Microfluidic Assay To Study the Combinatorial Impact of Substrate Properties on Mesenchymal Stem Cell Migration

ACS Applied Materials and Interfaces

Volumn 7, Issue 31, 2015, Pages 17095-17103

  Menon, Nishanth V ^a   Chuah, Yon Jin ^a   Phey, Samantha ^b   Zhang, Ying ^a   Wu, Yingnan ^a   Chan, Vincent ^a   Kang, Yuejun ^a  

^a Nanyang Technological University   (Singapore)

^b Hwa Chong Institution   (Singapore)

Author keywords

cell migration and spreading; extracellular matrix; human bone marrow derived mesenchymal stem cells; roughness; stiffness; substratum properties; wettability

Indexed keywords

BONE; CELL ADHESION; CELL CULTURE; CELLS; CYTOLOGY; ENZYME ACTIVITY; HYDROPHOBICITY; MICROCHANNELS; MICROFLUIDICS; PHYSICAL PROPERTIES; PHYSIOLOGICAL MODELS; PHYSIOLOGY; SILICONES; STEM CELLS; STIFFNESS; STIFFNESS MATRIX; SUBSTRATES; SURFACE ROUGHNESS; TISSUE; TISSUE ENGINEERING; TISSUE REGENERATION; WETTING;

CELL MIGRATION; COMBINATORIAL PROPERTIES; EXTRACELLULAR MATRICES; HUMAN BONE MARROW DERIVED MESENCHYMAL STEM CELLS; MESENCHYMAL STEM CELL; PHYSIOLOGICAL PROCESS; POLYDIMETHYLSILOXANE (PDMS) SUBSTRATES; SUBSTRATUM PROPERTIES;

SCAFFOLDS (BIOLOGY);

BAYSILON; DIMETICONE; RNA;

ATOMIC FORCE MICROSCOPY; BONE MARROW CELL; CELL ADHESION; CELL CULTURE TECHNIQUE; CELL MOTION; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DEVICES; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; HUMAN; ISOLATION AND PURIFICATION; MESENCHYMAL STROMA CELL; METABOLISM; MICROFLUIDIC ANALYSIS; PROCEDURES; REAL TIME POLYMERASE CHAIN REACTION; REGENERATION;

BONE MARROW CELLS; CELL ADHESION; CELL CULTURE TECHNIQUES; CELL MOVEMENT; CELL SURVIVAL; DIMETHYLPOLYSILOXANES; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; HUMANS; MESENCHYMAL STROMAL CELLS; MICROFLUIDIC ANALYTICAL TECHNIQUES; MICROSCOPY, ATOMIC FORCE; REAL-TIME POLYMERASE CHAIN REACTION; REGENERATION; RNA;

EID: 84939158725     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.5b03753     Document Type: Article

References (66)

1. Arthur, A.; Zannettino, A.; Gronthos, S. The Therapeutic Applications of Multipotential Mesenchymal/Stromal Stem Cells in Skeletal Tissue Repair J. Cell. Physiol. 2009, 218, 237-245 10.1002/jcp.21592
2. Barry, F. P.; Murphy, J. M. Mesenchymal Stem Cells: Clinical Applications and Biological Characterization Int. J. Biochem. Cell Biol. 2004, 36, 568-584 10.1016/j.biocel.2003.11.001
3. Sundelacruz, S.; Kaplan, D. L. Stem Cell- and Scaffold-Based Tissue Engineering Approaches to Osteochondral Regenerative Medicine Semin. Cell Dev. Biol. 2009, 20, 646-655 10.1016/j.semcdb.2009.03.017
4. Barbash, I. M.; Chouraqui, P.; Baron, J.; Feinberg, M. S.; Etzion, S.; Tessone, A.; Miller, L.; Guetta, E.; Zipori, D.; Kedes, L. H.; Kloner, R. A.; Leor, J. Systemic Delivery of Bone Marrow-Derived Mesenchymal Stem Cells to the Infarcted Myocardium: Feasibility, Cell Migration, and Body Distribution Circulation 2003, 108, 863-868 10.1161/01.CIR.0000084828.50310.6A
5. Drury, J. L.; Mooney, D. J. Hydrogels for Tissue Engineering: Scaffold Design Variables and Applications Biomaterials 2003, 24, 4337-4351 10.1016/S0142-9612(03)00340-5
6. Kim, D.-H.; Provenzano, P. P.; Smith, C. L.; Levchenko, A. Matrix Nanotopography as a Regulator of Cell Function J. Cell Biol. 2012, 197, 351-360 10.1083/jcb.201108062
7. Kleinman, H. K.; Philp, D.; Hoffman, M. P. Role of the Extracellular Matrix in Morphogenesis Curr. Opin. Biotechnol. 2003, 14, 526-532 10.1016/j.copbio.2003.08.002
8. Watt, F. M. The Extracellular Matrix and Cell Shape Trends Biochem. Sci. 1986, 11, 482-485 10.1016/0968-0004(86)90252-5
9. Reig, G.; Pulgar, E.; Concha, M. L. Cell Migration: From Tissue Culture to Embryos Development 2014, 141, 1999-2013 10.1242/dev.101451
10. Li, S.; Guan, J.-L.; Chien, S. Biochemstry and Biomechanics of Cell Motility Annu. Rev. Biomed. Eng. 2005, 7, 105-150 10.1146/annurev.bioeng.7.060804.100340
11. Brandl, F.; Sommer, F.; Goepferich, A. Rational Design of Hydrogels for Tissue Engineering: Impact of Physical Factors on Cell Behavior Biomaterials 2007, 28, 134-146 10.1016/j.biomaterials.2006.09.017
12. Han, J.; Menon, N. V.; Kang, Y.; Tee, S.-Y. An in Vitro Study on the Collective Tumor Cell Migration on Nanoroughened Poly(Dimethylsiloxane) Surfaces J. Mater. Chem. B 2015, 3, 1565-1572 10.1039/C4TB01783H
13. Shin, H. Fabrication Methods of an Engineered Microenvironment for Analysis of Cell-Biomaterial Interactions Biomaterials 2007, 28, 126-133 10.1016/j.biomaterials.2006.08.007
14. Zhu, J.; Marchant, R. E. Design Properties of Hydrogel Tissue-Engineering Scaffolds Expert Rev. Med. Devices 2011, 8, 607-626 10.1586/erd.11.27
15. Bose, S.; Roy, M.; Bandyopadhyay, A. Recent Advances in Bone Tissue Engineering Scaffolds Trends Biotechnol. 2012, 30, 546-554 10.1016/j.tibtech.2012.07.005
16. Mace, K. A.; Hansen, S. L.; Myers, C.; Young, D. M.; Boudreau, N. Hoxa3 Induces Cell Migration in Endothelial and Epithelial Cells Promoting Angiogenesis and Wound Repair J. Cell Sci. 2005, 118, 2567-2577 10.1242/jcs.02399
17. Chen, H. C. Boyden Chamber Assay Methods Mol. Biol. 2005, 294, 15-22 10.1385/1-59259-860-9:015
18. Meyvantsson, I.; Beebe, D. J. Cell Culture Models in Microfluidic Systems. Annu Annu. Rev. Anal. Chem. 2008, 1, 423-449 10.1146/annurev.anchem.1.031207.113042
19. Voldman, J.; Gray, M. L.; Schmidt, M. A. Microfabrication in Biology and Medicine Annu. Rev. Biomed. Eng. 1999, 1, 401-425 10.1146/annurev.bioeng.1.1.401
20. Beebe, D. J.; Mensing, G. A.; Walker, G. M. Physics and Applications of Microfluidics in Biology Annu. Rev. Biomed. Eng. 2002, 4, 261-286 10.1146/annurev.bioeng.4.112601.125916
21. Cimetta, E.; Cannizzaro, C.; James, R.; Biechele, T.; Moon, R. T.; Elvassore, N.; Vunjak-Novakovic, G. Microfluidic Device Generating Stable Concentration Gradients for Long Term Cell Culture: Application to Wnt3a Regulation of [Small Beta]-Catenin Signaling Lab Chip 2010, 10, 3277-3283 10.1039/c0lc00033g
22. Chung, S.; Sudo, R.; Mack, P. J.; Wan, C.-R.; Vickerman, V.; Kamm, R. D. Cell Migration into Scaffolds under Co-Culture Conditions in a Microfluidic Platform Lab Chip 2009, 9, 269-275 10.1039/B807585A
23. Sia, S. K.; Whitesides, G. M. Microfluidic Devices Fabricated in Poly(Dimethylsiloxane) for Biological Studies Electrophoresis 2003, 24, 3563-3576 10.1002/elps.200305584
24. Leclerc, E.; Sakai, Y.; Fujii, T. Cell Culture in 3-Dimensional Microfluidic Structure of Pdms (Polydimethylsiloxane) Biomed. Microdevices 2003, 5, 109-114 10.1023/A:1024583026925
25. Eroshenko, N.; Ramachandran, R.; Yadavalli, V. K.; Rao, R. R. Effect of Substrate Stiffness on Early Human Embryonic Stem Cell Differentiation J. Biol. Eng. 2013, 7, 7 10.1186/1754-1611-7-7
26. Palchesko, R. N.; Zhang, L.; Sun, Y.; Feinberg, A. W. Development of Polydimethylsiloxane Substrates with Tunable Elastic Modulus to Study Cell Mechanobiology in Muscle and Nerve PLoS One 2012, 7, e51499 10.1371/journal.pone.0051499
27. Park, J.; Yoo, S.; Lee, E.-J.; Lee, D.; Kim, J.; Lee, S.-H. Increased Poly(Dimethylsiloxane) Stiffness Improves Viability and Morphology of Mouse Fibroblast Cells BioChip J. 2010, 4, 230-236 10.1007/s13206-010-4311-9
28. Shen, Y.; Wang, G.; Huang, X.; Zhang, Q.; Wu, J.; Tang, C.; Yu, Q.; Liu, X. Surface Wettability of Plasma Sio(X):H Nanocoating-Induced Endothelial Cells'Migration and the Associated Fak-Rho GTPases Signalling Pathways J. R. Soc., Interface 2012, 9, 313-327 10.1098/rsif.2011.0278
29. Lo, C. M.; Wang, H. B.; Dembo, M.; Wang, Y. L. Cell Movement Is Guided by the Rigidity of the Substrate Biophys. J. 2000, 79, 144-152 10.1016/S0006-3495(00)76279-5
30. Pelham, R. J.; Wang, Y.-l. Cell Locomotion and Focal Adhesions Are Regulated by Substrate Flexibility Proc. Natl. Acad. Sci. U. S. A. 1997, 94, 13661-13665 10.1073/pnas.94.25.13661
31. DiMilla, P. A.; Stone, J. A.; Quinn, J. A.; Albelda, S. M.; Lauffenburger, D. A. Maximal Migration of Human Smooth Muscle Cells on Fibronectin and Type IV Collagen Occurs at an Intermediate Attachment Strength J. Cell Biol. 1993, 122, 729-737 10.1083/jcb.122.3.729
32. Hansen, T. D.; Koepsel, J. T.; Le, N. N.; Nguyen, E. H.; Zorn, S.; Parlato, M.; Loveland, S. G.; Schwartz, M. P.; Murphy, W. L. Biomaterial Arrays with Defined Adhesion Ligand Densities and Matrix Stiffness Identify Distinct Phenotypes for Tumorigenic and Non-Tumorigenic Human Mesenchymal Cell Types Biomater. Sci. 2014, 2, 745-756 10.1039/C3BM60278H
33. Peyton, S. R.; Putnam, A. J. Extracellular Matrix Rigidity Governs Smooth Muscle Cell Motility in a Biphasic Fashion J. Cell. Physiol. 2005, 204, 198-209 10.1002/jcp.20274
34. Stroka, K. M.; Aranda-Espinoza, H. Neutrophils Display Biphasic Relationship between Migration and Substrate Stiffness Cell Motil. Cytoskeleton 2009, 66, 328-341 10.1002/cm.20363
35. Mih, J. D.; Marinkovic, A.; Liu, F.; Sharif, A. S.; Tschumperlin, D. J. Matrix Stiffness Reverses the Effect of Actomyosin Tension on Cell Proliferation J. Cell Sci. 2012, 125, 5974-5983 10.1242/jcs.108886
36. Trkov, S.; Eng, G.; Di Liddo, R.; Parnigotto, P. P.; Vunjak-Novakovic, G. Micropatterned Three-Dimensional Hydrogel System to Study Human Endothelial-Mesenchymal Stem Cell Interactions J. Tissue Eng. Regener. Med. 2010, 4, 205-215 10.1002/term.231
37. McDonald, J. C.; Duffy, D. C.; Anderson, J. R.; Chiu, D. T.; Wu, H.; Schueller, O. J.; Whitesides, G. M. Fabrication of Microfluidic Systems in Poly(Dimethylsiloxane) Electrophoresis 2000, 21, 27-40 10.1002/(SICI)1522-2683(20000101)21:1<27::AID-ELPS27>3.3.CO;2-3
38. Menon, N. V.; Chuah, Y. J.; Cao, B.; Lim, M.; Kang, Y. A Microfluidic Co-Culture System to Monitor Tumor-Stromal Interactions on a Chip Biomicrofluidics 2014, 8, 064118 10.1063/1.4903762
39. Wu, Y.-N.; Law, J. B. K.; He, A. Y.; Low, H. Y.; Hui, J. H. P.; Lim, C. T.; Yang, Z.; Lee, E. H. Substrate Topography Determines the Fate of Chondrogenesis from Human Mesenchymal Stem Cells Resulting in Specific Cartilage Phenotype Formation Nanomedicine 2014, 10, 1507-1516 10.1016/j.nano.2014.04.002
40. Li, D.; Ding, J.; Wang, X.; Wang, C.; Wu, T. Fibronectin Promotes Tyrosine Phosphorylation of Paxillin and Cell Invasiveness in the Gastric Cancer Cell Line Ags Tumori 2009, 95, 769-779
41. Rago, L.; Beattie, R.; Taylor, V.; Winter, J. Mir379-410 Cluster Mirnas Regulate Neurogenesis and Neuronal Migration by Fine-Tuning N-Cadherin EMBO J. 2014, 33, 906-920 10.1002/embj.201386591
42. Fuard, D.; Tzvetkova-Chevolleau, T.; Decossas, S.; Tracqui, P.; Schiavone, P. Optimization of Poly-Di-Methyl-Siloxane (PDMS) Substrates for Studying Cellular Adhesion and Motility Microelectron. Eng. 2008, 85, 1289-1293 10.1016/j.mee.2008.02.004
43. Michael, J. O., Siloxane Surface Activity. In Silicon-Based Polymer Science; American Chemical Society: Washington, DC, 1989; Chapter 40, pp 705-739.
44. Borgioli, F.; Galvanetto, E.; Bacci, T. Influence of Surface Morphology and Roughness on Water Wetting Properties of Low Temperature Nitrided Austenitic Stainless Steels Mater. Charact. 2014, 95, 278-284 10.1016/j.matchar.2014.07.006
45. Yoshimitsu, Z.; Nakajima, A.; Watanabe, T.; Hashimoto, K. Effects of Surface Structure on the Hydrophobicity and Sliding Behavior of Water Droplets Langmuir 2002, 18, 5818-5822 10.1021/la020088p
46. Seo, J.-H.; Sakai, K.; Yui, N. Adsorption State of Fibronectin on Poly(Dimethylsiloxane) Surfaces with Varied Stiffness Can Dominate Adhesion Density of Fibroblasts Acta Biomater. 2013, 9, 5493-5501 10.1016/j.actbio.2012.10.015
47. Chastain, S. R.; Kundu, A. K.; Dhar, S.; Calvert, J. W.; Putnam, A. J. Adhesion of Mesenchymal Stem Cells to Polymer Scaffolds Occurs Via Distinct Ecm Ligands and Controls Their Osteogenic Differentiation J. Biomed. Mater. Res., Part A 2006, 78A, 73-85 10.1002/jbm.a.30686
48. Lee, J. W.; Kim, Y. H.; Park, K. D.; Jee, K. S.; Shin, J. W.; Hahn, S. B. Importance of Integrin B1-Mediated Cell Adhesion on Biodegradable Polymers under Serum Depletion in Mesenchymal Stem Cells and Chondrocytes Biomaterials 2004, 25, 1901-1909 10.1016/j.biomaterials.2003.08.037
49. Ayala, R.; Zhang, C.; Yang, D.; Hwang, Y.; Aung, A.; Shroff, S. S.; Arce, F. T.; Lal, R.; Arya, G.; Varghese, S. Engineering the Cell-Material Interface for Controlling Stem Cell Adhesion, Migration, and Differentiation Biomaterials 2011, 32, 3700-3711 10.1016/j.biomaterials.2011.02.004
50. Gail, M. H.; Boone, C. W. Cell-Substrate Adhesivity: A Determinant of Cell Motility Exp. Cell Res. 1972, 70, 33-40 10.1016/0014-4827(72)90178-4
51. Li, J.; Han, D.; Zhao, Y.-P. Kinetic Behaviour of the Cells Touching Substrate: The Interfacial Stiffness Guides Cell Spreading Sci. Rep. 2014, 4, 1-10 10.1038/srep03910
52. Rowlands, A. S.; George, P. A.; Cooper-White, J. J. Directing Osteogenic and Myogenic Differentiation of Mscs: Interplay of Stiffness and Adhesive Ligand Presentation Am. J. Physiol.: Cell Physiol 2008, 295, C1037-1044 10.1152/ajpcell.67.2008
53. Kawahara, H.; Soeda, Y.; Niwa, K.; Takahashi, M.; Kawahara, D.; Araki, N. In Vitro Study on Bone Formation and Surface Topography from the Standpoint of Biomechanics J. Mater. Sci.: Mater. Med. 2004, 15, 1297-1307 10.1007/s10856-004-5738-0
54. Hao, L.; Yang, H.; Du, C.; Fu, X.; Zhao, N.; Xu, S.; Cui, F.; Mao, C.; Wang, Y. Directing the Fate of Human and Mouse Mesenchymal Stem Cells by Hydroxyl-Methyl Mixed Self-Assembled Monolayers with Varying Wettability J. Mater. Chem. B 2014, 2, 4794-4801 10.1039/C4TB00597J
55. Kern, S.; Eichler, H.; Stoeve, J.; Klüter, H.; Bieback, K. Comparative Analysis of Mesenchymal Stem Cells from Bone Marrow, Umbilical Cord Blood, or Adipose Tissue Stem Cells 2006, 24, 1294-1301 10.1634/stemcells.2005-0342
56. Kim, H. N.; Hong, Y.; Kim, M. S.; Kim, S. M.; Suh, K.-Y. Effect of Orientation and Density of Nanotopography in Dermal Wound Healing Biomaterials 2012, 33, 8782-8792 10.1016/j.biomaterials.2012.08.038
57. Yeung, T.; Georges, P. C.; Flanagan, L. A.; Marg, B.; Ortiz, M.; Funaki, M.; Zahir, N.; Ming, W.; Weaver, V.; Janmey, P. A. Effects of Substrate Stiffness on Cell Morphology, Cytoskeletal Structure, and Adhesion Cell Motil. Cytoskeleton 2005, 60, 24-34 10.1002/cm.20041
58. Lampin, M.; Warocquier-Clérout, R.; Legris, C.; Degrange, M.; Sigot-Luizard, M. F. Correlation between Substratum Roughness and Wettability, Cell Adhesion, and Cell Migration J. Biomed. Mater. Res. 1997, 36, 99-108 10.1002/(SICI)1097-4636(199707)36:1<99::AID-JBM12>3.0.CO;2-E
59. Lipski, A. M.; Pino, C. J.; Haselton, F. R.; Chen, I. W.; Shastri, V. P. The Effect of Silica Nanoparticle-Modified Surfaces on Cell Morphology, Cytoskeletal Organization and Function Biomaterials 2008, 29, 3836-3846 10.1016/j.biomaterials.2008.06.002
60. Kuddannaya, S.; Chuah, Y. J.; Lee, M. H. A.; Menon, N. V.; Kang, Y.; Zhang, Y. Surface Chemical Modification of Poly(Dimethylsiloxane) for the Enhanced Adhesion and Proliferation of Mesenchymal Stem Cells ACS Appl. Mater. Interfaces 2013, 5, 9777-9784 10.1021/am402903e
61. Yun, S. P.; Ryu, J. M.; Han, H. J. Involvement of Beta1-Integrin Via Pip Complex and Fak/Paxillin in Dexamethasone-Induced Human Mesenchymal Stem Cells Migration J. Cell. Physiol. 2011, 226, 683-692 10.1002/jcp.22383
62. Wein, F.; Pietsch, L.; Saffrich, R.; Wuchter, P.; Walenda, T.; Bork, S.; Horn, P.; Diehlmann, A.; Eckstein, V.; Ho, A. D.; Wagner, W. N-Cadherin Is Expressed on Human Hematopoietic Progenitor Cells and Mediates Interaction with Human Mesenchymal Stromal Cells Stem Cell Res. 2010, 4, 129-139 10.1016/j.scr.2009.12.004
63. Blindt, R.; Bosserhoff, A.-K.; Dammers, J.; Krott, N.; Demircan, L.; Hoffmann, R.; Hanrath, P.; Weber, C.; Vogt, F. Downregulation of N-Cadherin in the Neointima Stimulates Migration of Smooth Muscle Cells by Rhoa Deactivation Cardiovasc. Res. 2004, 62, 212-222 10.1016/j.cardiores.2004.01.004
64. DeLise, A. M.; Tuan, R. S. Alterations in the Spatiotemporal Expression Pattern and Function of N-Cadherin Inhibit Cellular Condensation and Chondrogenesis of Limb Mesenchymal Cells in Vitro J. Cell. Biochem. 2002, 87, 342-59 10.1002/jcb.10308
65. Gao, L.; McBeath, R.; Chen, C. S. Stem Cell Shape Regulates a Chondrogenic Versus Myogenic Fate through Rac1 and N-Cadherin Stem Cells 2010, 28, 564-572 10.1002/stem.308
66. Yano, H.; Mazaki, Y.; Kurokawa, K.; Hanks, S. K.; Matsuda, M.; Sabe, H. Roles Played by a Subset of Integrin Signaling Molecules in Cadherin-Based Cell-Cell Adhesion J. Cell Biol. 2004, 166, 283-295 10.1083/jcb.200312013