Pro-osteogenic topographical cues promote early activation of osteoprogenitor differentiation via enhanced TGFβ, Wnt, and Notch signaling

Clinical Oral Implants Research

Volumn 25, Issue 4, 2014, Pages 475-486

  Chakravorty, Nishant ^a   Hamlet, Stephen ^b   Jaiprakash, Anjali ^a   Crawford, Ross ^a,c   Oloyede, Adekunle ^a   Alfarsi, Mohammed ^b,d   Xiao, Yin ^a   Ivanovski, Saso ^b  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

^c THE PRINCE CHARLES HOSPITAL   (Australia)

^d KING KHALID UNIVERSITY   (Saudi Arabia)

Author keywords

Cell signaling; Osteoprogenitor differentiation; Titanium surface modification; Topography

Indexed keywords

BONE MORPHOGENETIC PROTEIN; GDF15 PROTEIN, HUMAN; GROWTH DIFFERENTIATION FACTOR 15; NOTCH RECEPTOR; OSTEOCALCIN; SIALOGLYCOPROTEIN; TITANIUM; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN;

ASSOCIATION; ATOMIC FORCE MICROSCOPY; BONE DEVELOPMENT; CELL CULTURE; CELL DIFFERENTIATION; GENE EXPRESSION PROFILING; HUMAN; IN VITRO STUDY; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION; SURFACE PROPERTY;

BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELLS, CULTURED; CUES; GENE EXPRESSION PROFILING; GROWTH DIFFERENTIATION FACTOR 15; HUMANS; IN VITRO TECHNIQUES; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON, SCANNING; OSTEOCALCIN; OSTEOGENESIS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, NOTCH; SIALOGLYCOPROTEINS; SIGNAL TRANSDUCTION; SURFACE PROPERTIES; TITANIUM; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEINS;

EID: 84897645649     PISSN: 09057161     EISSN: 16000501     Source Type: Journal    
DOI: 10.1111/clr.12178     Document Type: Article

References (57)

1. Bagno, A., Piovan, A., Dettin, M., Chiarion, A., Brun, P., Gambaretto, R., Fontana, G., Di Bello, C., Palù, G. & Castagliuolo, I. (2007) Human osteoblast-like cell adhesion on titanium substrates covalently functionalized with synthetic peptides. Bone 40: 693-699.
2. Bornstein, M.M., Valderrama, P., Jones, A.A., Wilson, T.G., Seibl, R. & Cochran, D.L. (2008) Bone apposition around two different sandblasted and acid-etched titanium implant surfaces: a histomorphometric study in canine mandibles. Clinical Oral Implants Research 19: 233-241.
3. Bosshardt, D.D., Salvi, G.E., Huynh-Ba, G., Ivanovski, S., Donos, N. & Lang, N.P. (2011) The role of bone debris in early healing adjacent to hydrophilic and hydrophobic implant surfaces in man. Clinical Oral Implants Research 22: 357-364.
4. Brett, P.M., Harle, J., Salih, V., Mihoc, R., Olsen, I., Jones, F.H. & Tonetti, M. (2004) Roughness response genes in osteoblasts. Bone 35: 124-133.
5. Buser, D., Broggini, N., Wieland, M., Schenk, R.K., Denzer, A.J., Cochran, D.L., Hoffmann, B., Lussi, A. & Steinemann, S.G. (2004) Enhanced bone apposition to a chemically modified SLA titanium surface. Journal of Dental Research 83: 529-533.
6. Buser, D., Nydegger, T., Oxland, T., Cochran, D.L., Schenk, R.K., Hirt, H.P., Snetivy, D. & Nolte, L.P. (1999) Interface shear strength of titanium implants with a sandblasted and acid-etched surface: a biomechanical study in the maxilla of miniature pigs. Journal of Biomedical Materials Research 45: 75-83.
7. Buser, D., Schenk, R.K., Steinemann, S., Fiorellini, J.P., Fox, C.H. & Stich, H. (1991) Influence of surface characteristics on bone integration of titanium implants. A histomorphometric study in miniature pigs. Journal of Biomedical Materials Research 25: 889-902.
8. Chakravorty, N., Ivanovski, S., Prasadam, I., Crawford, R., Oloyede, A. & Xiao, Y. (2012) The microRNA expression signature on modified titanium implant surfaces influences genetic mechanisms leading to osteogenic differentiation. Acta Biomaterialia 8: 3516-3523.
9. Crabtree, G.R. & Olson, E.N. (2002) NFAT signaling: choreographing the social lives of cells. Cell 109(Suppl.): S67-S79.
10. Donos, N., Hamlet, S., Lang, N.P., Salvi, G.E., Huynh-Ba, G., Bosshardt, D.D. & Ivanovski, S. (2011a) Gene expression profile of osseointegration of a hydrophilic compared with a hydrophobic microrough implant surface. Clinical Oral Implants Research 22: 365-372.
11. Donos, N., Retzepi, M., Wall, I., Hamlet, S. & Ivanovski, S. (2011b) In vivo gene expression profile of guided bone regeneration associated with a microrough titanium surface. Clinical Oral Implants Research 22: 390-398.
12. Donoviel, D.B., Hadjantonakis, A.K., Ikeda, M., Zheng, H., Hyslop, P.S. & Bernstein, A. (1999) Mice lacking both Presenilin genes exhibit early embryonic patterning defects. Genes & Development 13: 2801-2810.
13. Engin, F., Yao, Z., Yang, T., Zhou, G., Bertin, T., Jiang, M.M., Chen, Y., Wang, L., Zheng, H., Sutton, R.E., Boyce, B.F. & Lee, B. (2008) Dimorphic effects of Notch signaling in bone homeostasis. Nature Medicine 14: 299-305.
14. Galli, C., Piemontese, M., Lumetti, S., Manfredi, E., Macaluso, G.M. & Passeri, G. (2012) The importance of Wnt pathways for bone metabolism and their regulation by implant topography. European Cells & Materials 24: 46-59.
15. Gregory, C.A., Gunn, W.G., Peister, A. & Prockop, D.J. (2004) An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with Cetylpyridinium chloride extraction. Analytical Biochemistry 329: 77-84.
16. Haase, H.R., Ivanovski, S., Waters, M.J. & Bartold, P.M. (2003) Growth hormone regulates osteogenic marker mRNA expression in human periodontal fibroblasts and alveolar bone-derived cells. Journal of Periodontal Research 38: 366-374.
17. Hamlet, S., Alfarsi, M., George, R. & Ivanovski, S. (2012) The effect of hydrophilic titanium surface modification on macrophage inflammatory cytokine gene expression. Clinical Oral Implants Research 23: 584-590.
18. Han, P., Wu, C., Chang, J. & Xiao, Y. (2012) The cementogenic differentiation of periodontal ligament cells via the activation of Wnt/beta-catenin signalling pathway by Li(+) ions released from bioactive scaffolds. Biomaterials 33: 6370-6379.
19. Hemming, M.L., Elias, J.E., Gygi, S.P. & Selkoe, D.J. (2008) Proteomic profiling of gamma-secretase substrates and mapping of substrate requirements. PLoS Biology 6: e257.
20. Herreman, A., Hartmann, D., Annaert, W., Saftig, P., Craessaerts, K., Serneels, L., Umans, L., Schrijvers, V., Checler, F., Vanderstichele, H., Baekelandt, V., Dressel, R., Cupers, P., Huylebroeck, D., Zwijsen, A., Van Leuven, F. & De Strooper, B. (1999) Presenilin 2 deficiency causes a mild pulmonary phenotype and no changes in amyloid precursor protein processing but enhances the embryonic lethal phenotype of Presenilin 1 deficiency. Proceedings of the National Academy of Sciences of the United States of America 96: 11872-11877.
21. Ito, T., Sawada, R., Fujiwara, Y. & Tsuchiya, T. (2008) FGF-2 increases osteogenic and chondrogenic differentiation potentials of human mesenchymal stem cells by inactivation of Tgf-beta signaling. Cytotechnology 56: 1-7.
22. Ivanovski, S., Hamlet, S., Retzepi, M., Wall, I. & Donos, N. (2011b) Transcriptional profiling of "guided bone regeneration" in a critical-size calvarial defect. Clinical Oral Implants Research 22: 382-389.
23. Ivanovski, S., Hamlet, S., Salvi, G.E., Huynh-Ba, G., Bosshardt, D.D., Lang, N.P. & Donos, N. (2011a) Transcriptional profiling of osseointegration in humans. Clinical Oral Implants Research 22: 373-381.
24. Kaether, C., Haass, C. & Steiner, H. (2006) Assembly, trafficking and function of gamma-secretase. Neuro-Degenerative Diseases 3: 275-283.
25. Koga, T., Matsui, Y., Asagiri, M., Kodama, T., de Crombrugghe, B., Nakashima, K. & Takayanagi, H. (2005) NFAT and Osterix cooperatively regulate bone formation. Nature Medicine 11: 880-885.
26. Lai, H.C., Zhuang, L.F., Zhang, Z.Y., Wieland, M. & Liu, X. (2009) Bone apposition around two different sandblasted, large-grit and acid-etched implant surfaces at sites with coronal circumferential defects: an experimental study in dogs. Clinical Oral Implants Research 20: 247-253.
27. Lang, N.P., Salvi, G.E., Huynh-Ba, G., Ivanovski, S., Donos, N. & Bosshardt, D.D. (2011) Early osseointegration to hydrophilic and hydrophobic implant surfaces in humans. Clinical Oral Implants Research 22: 349-356.
28. Lin, G.L. & Hankenson, K.D. (2011) Integration of BMP, Wnt, and Notch signaling pathways in osteoblast differentiation. Journal of Cellular Biochemistry 112: 3491-3501.
29. Liu, L., Ling, J., Wei, X., Wu, L. & Xiao, Y. (2009) Stem cell regulatory gene expression in human adult dental pulp and periodontal ligament cells undergoing odontogenic/osteogenic differentiation. Journal of Endodontics 35: 1368-1376.
30. Mak, K.K., Chen, M.H., Day, T.F., Chuang, P.T. & Yang, Y. (2006) Wnt/beta-catenin signaling interacts differentially with Ihh signaling in controlling endochondral bone and synovial joint formation. Development 133: 3695-3707.
31. Mao, X., Peng, H., Ling, J., Friis, T., Whittaker, A.K., Crawford, R. & Xiao, Y. (2009) Enhanced human bone marrow stromal cell affinity for modified poly(l-lactide) surfaces by the upregulation of adhesion molecular genes. Biomaterials 30: 6903-6911.
32. Mareddy, S., Dhaliwal, N., Crawford, R. & Xiao, Y. (2010) Stem cell-related gene expression in clonal populations of mesenchymal stromal cells from bone marrow. Tissue Engineering Part A 16: 749-758.
33. Nobta, M., Tsukazaki, T., Shibata, Y., Xin, C., Moriishi, T., Sakano, S., Shindo, H. & Yamaguchi, A. (2005) Critical regulation of Bone Morphogenetic Protein-induced osteoblastic differentiation by Delta1/Jagged1-activated Notch1 signaling. The Journal of Biological Chemistry 280: 15842-15848.
34. Olivares-Navarrete, R., Hyzy, S.L., Hutton, D.L., Dunn, G.R., Appert, C., Boyan, B.D. & Schwartz, Z. (2011a) Role of non-canonical Wnt signaling in osteoblast maturation on microstructured titanium surfaces. Acta Biomaterialia 7: 2740-2750.
35. Olivares-Navarrete, R., Hyzy, S.L., Hutton, D.L., Erdman, C.P., Wieland, M., Boyan, B.D. & Schwartz, Z. (2010a) Direct and indirect effects of microstructured titanium substrates on the induction of mesenchymal stem cell differentiation towards the osteoblast lineage. Biomaterials 31: 2728-2735.
36. Olivares-Navarrete, R., Hyzy, S.L., Park, J.H., Dunn, G.R., Haithcock, D.A., Wasilewski, C.E., Boyan, B.D. & Schwartz, Z. (2011b) Mediation of osteogenic differentiation of human mesenchymal stem cells on titanium surfaces by a Wnt-integrin feedback loop. Biomaterials 32: 6399-6411.
37. Olivares-Navarrete, R., Hyzy, S.L., Wieland, M., Boyan, B.D. & Schwartz, Z. (2010b) The roles of Wnt signaling modulators Dickkopf-1 (Dkk1) and Dickkopf-2 (Dkk2) and cell maturation state in osteogenesis on microstructured titanium surfaces. Biomaterials 31: 2015-2024.
38. Roccuzzo, M., Bunino, M., Prioglio, F. & Bianchi, S.D. (2001) Early loading of sandblasted and acid-etched (SLA) implants: a prospective split-mouth comparative study. Clinical Oral Implants Research 12: 572-578.
39. Saneyoshi, T., Kume, S., Amasaki, Y. & Mikoshiba, K. (2002) The Wnt/Calcium pathway activates NFAT and promotes ventral cell fate in Xenopus embryos. Nature 417: 295-299.
40. Schwartz, Z., Lohmann, C.H., Sisk, M., Cochran, D.L., Sylvia, V.L., Simpson, J., Dean, D.D. & Boyan, B.D. (2001) 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 22: 731-741.
41. Seifert, J.R. & Mlodzik, M. (2007) Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility. Nature Reviews Genetics 8: 126-138.
42. Slusarski, D.C. & Pelegri, F. (2007) Calcium signaling in vertebrate embryonic patterning and morphogenesis. Developmental Biology 307: 1-13.
43. St-Jacques, B., Hammerschmidt, M. & McMahon, A.P. (1999) Indian Hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes & Development 13: 2072-2086.
44. Swain, P.S. (2004) Efficient attenuation of stochasticity in gene expression through post-transcriptional control. Journal of Molecular Biology 344: 965-976.
45. Taniguchi, Y., Karlstrom, H., Lundkvist, J., Mizutani, T., Otaka, A., Vestling, M., Bernstein, A., Donoviel, D., Lendahl, U. & Honjo, T. (2002) Notch receptor cleavage depends on but is not directly executed by Presenilins. Proceedings of the National Academy of Sciences of the United States of America 99: 4014-4019.
46. Tsutsumi, S., Shimazu, A., Miyazaki, K., Pan, H., Koike, C., Yoshida, E., Takagishi, K. & Kato, Y. (2001) Retention of multilineage differentiation potential of mesenchymal cells during proliferation in response to FGF. Biochemical and Biophysical Research Communications 288: 413-419.
47. Vlacic-Zischke, J., Hamlet, S.M., Friis, T., Tonetti, M.S. & Ivanovski, S. (2011) The influence of surface microroughness and hydrophilicity of titanium on the up-regulation of TGFβ/BMP signalling in osteoblasts. Biomaterials 32: 665-671.
48. Wall, I., Donos, N., Carlqvist, K., Jones, F. & Brett, P. (2009) Modified titanium surfaces promote accelerated osteogenic differentiation of mesenchymal stromal cells in vitro. Bone 45: 17-26.
49. Wang, W., Zhao, L., Ma, Q., Wang, Q., Chu, P.K. & Zhang, Y. (2012) The role of the Wnt/beta-catenin pathway in the effect of implant topography on MG63 differentiation. Biomaterials 33: 7993-8002.
50. Wennerberg, A., Galli, S. & Albrektsson, T. (2011) Current knowledge about the hydrophilic and nanostructured SLActive surface. Clinical, Cosmetic and Investigational Dentistry 3: 59-67.
51. Wennerberg, A., Svanborg, L.M., Berner, S. & Andersson, M. (2013) Spontaneously formed nanostructures on titanium surfaces. Clinical Oral Implants Research 24: 203-209.
52. Wieland, M., Textor, M., Chehroudi, B. & Brunette, D.M. (2005) Synergistic interaction of topographic features in the production of bone-like nodules on Ti surfaces by rat osteoblasts. Biomaterials 26: 1119-1130.
53. Xiao, Y., Haase, H., Young, W.G. & Bartold, P.M. (2004) Development and transplantation of a mineralized matrix formed by osteoblasts in vitro for bone regeneration. Cell Transplantation 13: 15-25.
54. Xiao, Y., Qian, H., Young, W.G. & Bartold, P.M. (2003) Tissue engineering for bone regeneration using differentiated alveolar bone cells in collagen scaffolds. Tissue Engineering 9: 1167-1177.
55. Zamurovic, N., Cappellen, D., Rohner, D. & Susa, M. (2004) Coordinated activation of Notch, Wnt, and Transforming Growth Factor-beta signaling pathways in Bone Morphogenic Protein 2-induced osteogenesis. Notch target gene Hey1 inhibits mineralization and Runx2 transcriptional activity. The Journal of Biological Chemistry 279: 37704-37715.
56. Zhao, G., Raines, A.L., Wieland, M., Schwartz, Z. & Boyan, B.D. (2007) Requirement for both micron- and submicron scale structure for synergistic responses of osteoblasts to substrate surface energy and topography. Biomaterials 28: 2821-2829.
57. Zinger, O., Zhao, G., Schwartz, Z., Simpson, J., Wieland, M., Landolt, D. & Boyan, B. (2005) Differential regulation of osteoblasts by substrate microstructural features. Biomaterials 26: 1837-1847.