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

Volumn 30, Issue 28, 2009, Pages 5094-5103

  Biggs, Manus J P ^a   Richards, R Geoff ^b   Gadegaard, Nikolaj ^a   Wilkinson, Chris D W ^a   Oreffo, Richard O C ^c   Dalby, Matthew J ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b AO RESEARCH INSTITUTE   (Switzerland)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

ERK MAPK; Focal adhesions; Mesenchymal stem cells; Nanotopography; Osteoblasts

Indexed keywords

ACTIN CYTOSKELETON; BONE RESORPTION; CELLULAR ADHESION; CELLULAR FUNCTION; ERK/MAPK; FOCAL ADHESIONS; HUMAN OSTEOBLAST; IN-VITRO; IN-VIVO; INTEGRIN; INTEGRINS; MESENCHYMAL STEM CELLS; NANO SCALE; NANOSCALE TOPOGRAPHY; NANOTOPOGRAPHY; ORTHOPAEDIC IMPLANTS; OSTEOGENESIS; PHYSIO-CHEMICAL; PLANAR SUBSTRATE; SIGNALLING CASCADES; SIGNALLING PATHWAYS; STEM CELL; TISSUE INTEGRATION; TISSUE LEVELS; TOPOGRAPHICAL MODIFICATIONS;

CELL ADHESION; CELL CULTURE; CELL MEMBRANES; CELLULAR ARRAYS; FOCUSING; LAWS AND LEGISLATION; NANOSTRUCTURED MATERIALS; OSTEOBLASTS;

ADHESION;

MITOGEN ACTIVATED PROTEIN KINASE; NANOMATERIAL;

ARTICLE; CELL ADHESION; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CELL SPREADING; CONTROLLED STUDY; ENZYME ACTIVATION; GENE EXPRESSION; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MICROARRAY ANALYSIS; MOLECULAR DYNAMICS; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STEM CELL; UPREGULATION;

CELL ADHESION; CELLS, CULTURED; HUMANS; MAP KINASE SIGNALING SYSTEM; MESENCHYMAL STEM CELLS; MICROTECHNOLOGY; NANOSTRUCTURES; NANOTECHNOLOGY; OSTEOBLASTS;

EID: 67849101009     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2009.05.049     Document Type: Article

References (51)

1. Smith L.L., Niziolek P.J., Haberstroh K.M., Nauman E.A., and Webster T.J. Decreased fibroblast and increased osteoblast adhesion on nanostructured NaOH-etched PLGA scaffolds. Int J Nanomedicine 2 (2007) 383-388
2. Dalby M.J., Gadegaard N., Tare R., Andar A., Riehle M.O., Herzyk P., et al. The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater 6 (2007) 997-1003
3. Dalby M.J., McCloy D., Robertson M., Agheli H., Sutherland D., Affrossman S., et al. Osteoprogenitor response to semi-ordered and random nanotopographies. Biomaterials 27 (2006) 2980-2987
4. Martines E., Seunarine K., Morgan H., Gadegaard N., Wilkinson C.D., and Riehle M.O. Superhydrophobicity and superhydrophilicity of regular nanopatterns. Nano Lett 5 (2005) 2097-2103
5. Martines E., Seunarine K., Morgan H., Gadegaard N., Wilkinson C.D., and Riehle M.O. Air-trapping on biocompatible nanopatterns. Langmuir 22 (2006) 11230-11233
6. Andersson A.S., Brink J., Lidberg U., and Sutherland D.S. Influence of systematically varied nanoscale topography on the morphology of epithelial cells. IEEE Trans Nanobioscience 2 (2003) 49-57
7. Liu S., Calderwood D.A., and Ginsberg M.H. Integrin cytoplasmic domain-binding proteins. J Cell Sci 113 Pt 20 (2000) 3563-3571
8. Schaller M.D., Borgman C.A., Cobb B.S., Vines R.R., Reynolds A.B., and Parsons J.T. pp125FAK a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc Natl Acad Sci U S A 89 (1992) 5192-5196
9. Ge C., Xiao G., Jiang D., and Franceschi R.T. Critical role of the extracellular signal-regulated kinase-MAPK pathway in osteoblast differentiation and skeletal development. J Cell Biol 176 (2007) 709-718
10. Jadlowiec J., Koch H., Zhang X., Campbell P.G., Seyedain M., and Sfeir C. Phosphophoryn regulates the gene expression and differentiation of NIH3T3, MC3T3-E1, and human mesenchymal stem cells via the integrin/MAPK signaling pathway. J Biol Chem 279 (2004) 53323-53330
11. Jaiswal R.K., Jaiswal N., Bruder S.P., Mbalaviele G., Marshak D.R., and Pittenger M.F. Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase. J Biol Chem 275 (2000) 9645-9652
12. Klees R.F., Salasznyk R.M., Kingsley K., Williams W.A., Boskey A., and Plopper G.E. Laminin-5 induces osteogenic gene expression in human mesenchymal stem cells through an ERK-dependent pathway. Mol Biol Cell 16 (2005) 881-890
13. Xiao G., Gopalakrishnan R., Jiang D., Reith E., Benson M.D., and Franceschi R.T. Bone morphogenetic proteins, extracellular matrix, and mitogen-activated protein kinase signaling pathways are required for osteoblast-specific gene expression and differentiation in MC3T3-E1 cells. J Bone Miner Res 17 (2002) 101-110
14. Takeuchi Y., Suzawa M., Kikuchi T., Nishida E., Fujita T., and Matsumoto T. Differentiation and transforming growth factor-beta receptor down-regulation by collagen-alpha2beta1 integrin interaction is mediated by focal adhesion kinase and its downstream signals in murine osteoblastic cells. J Biol Chem 272 (1997) 29309-29316
15. You J., Reilly G.C., Zhen X., Yellowley C.E., Chen Q., Donahue H.J., et al. Osteopontin gene regulation by oscillatory fluid flow via intracellular calcium mobilization and activation of mitogen-activated protein kinase in MC3T3-E1 osteoblasts. J Biol Chem 276 (2001) 13365-13371
16. Gadegaard N., Thoms S., Macintyre D.S., Mcghee K., Gallagher J., Casey B., et al. Arrays of nano-dots for cellular engineering. Microelectron Eng 67-68 (2003) 126-168
17. Gadegaard N., Mosler M., and Larsen M.B. Biomimetic polymer nanostructures by injection molding. Macromol Mater Eng 288 (2003) 76-83
18. Biggs M.J., Richards R.G., McFarlane S., Wilkinson C.D., Oreffo R.O., and 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 5 (2008) 1231-1242
19. Cohen D.M., Chen H., Johnson R.P., Choudhury B., and Craig S.W. Two distinct head-tail interfaces cooperate to suppress activation of vinculin by talin. J Biol Chem 280 (2005) 17109-17117
20. Howard D., Partridge K., Yang X., Clarke N.M., Okubo Y., Bessho K., et al. Immunoselection and adenoviral genetic modulation of human osteoprogenitors: in vivo bone formation on PLA scaffold. Biochem Biophys Res Commun 299 (2002) 208-215
21. Mirmalek-Sani S.H., Tare R.S., Morgan S.M., Roach H.I., Wilson D.I., Hanley N.A., et al. Characterization and multipotentiality of human fetal femur-derived cells: implications for skeletal tissue regeneration. Stem Cells 24 (2006) 1042-1053
22. Gronthos S., and Zannettino A.C. A method to isolate and purify human bone marrow stromal stem cells. Methods Mol Biol 449 (2008) 45-57
23. Dalby M.J., Riehle M.O., Yarwood S.J., Wilkinson C.D., and Curtis A.S. Nucleus alignment and cell signaling in fibroblasts: response to a micro-grooved topography. Exp Cell Res 284 (2003) 274-282
24. Clark E.A., and Brugge J.S. Integrins and signal transduction pathways: the road taken. Science 268 (1995) 233-239
25. Kundu A.K., Khatiwala C.B., and Putnam A.J. Extracellular matrix remodeling, integrin expression, and downstream signaling pathways influence the osteogenic differentiation of mesenchymal stem cells on poly(lactide-co-glycolide) substrates. Tissue Eng Part A 15 (2009) 273-282
26. Reusch H.P., Chan G., Ives H.E., and Nemenoff R.A. Activation of JNK/SAPK and ERK by mechanical strain in vascular smooth muscle cells depends on extracellular matrix composition. Biochem Biophys Res Commun 237 (1997) 239-244
27. Kapur S., Baylink D.J., and Lau K.H. Fluid flow shear stress stimulates human osteoblast proliferation and differentiation through multiple interacting and competing signal transduction pathways. Bone 32 (2003) 241-251
28. Yee K.L., Weaver V.M., and Hammer D.A. Integrin-mediated signalling through the MAP-kinase pathway. IET Syst Biol 2 (2008) 8-15
29. Salasznyk R.M., Klees R.F., Boskey A., and Plopper G.E. Activation of FAK is necessary for the osteogenic differentiation of human mesenchymal stem cells on laminin-5. J Cell Biochem 100 (2007) 499-514
30. Klemke R.L., Cai S., Giannini A.L., Gallagher P.J., de Lanerolle P., and Cheresh D.A. Regulation of cell motility by mitogen-activated protein kinase. J Cell Biol 137 (1997) 481-492
31. Liu Z.X., Yu C.F., Nickel C., Thomas S., and Cantley L.G. Hepatocyte growth factor induces ERK-dependent paxillin phosphorylation and regulates paxillin-focal adhesion kinase association. J Biol Chem 277 (2002) 10452-10458
32. Cheng C., Kong X., Wang H., Gan H., Hao Y., Zou W., et al. Trihydrophobin 1 interacts with PAK1 and regulates ERK/MAPK activation and cell migration. J Biol Chem 284 (2009) 8786-8796
33. Kokubu E, Hamilton DW, Inoue T, Brunette DM. Modulation of human gingival fibroblast adhesion, morphology, tyrosine phosphorylation, and ERK 1/2 localization on polished, grooved and SLA substratum topographies. J Biomed Mater Res A, in press.
34. Hamilton D.W., and Brunette D.M. The effect of substratum topography on osteoblast adhesion mediated signal transduction and phosphorylation. Biomaterials 28 (2007) 1806-1819
35. Zhang Y., Hassan M.Q., Li Z.Y., Stein J.L., Lian J.B., van Wijnen A.J., et al. Intricate gene regulatory networks of helix-loop-helix (HLH) proteins support regulation of bone-tissue related genes during osteoblast differentiation. J Cell Biochem 105 (2008) 487-496
36. Tanaka N., and Fukuzawa M. MYCN downregulates integrin alpha1 to promote invasion of human neuroblastoma cells. Int J Oncol 33 (2008) 815-821
37. Raouf A., and Seth A. Ets transcription factors and targets in osteogenesis. Oncogene 19 (2000) 6455-6463
38. Turhani D., Watzinger E., Weissenbock M., Yerit K., Cvikl B., Ewers R., et al. Expression pattern of the chromosome 21 transcription factor Ets2 in cell-seeded three-dimensional bone constructs. J Biomed Mater Res A 73 (2005) 445-455
39. Qi M.C., Hu J., Zou S.J., Chen H.Q., Zhou H.X., and Han L.C. Mechanical strain induces osteogenic differentiation: Cbfa1 and Ets-1 expression in stretched rat mesenchymal stem cells. Int J Oral Maxillofac Surg 37 (2008) 453-458
40. Muruganandan S., Roman A.A., and Sinal C.J. Adipocyte differentiation of bone marrow-derived mesenchymal stem cells: cross talk with the osteoblastogenic program. Cell Mol Life Sci 66 (2009) 236-253
41. Tontonoz P., Hu E., Graves R.A., Budavari A.I., and Spiegelman B.M. mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Dev 8 (1994) 1224-1234
42. Pan Z., Yang J., Guo C., Shi D., Shen D., Zheng Q., et al. Effects of hindlimb unloading on ex vivo growth and osteogenic/adipogenic potentials of bone marrow-derived mesenchymal stem cells in rats. Stem Cells Dev 17 (2008) 795-804
43. McBeath R., Pirone D.M., Nelson C.M., Bhadriraju K., and Chen C.S. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6 (2004) 483-495
44. Itoh S., Udagawa N., Takahashi N., Yoshitake F., Narita H., Ebisu S., et al. A critical role for interleukin-6 family-mediated Stat3 activation in osteoblast differentiation and bone formation. Bone 39 (2006) 505-512
45. Kim S., Koga T., Isobe M., Kern B.E., Yokochi T., Chin Y.E., et al. Stat1 functions as a cytoplasmic attenuator of Runx2 in the transcriptional program of osteoblast differentiation. Genes Dev 17 (2003) 1979-1991
46. Xiao L., Naganawa T., Obugunde E., Gronowicz G., Ornitz D.M., Coffin J.D., et al. Stat1 controls postnatal bone formation by regulating fibroblast growth factor signaling in osteoblasts. J Biol Chem 279 (2004) 27743-27752
47. Lee C.H., Shin H.J., Cho I.H., Kang Y.M., Kim I.A., Park K.D., et al. Nanofiber alignment and direction of mechanical strain affect the ECM production of human ACL fibroblast. Biomaterials 26 (2005) 1261-1270
48. Manwaring M.E., Walsh J.F., and Tresco P.A. Contact guidance induced organization of extracellular matrix. Biomaterials 25 (2004) 3631-3638
49. Wang J.H., Jia F., Gilbert T.W., and Woo S.L. Cell orientation determines the alignment of cell-produced collagenous matrix. J Biomech 36 (2003) 97-102
50. Franceschi R.T., Ge C., Xiao G., Roca H., and Jiang D. Transcriptional regulation of osteoblasts. Cells Tissues Organs 189 (2009) 144-152
51. Leucht P., Kim J.B., Currey J.A., Brunski J., and Helms J.A. FAK-mediated mechanotransduction in skeletal regeneration. PLoS ONE 2 (2007) e390