Mediation of osteogenic differentiation of human mesenchymal stem cells on titanium surfaces by a Wnt-integrin feedback loop

Biomaterials

Volumn 32, Issue 27, 2011, Pages 6399-6411

  Olivares Navarrete, Rene ^a   Hyzy, Sharon L ^a   Park, Jung Hwa ^b   Dunn, Ginger R ^a   Haithcock, David A ^a   Wasilewski, Christine E ^a   Boyan, Barbara D ^a   Schwartz, Zvi ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b Georgia Institute of Technology   (United States)

Author keywords

Cell signaling; Growth factors; Stem cell; Surface roughness; Titanium

Indexed keywords

CELL SIGNALING; EXOGENOUS FACTORS; FEED-BACK LOOP; GROWTH FACTORS; HUMAN MESENCHYMAL STEM CELLS; HUMAN MESENCHYMAL STEM CELLS (HMSCS); IMPLANT SURFACE; INTEGRINS; MESENCHYMAL CELLS; OSTEOBLAST DIFFERENTIATION; OSTEOBLAST PHENOTYPE; OSTEOBLASTIC DIFFERENTIATION; OSTEOGENESIS; OSTEOGENIC DIFFERENTIATION; PERI-IMPLANT BONES; SMOOTH SURFACE; TIME-DEPENDENT; TISSUE CULTURE POLYSTYRENES; TITANIUM SURFACES; WNT PATHWAY; WNT SIGNALING;

FEEDBACK; GLYCOPROTEINS; LIGANDS; OSTEOBLASTS; POLYSTYRENES; SIGNALING; SURFACE PROPERTIES; SURFACE ROUGHNESS; TISSUE; TISSUE CULTURE; TITANIUM;

STEM CELLS;

INTEGRIN; POLYSTYRENE; TITANIUM; VERY LATE ACTIVATION ANTIGEN 1; VERY LATE ACTIVATION ANTIGEN 2; VERY LATE ACTIVATION ANTIGEN 5; WNT PROTEIN; WNT3A PROTEIN; WNT5A PROTEIN;

ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CONTROLLED STUDY; CORRELATIONAL STUDY; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MESENCHYME CELL; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; SURFACE PROPERTY; TISSUE CULTURE;

CELL DIFFERENTIATION; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; INTEGRINS; MESENCHYMAL STEM CELLS; OSTEOGENESIS; SIGNAL TRANSDUCTION; SURFACE PROPERTIES; THERMODYNAMICS; TIME FACTORS; TITANIUM; WNT PROTEINS;

EID: 79960096790     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.05.036     Document Type: Article

References (50)

1. Protivinsky J., Appleford M., Strnad J., Helebrant A., Ong J.L. Effect of chemically modified titanium surfaces on protein adsorption and osteoblast precursor cell behavior. Int J Oral Maxillofac Implants 2007, 22:542-550.
2. Hao L., Lawrence J. Wettability modification and the subsequent manipulation of protein adsorption on a Ti6Al4V alloy by means of CO2 laser surface treatment. J Mater Sci Mater Med 2007, 18:807-817.
3. Cai K., Bossert J., Jandt K.D. Does the nanometre scale topography of titanium influence protein adsorption and cell proliferation?. Colloids Surf B Biointerfaces 2006, 49:136-144.
4. Zhao G., Raines A.L., Wieland M., Schwartz Z., Boyan B.D. Requirement for both micron- and submicron scale structure for synergistic responses of osteoblasts to substrate surface energy and topography. Biomaterials 2007, 28:2821-2829.
5. Yang Y., Tian J., Deng L., Ong J.L. Morphological behavior of osteoblast-like cells on surface-modified titanium in vitro. Biomaterials 2002, 23:1383-1389.
6. Raghavendra S., Wood M.C., Taylor T.D. Early wound healing around endosseous implants: a review of the literature. Int J Oral Maxillofac Implants 2005, 20:425-431.
7. Davies J.E. Understanding peri-implant endosseous healing. J Dent Educ 2003, 67:932-949.
8. Olivares-Navarrete R., Raz P., Zhao G., Chen J., Wieland M., Cochran D.L., et al. Integrin α2β1 plays a critical role in osteoblast response to micron-scale surface structure and surface energy of titanium substrates. Proc Natl Acad Sci U S A 2008, 105:15767-15772.
9. Wang L., Zhao G., Olivares-Navarrete R., Bell B.F., Wieland M., Cochran D.L., et al. Integrin β1 silencing in osteoblasts alters substrate-dependent responses to 1,25-dihydroxy vitamin D3. Biomaterials 2006, 27:3716-3725.
10. Le Guillou-Buffello D., Bareille R., Gindre M., Sewing A., Laugier P., Amedee J. Additive effect of RGD coating to functionalized titanium surfaces on human osteoprogenitor cell adhesion and spreading. Tissue Eng Part A 2008, 14:1445-1455.
11. Caplan A.I. Why are MSCs therapeutic? New data: new insight. J Pathol 2009, 217:318-324.
12. Caplan A.I., Dennis J.E. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006, 98:1076-1084.
13. Olivares-Navarrete R., Hyzy S.L., Hutton D.L., Erdman C.P., Wieland M., Boyan B.D., et al. Direct and indirect effects of microstructured titanium substrates on the induction of mesenchymal stem cell differentiation towards the osteoblast lineage. Biomaterials 2010, 31:2728-2735.
14. Watson P.A. Function follows form: generation of intracellular signals by cell deformation. FASEB J 1991, 5:2013-2019.
15. Bachle M., Kohal R.J. A systematic review of the influence of different titanium surfaces on proliferation, differentiation and protein synthesis of osteoblast-like MG63 cells. Clin Oral Implants Res 2004, 15:683-692.
16. Boyan B.D., Lossdorfer S., Wang L., Zhao G., Lohmann C.H., Cochran D.L., et al. Osteoblasts generate an osteogenic microenvironment when grown on surfaces with rough microtopographies. Eur Cell Mater 2003, 6:22-27.
17. Schwartz Z., Lohmann C.H., Sisk M., Cochran D.L., Sylvia V.L., Simpson J., et al. Local factor production by MG63 osteoblast-like cells in response to surface roughness and 1,25-(OH)2D3 is mediated via protein kinase C- and protein kinase A-dependent pathways. Biomaterials 2001, 22:731-741.
18. Olivares-Navarrete R., Hyzy S., Wieland M., Boyan B.D., Schwartz Z. The roles of Wnt signaling modulators Dickkopf-1 (Dkk1) and Dickkopf-2 (Dkk2) and cell maturation state in osteogenesis on microstructured titanium surfaces. Biomaterials 2010, 31:2015-2024.
19. Easwaran V., Lee S.H., Inge L., Guo L., Goldbeck C., Garrett E., et al. β-catenin regulates vascular endothelial growth factor expression in colon cancer. Cancer Res 2003, 63:3145-3153.
20. Day T.F., Guo X., Garrett-Beal L., Yang Y. Wnt/β-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev Cell 2005, 8:739-750.
21. Hu B., Nikolakopoulou A.M., Cohen-Cory S. BDNF stabilizes synapses and maintains the structural complexity of optic axons in vivo. Development 2005, 132:4285-4298.
22. Hill T.P., Spater D., Taketo M.M., Birchmeier W., Hartmann C. Canonical Wnt/β-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev Cell 2005, 8:727-738.
23. Rodda S.J., McMahon A.P. Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 2006, 133:3231-3244.
24. Takada I., Mihara M., Suzawa M., Ohtake F., Kobayashi S., Igarashi M., et al. A histone lysine methyltransferase activated by non-canonical Wnt signalling suppresses PPAR-gamma transactivation. Nat Cell Biol 2007, 9:1273-1285.
25. Baksh D., Boland G.M., Tuan R.S. Cross-talk between Wnt signaling pathways in human mesenchymal stem cells leads to functional antagonism during osteogenic differentiation. J Cell Biochem 2007, 101:1109-1124.
26. Baksh D., Tuan R.S. Canonical and non-canonical Wnts differentially affect the development potential of primary isolate of human bone marrow mesenchymal stem cells. J Cell Physiol 2007, 212:817-826.
27. Zhao G., Schwartz Z., Wieland M., Rupp F., Geis-Gerstorfer J., Cochran D.L., et al. High surface energy enhances cell response to titanium substrate microstructure. J Biomed Mater Res A 2005, 74:49-58.
28. Thomas T.R. Characterization of surface roughness. Precision Eng 1981, 3:97-104.
29. Udupa G., Singaperumal M., Sirohi R.S., Kothiyal M.P. Characterization of surface topography by confocal microscopy: II. The micro and macro surface irregularities. Meas Sci Technol 2000, 11:315-329.
30. Lossdorfer S., Schwartz Z., Wang L., Lohmann C.H., Turner J.D., Wieland M., et al. Microrough implant surface topographies increase osteogenesis by reducing osteoclast formation and activity. J Biomed Mater Res A 2004, 70:361-369.
31. Kieswetter K., Schwartz Z., Hummert T.W., Cochran D.L., Simpson J., Dean D.D., et al. Surface roughness modulates the local production of growth factors and cytokines by osteoblast-like MG-63 cells. J Biomed Mater Res 1996, 32:55-63.
32. Lausmaa J. Surface spectroscopic characterization of titanium implant materials. J Electron Spectros Relat Phenomena 1996, 81:343-361.
33. Baron R., Rawadi G. Targeting the Wnt/β-catenin pathway to regulate bone formation in the adult skeleton. Endocrinology 2007, 148:2635-2643.
34. Bodine P.V., Komm B.S. Wnt signaling and osteoblastogenesis. Rev Endocr Metab Disord 2006, 7:33-39.
35. Glass D.A., Karsenty G. In vivo analysis of Wnt signaling in bone. Endocrinology 2007, 148:2630-2634.
36. Milat F., Ng K.W. Is Wnt signalling the final common pathway leading to bone formation?. Mol Cell Endocrinol 2009, 310:52-62.
37. Olivares-Navarrete R., Hyzy S.L., Hutton D.L., Dunn G.R., Appert C., Boyan B.D., et al. Role of non-canonical Wnt signaling in osteoblast maturation on microstructured titanium surfaces. Acta Biomater 2011.
38. Shang Y.C., Wang S.H., Xiong F., Zhao C.P., Peng F.N., Feng S.W., et al. Wnt3a signaling promotes proliferation, myogenic differentiation, and migration of rat bone marrow mesenchymal stem cells. Acta Pharmacol Sin 2007, 28:1761-1774.
39. Tu X., Joeng K.S., Nakayama K.I., Nakayama K., Rajagopal J., Carroll T.J., et al. Noncanonical Wnt signaling through G protein-linked PKCdelta activation promotes bone formation. Dev Cell 2007, 12:113-127.
40. Boland G.M., Perkins G., Hall D.J., Tuan R.S. Wnt 3a promotes proliferation and suppresses osteogenic differentiation of adult human mesenchymal stem cells. J Cell Biochem 2004, 93:1210-1230.
41. Clifford R.L., Deacon K., Knox A.J. Novel regulation of vascular endothelial growth factor-A (VEGF-A) by transforming growth factor β1: requirement for Smads, β-catenin, and GSK3β. J Biol Chem 2008, 283:35337-35353.
42. Zhou T., Hu Y., Chen Y., Zhou K., Zhang B., Gao G., et al. The pathogenic role of the canonical Wnt pathway in age-related macular degeneration. Invest Ophthalmol Vis Sci 2009, 51:4371-4379.
43. Klapholz-Brown Z., Walmsley G.G., Nusse Y.M., Nusse R., Brown P.O. Transcriptional program induced by Wnt protein in human fibroblasts suggests mechanisms for cell cooperativity in defining tissue microenvironments. PLoS One 2007, 2:e945.
44. Bilkovski R., Schulte D.M., Oberhauser F., Gomolka M., Udelhoven M., Hettich M.M., et al. Role of WNT-5a in the determination of human mesenchymal stem cells into preadipocytes. J Biol Chem 2010, 285:6170-6178.
45. Guo J., Jin J., Cooper L.F. Dissection of sets of genes that control the character of wnt5a-deficient mouse calvarial cells. Bone 2008, 43:961-971.
46. Yamaguchi T.P., Bradley A., McMahon A.P., Jones S. A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 1999, 126:1211-1223.
47. Yang Y., Topol L., Lee H., Wu J. Wnt5a and Wnt5b exhibit distinct activities in coordinating chondrocyte proliferation and differentiation. Development 2003, 130:1003-1015.
48. Wall I., Donos N., Carlqvist K., Jones F., Brett P. Modified titanium surfaces promote accelerated osteogenic differentiation of mesenchymal stromal cells in vitro. Bone 2009, 45:17-26.
49. Safholm A., Tuomela J., Rosenkvist J., Dejmek J., Harkonen P., Andersson T. The Wnt-5a-derived hexapeptide Foxy-5 inhibits breast cancer metastasis in vivo by targeting cell motility. Clin Cancer Res 2008, 14:6556-6563.
50. Safholm A. A formylated hexapeptide ligand mimics the ability of Wnt-5a to impair migration of human breast epithelial cells. J Biol Chem 2005, 281:2740-2749.