiation through Focal Adhesion Kinase ACS Nano 2013, 7, 4785-4798
18. Teo, B. K.; Ankam, S.; Chan, L. Y.; Yim, E. K. Nanotopography/Mechanical Induction of Stem-Cell Differentiation Methods Cell Biol. 2010, 98, 241-294
19. Lee, M. R.; Kwon, K. W.; Jung, H.; Kim, H. N.; Suh, K. Y.; Kim, K.; Kim, K.-S. Direct Differentiation of Human Embryonic Stem Cells into Selective Neurons on Nanoscale Ridge/Groove Pattern Arrays Biomaterials 2010, 31, 4360-4366
20. Ahn, E. H.; Kim, Y.; Kshitiz, A. S. S.; Afzal, J.; Lee, S.; Kwak, M.; Suh, K. Y.; Kim, D. H.; Levchenko, A. Spatial Control of Adult Stem Cell Fate Using Nanotopographic Cues Biomaterials 2014, 35, 2401-2410
21. Ankam, S.; Suryana, M.; Chan, L. Y.; Moe, A. A.; Teo, B. K.; Law, J. B.; Sheetz, M. P.; Low, H. Y.; Yim, E. K. Substrate Topography and Size Determine the Fate of Human Embryonic Stem Cells to Neuronal or Glial Lineage Acta Biomater. 2013, 9, 4535-4545
22. Yang, K.; Jung, K.; Ko, E.; Kim, J.; Park, K. I.; Kim, J.; Cho, S.-W. Nanotopographical Manipulation of Focal Adhesion Formation for Enhanced Differentiation of Human Neural Stem Cells ACS Appl. Mater. Interfaces 2013, 5, 10529-10540
23. Kim, M. J.; Lee, B.; Yang, K.; Park, J.; Jeon, S.; Um, S. H.; Kim, D. I.; Im, S. G.; Cho, S. W. BMP-2 Peptide-Functionalized Nanopatterned Substrates for Enhanced Osteogenic Differentiation of Human Mesenchymal Stem Cells Biomaterials 2013, 34, 7236-7246
24. Tay, C. Y.; Yu, H.; Pal, M.; Leong, W. S.; Tan, N. S.; Ng, K. W.; Leong, D. T.; Tan, L. P. Micropatterned Matrix Directs Differentiation of Human Mesenchymal Stem Cells Towards Myocardial Lineage Exp. Cell. Res. 2010, 316, 1159-1168
25. Xiong, J. P.; Stehle, T.; Zhang, R.; Joachimiak, A.; Frech, M.; Goodman, S. L.; Arnaout, M. A. Crystal Structure of the Extracellular Segment of Integrin Alpha Vbeta3 in Complex with an Arg-Gly-Asp Ligand Science 2002, 296, 151-155
26. Wang, X.; Yan, C.; Ye, K.; He, Y.; Li, Z.; Ding, J. Effect of RGD Nanospacing on Differentiation of Stem Cells Biomaterials 2013, 34, 2865-2874
27. Petrie, T. A.; Raynor, J. E.; Dumbauld, D. W.; Lee, T. T.; Jagtap, S.; Templeman, K. L.; Collard, D. M.; Garcia, A. J. Multivalent Integrin-Specific Ligands Enhance Tissue Healing and Biomaterial Integration Sci. Transl. Med. 2010, 2, 45ra60
28. Moe, A. A.; Suryana, M.; Marcy, G.; Lim, S. K.; Ankam, S.; Goh, J. Z.; Jin, J.; Teo, B. K.; Law, J. B.; Low, H. Y. et al. Microarray with Micro- and Nano-Topographies Enables Identification of the Optimal Topography for Directing the Differentiation of Primary Murine Neural Progenitor Cells Small 2012, 8, 3050-3061
29. Bang, J.; Jeong, U.; Ryu, D. Y.; Russell, T. P.; Hawker, C. J. Block Copolymer Nanolithography: Translation of Molecular Level Control to Nanoscale Patterns Adv. Mater. 2009, 21, 4769-4792
30. Stoykovich, M. P.; Nealey, P. F. Block Copolymers and Conventional Lithography Mater. Today 2006, 9, 20-29
31. Hawker, C. J.; Russell, T. P. Block Copolymer Lithography: Merging "Bottom-up" with "Top-Down" Processes MRS Bull. 2005, 30, 952-966
32. Bang, J.; Bae, J.; Löwenhielm, P.; Spiessberger, C.; Given-Beck, S. A.; Russell, T. P.; Hawker, C. J. Facile Routes to Patterned Surface Neutralization Layers for Block Copolymer Lithography Adv. Mater. 2007, 19, 4552-4557
33. Leibfarth, F. A.; Kang, M.; Ham, M.; Kim, J.; Campos, L. M.; Gupta, N.; Moon, B.; Hawker, C. J. A Facile Route to Ketene-Functionalized Polymers for General Materials Applications Nat. Chem. 2010, 2, 207-212
34. Jung, H.; Leibfarth, F. A.; Woo, S.; Lee, S.; Kang, M.; Moon, B.; Hawker, C. J.; Bang, J. Efficient Surface Neutralization and Enhanced Substrate Adhesion through Ketene Mediated Crosslinking and Functionalization Adv. Funct. Mater. 2012, 23, 1597-1602
35. Jung, H.; Hwang, D.; Kim, E.; Kim, B.-J.; Lee, W. B.; Poelma, J. E.; Kim, J.; Hawker, C. J.; Huh, J.; Ryu, D. Y. Three-Dimensional Multilayered Nanostructures with Controlled Orientation of Microdomains from Cross-Linkable Block Copolymers ACS Nano 2011, 5, 6164-6173
36. Chen, Y.-C.; Lee, D.-C.; Tsai, T.-Y.; Hsiao, C.-Y.; Liu, J.-W.; Kao, C.-Y.; Lin, H.-K.; Chen, H.-C.; Palathinkal, T. J.; Pong, W.-F. Induction and Regulation of Differentiation in Neural Stem Cells on Ultra-Nanocrystalline Diamond Films Biomaterials 2010, 31, 5575-5587
37. Wang, X.; Song, W.; Kawazoe, N.; Chen, G. The Osteogenic Differentiation of Mesenchymal Stem Cells by Controlled Cell-Cell Interaction on Micropatterned Surfaces J. Biomed. Mater. Res., Part A 2013, 101, 3388-3395
38. Hynes, R. O. Integrins: Versatility, Modulation, and Signaling in Cell Adhesion Cell 1992, 69, 11-25
39. Kuo, S. W.; Lin, H. I.; Ho, J. H.; Shih, Y. R.; Chen, H. F.; Yen, T. J.; Lee, O. K. Regulation of the Fate of Human Mesenchymal Stem Cells by Mechanical and Stereo-Topographical Cues Provided by Silicon Nanowires Biomaterials 2012, 33, 5013-5022
40. Seo, C. H.; Furukawa, K.; Montagne, K.; Jeong, H.; Ushida, T. The Effect of Substrate Microtopography on Focal Adhesion Maturation and Actin Organization via the Rhoa/Rock Pathway Biomaterials 2011, 32, 9568-9575
41. Seo, C. H.; Jeong, H.; Feng, Y.; Montagne, K.; Ushida, T.; Suzuki, Y.; Furukawa, K. S. Micropit Surfaces Designed for Accelerating Osteogenic Differentiation of Murine Mesenchymal Stem Cells via Enhancing Focal Adhesion and Actin Polymerization Biomaterials 2014, 35, 2245-2252
42. Shih, Y. R.; Tseng, K. F.; Lai, H. Y.; Lin, C. H.; Lee, O. K. Matrix Stiffness Regulation of Integrin-Mediated Mechanotransduction During Osteogenic Differentiation of Human Mesenchymal Stem Cells J. Bone Miner. Res. 2011, 26, 730-738
43. Sun, Y.; Yong, K. M.; Villa-Diaz, L. G.; Zhang, X.; Chen, W.; Philson, R.; Weng, S.; Xu, H.; Krebsbach, P. H.; Fu, J. Hippo/Yap-Mediated Rigidity-Dependent Motor Neuron Differentiation of Human Pluripotent Stem Cells Nat. Mater. 2014, 13, 599-604
44. Yang, C.; Tibbitt, M. W.; Basta, L.; Anseth, K. S. Mechanical Memory and Dosing Influence Stem Cell Fate Nat. Mater. 2014, 13, 645-652
45. Dupont, S.; Morsut, L.; Aragona, M.; Enzo, E.; Giulitti, S.; Cordenonsi, M.; Zanconato, F.; Le Digabel, J.; Forcato, M.; Bicciato, S. et al. Role of Yap/Taz in Mechanotransduction Nature 2011, 474, 179-183
46. Zala, D.; Hinckelmann, M. V.; Yu, H.; Lyra da Cunha, M. M.; Liot, G.; Cordelieres, F. P.; Marco, S.; Saudou, F. Vesicular Glycolysis Provides on-Board Energy for Fast Axonal Transport Cell 2013, 152, 479-491
47. Morgan, P. J.; Liedmann, A.; Hubner, R.; Hovakimyan, M.; Rolfs, A.; Frech, M. J. Human Neural Progenitor Cells Show Functional Neuronal Differentiation and Regional Preference after Engraftment onto Hippocampal Slice Cultures Stem Cells Dev. 2012, 21, 1501-1512
48. Vukicevic, V.; Schmid, J.; Hermann, A.; Lange, S.; Qin, N.; Gebauer, L.; Chunk, K. F.; Ravens, U.; Eisenhofer, G.; Storch, A. et al. Differentiation of Chromaffin Progenitor Cells to Dopaminergic Neurons Cell Transplant. 2012, 21, 2471-2486
49. Yang, K.; Han, S.; Shin, Y.; Ko, E.; Kim, J.; Park, K. I.; Chung, S.; Cho, S.-W. A Microfluidic Array for Quantitative Analysis of Human Neural Stem Cell Self-Renewal and Differentiation in Three-Dimensional Hypoxic Microenvironment Biomaterials 2013, 34, 6607-6614
50. Cho, S. W.; Goldberg, M.; Son, S. M.; Xu, Q.; Yang, F.; Mei, Y.; Bogatyrev, S.; Langer, R.; Anderson, D. G. Lipid-Like Nanoparticles for Small Interfering RNA Delivery to Endothelial Cells Adv. Funct. Mater. 2009, 19, 3112-3118
51. Savic, R.; Azzam, T.; Eisenberg, A.; Maysinger, D. Assessment of the Integrity of Poly(Caprolactone)- b -Poly(Ethylene Oxide) Micelles under Biological Conditions: A Fluorogenic-Based Approach Langmuir 2006, 22, 3570-3578