Osteogenesis of mesenchymal stem cells by nanoscale mechanotransduction

ACS Nano

Volumn 7, Issue 3, 2013, Pages 2758-2767

  Nikukar, Habib ^a,c   Reid, Stuart ^b   Tsimbouri, P Monica ^a   Riehle, Mathis O ^a   Curtis, Adam S G ^a   Dalby, Matthew J ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF THE WEST OF SCOTLAND   (United Kingdom)

^c SHAHID SADOUGHI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

mechanotransduction; mesenchymal stem cells; nanoscale; osteogenesis

Indexed keywords

HUMAN MESENCHYMAL STEM CELLS; MECHANOTRANSDUCTION; MESENCHYMAL STEM CELL; NANO SCALE; OSTEOBLASTIC DIFFERENTIATION; OSTEOGENESIS; PHARMACOLOGICAL INHIBITION; STIMULATION PROTOCOLS;

CELL CULTURE; STEM CELLS;

NANOTECHNOLOGY;

RHO KINASE;

ARTICLE; BONE DEVELOPMENT; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; EQUIPMENT; HUMAN; MECHANICAL STRESS; MECHANOTRANSDUCTION; MESENCHYMAL STROMA CELL; METABOLISM; NANOTECHNOLOGY; OSTEOBLAST; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSDUCER;

CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MESENCHYMAL STROMAL CELLS; NANOTECHNOLOGY; OSTEOBLASTS; OSTEOGENESIS; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION; STRESS, MECHANICAL; TRANSDUCERS;

EID: 84875662025     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn400202j     Document Type: Article

References (72)

1. Dalby, M. J.; Yarwood, S. J.; Riehle, M. O.; Johnstone, H. J. H.; Affrossman, S.; Curtis, A. S. G. Increasing Fibroblast Response to Materials Using Nanotopography: Morphological and Genetic Measurements of Cell Response to 13-nm-High Polymer Demixed Islands Exp. Cell Res. 2002, 276, 1-9
2. Dalby, M. J.; Riehle, M. O.; Johnstone, H.; Affrossman, S.; Curtis, A. S. G. In Vitro Reaction of Endothelial Cells to Polymer Demixed Nanotopography Biomaterials 2002, 23, 2945-2954
3. Andersson, A. S.; Backhed, F.; von Euler, A.; Richter-Dahlfors, A.; Sutherland, D.; Kasemo, B. Nanoscale Features Influence Epithelial Cell Morphology and Cytokine Production Biomaterials 2003, 24, 3427-3436
4. Yim, E. K.; Reano, R. M.; Pang, S. W.; Yee, A. F.; Chen, C. S.; Leong, K. W. Nanopattern-Induced Changes in Morphology and Motility of Smooth Muscle Cells Biomaterials 2005, 26, 5405-5413
5. Child, H. W.; Del Pino, P. A.; De La Fuente, J. M.; Hursthouse, A. S.; Stirling, D.; Mullen, M.; McPhee, G. M.; Nixon, C.; Jayawarna, V.; Berry, C. C. Working Together: The Combined Application of a Magnetic Field and Penetratin for the Delivery of Magnetic Nanoparticles to Cells in 3D ACS Nano 2011, 5, 7910-7919
6. Conde, J.; Ambrosone, A.; Sanz, V.; Hernandez, Y.; Marchesano, V.; Tian, F.; Child, H.; Berry, C. C.; Ibarra, M. R.; Baptista, P. V. et al. Design of Multifunctional Gold Nanoparticles for In Vitro and In Vivo Gene Silencing ACS Nano 2012, 6, 8316-8324
7. Yim, E. K.; Pang, S. W.; Leong, K. W. Synthetic Nanostructures Inducing Differentiation of Human Mesenchymal Stem Cells into Neuronal Lineage Exp. Cell Res. 2007, 313, 1820-1829
8. 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
9. Oh, S.; Brammer, K. S.; Li, Y. S.; Teng, D.; Engler, A. J.; Chien, S.; Jin, S. Stem Cell Fate Dictated Solely by Altered Nanotube Dimension Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 2130-2135
10. Dalby, M. J.; Gadegaard, N.; Tare, R.; Andar, A.; Riehle, M. O.; Herzyk, P.; Wilkinson, C. D. W.; Oreffo, R. O. C. The Control of Human Mesenchymal Cell Differentiation Using Nanoscale Symmetry and Disorder Nat. Mater. 2007, 6, 997-1003
11. McMurray, R. J.; Gadegaard, N.; Tsimbouri, P. M.; Burgess, K. V.; McNamara, L. E.; Tare, R.; Murawski, K.; Kingham, E.; Oreffo, R. O.; Dalby, M. J. Nanoscale Surfaces for the Long-Term Maintenance of Mesenchymal Stem Cell Phenotype and Multipotency Nat. Mater. 2011, 10, 637-644
12. Tare, R. S.; Babister, J. C.; Kanczler, J.; Oreffo, R. O. Skeletal Stem Cells: Phenotype, Biology and Environmental Niches Informing Tissue Regeneration Mol. Cell. Endocrinol. 2008, 288, 11-21
13. Huang, G. T.; Gronthos, S.; Shi, S. Mesenchymal Stem Cells Derived from Dental Tissues vs. Those from Other Sources: Their Biology and Role in Regenerative Medicine J. Dent. Res. 2009, 88, 792-806
14. Schaffler, A.; Buchler, C. Concise Review: Adipose Tissue-Derived Stromal Cells-Basic and Clinical Implications for Novel Cell-Based Therapies Stem Cells 2007, 25, 818-827
15. Longo, U. G.; Loppini, M.; Berton, A.; La Verde, L.; Khan, W. S.; Denaro, V. Stem Cells from Umbilical Cord and Placenta for Musculoskeletal Tissue Engineering Curr. Stem Cell Res. Ther. 2012, 7, 272-281
16. Vater, C.; Kasten, P.; Stiehler, M. Culture Media for the Differentiation of Mesenchymal Stromal Cells Acta Biomater. 2011, 7, 463-477
17. Liu, J.; Song, L.; Jiang, C.; Liu, Y.; George, J.; Ye, H.; Cui, Z. Electrophysiological Properties and Synaptic Function of Mesenchymal Stem Cells During Neurogenic Differentiation: A Mini-Review Int. J. Artif. Organs 2012, 35, 323-337
18. Tsimbouri, P. M.; McMurray, R. J.; Burgess, K. V.; Alakpa, E. V.; Reynolds, P. M.; Murawski, K.; Kingham, E.; Oreffo, R. O.; Gadegaard, N.; Dalby, M. J. Using Nanotopography and Metabolomics To Identify Biochemical Effectors of Multipotency ACS Nano 2012, 6, 10239-10249
19. Biggs, M. J. P.; Richards, R. G.; Gadegaard, N.; Wilkinson, C. D. W.; Oreffo, R. O. C.; Dalby, M. J. The Use of Nanoscale Topography To Modulate the Dynamics of Adhesion Formation in Primary Osteoblasts and Erk/Mapk Signalling in Stro-1+Enriched Skeletal Stem Cells Biomaterials 2009, 30, 5094-5103
20. Engler, A. J.; Sen, S.; Sweeney, H. L.; Discher, D. E. Matrix Elasticity Directs Stem Cell Lineage Specification Cell 2006, 126, 677-689
21. McBeath, R.; Pirone, D. M.; Nelson, C. M.; Bhadriraju, K.; Chen, C. S. Cell Shape, Cytoskeletal Tension, and RhoA Regulate Stem Cell Lineage Commitment Dev. Cell 2004, 6, 483-495
22. 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
23. Kilian, K. A.; Bugarija, B.; Lahn, B. T.; Mrksich, M. Geometric Cues for Directing the Differentiation of Mesenchymal Stem Cells Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 4872-4877
24. Sawada, Y.; Sheetz, M. P. Force Transduction by Triton Cytoskeletons J. Cell Biol. 2002, 156, 609-615
25. Galbraith, C. G.; Yamada, K. M.; Sheetz, M. P. The Relationship between Force and Focal Complex Development J. Cell Biol. 2002, 159, 695-705
26. Vogel, V.; Sheetz, M. Local Force and Geometry Sensing Regulate Cell Functions Nat. Rev. Mol. Cell. Biol. 2006, 7, 265-275
27. Sawada, Y.; Tamada, M.; Dubin-Thaler, B. J.; Cherniavskaya, O.; Sakai, R.; Tanaka, S.; Sheetz, M. P. Force Sensing by Mechanical Extension of the Src Family Kinase Substrate P130cas Cell 2006, 127, 1015-1026
28. del Rio, A.; Perez-Jimenez, R.; Liu, R.; Roca-Cusachs, P.; Fernandez, J. M.; Sheetz, M. P. Stretching Single Talin Rod Molecules Activates Vinculin Binding Science 2009, 323, 638-641
29. Biggs, M. J. P.; Richards, R. G.; McFarlane, S.; Wilkinson, C. D. W.; Oreffo, R. O. C.; Dalby, M. J. Adhesion Formation of Primary Human Osteoblasts and the Functional Response of Mesenchymal Stem Cells to 330 nm Deep Microgrooves J. R. Soc. Interface 2008, 5, 1231-1242
30. Biggs, M. J. P.; Richards, R. G.; Gadegaard, N.; McMurray, R. J.; Affrossman, S.; Wilkinson, C. D. W.; Oreffo, R. O. C.; Dalby, M. J. Interactions with Nanoscale Topography: Adhesion Quantification and Signal Transduction in Cells of Osteogenic and Multipotent Lineage J. Biomed. Mater. Res., Part A 2009, 91A, 195-208
31. Pierres, A.; Benoliel, A. M.; Touchard, D.; Bongrand, P. How Cells Tiptoe on Adhesive Surfaces before Sticking Biophys. J. 2008, 94, 4114-4122
32. Guilak, F.; Cohen, D. M.; Estes, B. T.; Gimble, J. M.; Liedtke, W.; Chen, C. S. Control of Stem Cell Fate by Physical Interactions with the Extracellular Matrix Cell Stem Cell 2009, 5, 17-26
33. Park, S. H.; Sim, W. Y.; Min, B. H.; Yang, S. S.; Khademhosseini, A.; Kaplan, D. L. Chip-Based Comparison of the Osteogenesis of Human Bone Marrow- and Adipose Tissue-Derived Mesenchymal Stem Cells under Mechanical Stimulation PLoS ONE 2012, 7, e46689
34. Shi, Y.; Fu, Y.; Tong, W.; Geng, Y.; Lui, P. P.; Tang, T.; Zhang, X.; Dai, K. Uniaxial Mechanical Tension Promoted Osteogenic Differentiation of Rat Tendon-Derived Stem Cells (Rtdscs) via the Wnt5a-RhoA Pathway J. Cell. Biochem. 2012, 113, 3133-3142
35. Pingguan-Murphy, B.; Lee, D. A.; Bader, D. L.; Knight, M. M. Activation of Chondrocytes Calcium Signalling by Dynamic Compression Is Independent of Number of Cycles Arch. Biochem. Biophys. 2005, 444, 45-51
36. Knight, M. M.; van de Breevaart Bravenboer, J.; Lee, D. A.; van Osch, G. J.; Weinans, H.; Bader, D. L. Cell and Nucleus Deformation in Compressed Chondrocyte-Alginate Constructs: Temporal Changes and Calculation of Cell Modulus Biochim. Biophys. Acta 2002, 1570, 1-8
37. Cheema, U.; Chuo, C.-P.; Sarathchandra, P.; Nazhat, S. N.; Brown, R. A. Engineering Functional Collagen Scaffolds: Cyclical Loading Increases Material Strength and Fibril Aggregation Adv. Funct. Mater. 2007, 17, 2426-2431
38. Eastwood, M.; McGrouther, D. A.; Brown, R. A. Fibroblast Responses to Mechanical Forces Proc. Inst. Mech. Eng., Part H 1998, 212, 85-92
39. Kanaka, T. S.; Kumar, M. M. Neural Stimulation for Spinal Spasticity Paraplegia 1990, 28, 399-405
40. Chen, I. I.; Saha, S. Analysis of the Current Distribution in Bone Produced by Pulsed Electro-Magnetic Field Stimulation of Bone Biomater. Artif. Cells Artif. Organs 1987, 15, 737-744
41. Pompeiano, O.; Wand, P.; Sontag, K. H. The Sensitivity of Renshaw Cells to Velocity of Sinusoidal Stretches of the Triceps Surae Muscle Arch. Ital. Biol. 1975, 113, 280-294
42. Ingber, D. E. Tensegrity and Mechanotransduction J. Bodyw. Mov. Ther. 2008, 12, 198-200
43. Ward, D. F., Jr.; Salasznyk, R. M.; Klees, R. F.; Backiel, J.; Agius, P.; Bennett, K.; Boskey, A.; Plopper, G. E. Mechanical Strain Enhances Extracellular Matrix-Induced Gene Focusing and Promotes Osteogenic Differentiation of Human Mesenchymal Stem Cells through an Extracellular-Related Kinase-Dependent Pathway Stem Cells Dev. 2007, 16, 467-480
44. Hamilton, D. W.; Brunette, D. M. The Effect of Substratum Topography on Osteoblast Adhesion Mediated Signal Transduction and Phosphorylation Biomaterials 2007, 28, 1806-1819
45. Ge, C.; Xiao, G.; Jiang, D.; Franceschi, R. T. Critical Role of the Extracellular Signal-Regulated Kinase-Mapk Pathway in Osteoblast Differentiation and Skeletal Development J. Cell Biol. 2007, 176, 709-718
46. Xiao, G.; Jiang, D.; Gopalakrishnan, R.; Franceschi, R. T. Fibroblast Growth Factor 2 Induction of the Osteocalcin Gene Requires Mapk Activity and Phosphorylation of the Osteoblast Transcription Factor, Cbfa1/Runx2 J. Biol. Chem. 2002, 277, 36181-36187
47. Willis, D. M.; Loewy, A. P.; Charlton-Kachigian, N.; Shao, J.-S.; Ornitz, D. M.; Towler, D. A. Regulation of Osteocalcin Gene Expression by a Novel Ku Antigen Transcription Factor Complex J. Biol. Chem. 2002, 277, 37280-37291
48. Stein, G. S.; Lian, J. B. Molecular Mechanisms Mediating Proliferation/Differentiation Interrelationships during Progressive Development of the Osteoblast Phenotype Endocr. Rev. 1993, 14, 424-442
49. Huang, Y. F.; Lin, J. J.; Lin, C. H.; Su, Y.; Hung, S. C. C-Jun N-Terminal Kinase 1 Negatively Regulates Osteoblastic Differentiation Induced by Bmp2 via Phosphorylation of Runx2 at Ser104 J. Bone Miner. Res. 2012, 27, 1093-1105
50. Jang, W. G.; Kim, E. J.; Kim, D. K.; Ryoo, H. M.; Lee, K. B.; Kim, S. H.; Choi, H. S.; Koh, J. T. Bmp2 Protein Regulates Osteocalcin Expression via Runx2-Mediated Atf6 Gene Transcription J. Biol. Chem. 2012, 287, 905-915
51. Kim, W. K.; Meliton, V.; Bourquard, N.; Hahn, T. J.; Parhami, F. Hedgehog Signaling and Osteogenic Differentiation in Multipotent Bone Marrow Stromal Cells Are Inhibited by Oxidative Stress J. Cell. Biochem. 2010, 111, 1199-1209
52. Dai, Z.; Li, Y.; Quarles, L. D.; Song, T.; Pan, W.; Zhou, H.; Xiao, Z. Resveratrol Enhances Proliferation and Osteoblastic Differentiation in Human Mesenchymal Stem Cells via ER-Dependent ERK1/2 Activation Phytomedicine 2007, 14, 806-814
53. James, A. W.; Leucht, P.; Levi, B.; Carre, A. L.; Xu, Y.; Helms, J. A.; Longaker, M. T. Sonic Hedgehog Influences the Balance of Osteogenesis and Adipogenesis in Mouse Adipose-Derived Stromal Cells Tissue Eng., Part A 2010, 16, 2605-2616
54. Day, T. F.; Yang, Y. Wnt and Hedgehog Signaling Pathways in Bone Development J. Bone Joint Surg. Am. 2008, 90 Suppl 1, 19-24
55. Pierres, A.; Monnet-Corti, V.; Benoliel, A. M.; Bongrand, P. Do Membrane Undulations Help Cells Probe the World? Trends Cell. Biol. 2009, 19, 428-433
56. Evans, E. Kinetics of Granulocyte Phagocytosis: Rate Limited by Cytoplasmic Viscosity and Constrained by Cell Size Cell Motil. Cytoskeleton 1989, 14, 544-551
57. Shamri, R.; Grabovsky, V.; Gauguet, J. M.; Feigelson, S.; Manevich, E.; Kolanus, W.; Robinson, M. K.; Staunton, D. E.; von Andrian, U. H.; Alon, R. Lymphocyte Arrest Requires Instantaneous Induction of an Extended Lfa-1 Conformation Mediated by Endothelium-Bound Chemokines Nat. Immunol. 2005, 6, 497-506
58. Rappaz, B.; Barbul, A.; Hoffmann, A.; Boss, D.; Korenstein, R.; Depeursinge, C.; Magistretti, P. J.; Marquet, P. Spatial Analysis of Erythrocyte Membrane Fluctuations by Digital Holographic Microscopy Blood Cells, Mol., Dis. 2009, 42, 228-232
59. Evans, J.; Gratzer, W.; Mohandas, N.; Parker, K.; Sleep, J. Fluctuations of the Red Blood Cell Membrane: Relation to Mechanical Properties and Lack of ATP Dependence Biophys. J. 2008, 94, 4134-4144
60. Krol, A.; Grinfeldt, M. G.; Levin, S. V.; Smilgavichus, A. D. Local Mechanical Oscillations of the Cell Surface within the Range 0.2-30 Hz Eur. Biophys. J. 1990, 19, 93-99
61. Pelling, A. E.; Veraitch, F. S.; Pui-Kei Chu, C.; Nicholls, B. M.; Hemsley, A. L.; Mason, C.; Horton, M. A. Mapping Correlated Membrane Pulsations and Fluctuations in Human Cells J. Mol. Recognit. 2007, 20, 467-475
62. Szabo, B.; Selmeczi, D.; Kornyei, Z.; Madarasz, E.; Rozlosnik, N. Atomic Force Microscopy of Height Fluctuations of Fibroblast Cells Phys. Rev. E 2002, 65, 041910
63. Reinish, G. B.; Nowick, A. S. Piezoelectric Properties of Bone as Functions of Moisture Content Nature 1975, 253, 626-627
64. Finkelstein, E. I.; Chao, P. H.; Hung, C. T.; Bulinski, J. C. Electric Field-Induced Polarization of Charged Cell Surface Proteins Does Not Determine the Direction of Galvanotaxis Cell Motil. Cytoskeleton 2007, 64, 833-846
65. Mycielska, M. E.; Djamgoz, M. B. Cellular Mechanisms of Direct-Current Electric Field Effects: Galvanotaxis and Metastatic Disease J. Cell. Sci. 2004, 117, 1631-1639
66. Goldstein, C.; Sprague, S.; Petrisor, B. A. Electrical Stimulation for Fracture Healing: Current Evidence J. Orthop. Trauma 2010, 24 Suppl 1, S62-S65
67. Noris-Suarez, K.; Lira-Olivares, J.; Ferreira, A. M.; Feijoo, J. L.; Suarez, N.; Hernandez, M. C.; Barrios, E. In Vitro Deposition of Hydroxyapatite on Cortical Bone Collagen Stimulated by Deformation-Induced Piezoelectricity Biomacromolecules 2007, 8, 941-948
68. Fernandez, J. R.; Garcia-Aznar, J. M.; Martinez, R. Piezoelectricity Could Predict Sites of Formation/Resorption in Bone Remodelling and Modelling J. Theor. Biol. 2012, 292, 86-92
69. Wysocki, A.; Butler, M.; Shamliyan, T.; Kane, R. L. Whole-Body Vibration Therapy for Osteoporosis: State of the Science Ann. Intern. Med. 2011, 155, 680-686 W206-613
70. Alizadeh-Meghrazi, M.; Masani, K.; Popovic, M. R.; Craven, B. C. Whole-Body Vibration During Passive Standing in Individuals with Spinal Cord Injury: Effects of Plate Choice, Frequency, Amplitude, and Subject's Posture on Vibration Propagation PM&R 2012, 4, 963-975
71. Tamma, R.; dell'Endice, S.; Notarnicola, A.; Moretti, L.; Patella, S.; Patella, V.; Zallone, A.; Moretti, B. Extracorporeal Shock Waves Stimulate Osteoblast Activities Ultrasound Med. Biol. 2009, 35, 2093-2100
72. Breitling, R.; Armengaud, P.; Amtmann, A.; Herzyk, P. Rank Products: A Simple, Yet Powerful, New Method To Detect Differentially Regulated Genes in Replicated Microarray Experiments FEBS Lett. 2004, 573, 83-92