The importance of WNT pathways for bone metabolism and their regulation by implant topography

European Cells and Materials

Volumn 24, Issue , 2012, Pages 46-59

  Galli, C ^a   Piemontese, M ^a   Lumetti, S ^a   Manfredi, E ^a   MacAluso, G M ^a   Passeri, G ^a  

^a UNIVERSITY OF PARMA   (Italy)

Author keywords

Cytoskeleton; Osteoblasts; Titanium implants; Topography; WNT

Indexed keywords

BETA CATENIN; CALCIUM; DICKKOPF 1 PROTEIN; DICKKOPF 2 PROTEIN; DISHEVELLED PROTEIN; FRIZZLED PROTEIN; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; NANOTUBE; OSTEOCALCIN; OSTEOCLAST DIFFERENTIATION FACTOR; PROTEIN; PROTEIN KINASE C; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; T CELL FACTOR PROTEIN; TITANIUM; TITANIUM DIOXIDE; TITANIUM OXIDE NANOTUBE; TRANSCRIPTION FACTOR OSTERIX; UNCLASSIFIED DRUG; WNT PROTEIN; WNT3 PROTEIN; WNT5A PROTEIN;

ADIPOCYTE; BONE METABOLISM; CELL ACTIVITY; CELL CONTRACTILITY; CELL DIFFERENTIATION; CELL GROWTH; CELL JUNCTION; CELL POLARITY; CELL PROLIFERATION; CELL SHAPE; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; ENDOSSEOUS IMPLANT; GENE EXPRESSION PROFILING; HUMAN; IMPLANT; INTRACELLULAR SIGNALING; MECHANICAL STIMULATION; NONHUMAN; OSTEOBLAST; PLANAR CELL POLARITY; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SURFACE PROPERTY;

EID: 84864051341     PISSN: 14732262     EISSN: None     Source Type: Journal    
DOI: 10.22203/eCM.v024a04     Document Type: Review

References (167)

1. Angers S, Moon RT (2009) Proximal events in Wnt signal transduction. Nat Rev Mol Cell Biol 10: 468-477.
2. Anselme K (2011) Biomaterials and interface with bone. Osteoporos Int 22: 2037-2042.
3. Anselme K, Ponche A, Bigerelle M (2010) Relative influence of surface topography and surface chemistry on cell response to bone implant materials. Part 2: biological aspects. Proc Inst Mech Eng H 224: 1487-1507.
4. Anton R, Kestler HA, Kuhl M (2007). Beta-catenin signaling contributes to stemness and regulates early differentiation in murine embryonic stem cells. FEBS Lett 581: 5247-5254.
5. Arce L, Yokoyama NN, Waterman ML (2006) Diversity of LEF/TCF action in development and disease. Oncogene 25: 7492-7504.
6. Arcelli D, Palmieri A, Pezzetti F, Brunelli G, Zollino I, Carinci F (2007) Genetic effects of a titanium surface on osteoblasts: a meta-analysis. J Oral Sci 49: 299-309.
7. Arnsdorf EJ, Tummala P, Jacobs CR (2009a) Non-canonical Wnt signaling and N-cadherin related beta-catenin signaling play a role in mechanically induced osteogenic cell fate. PLoS One 4: e5388.
8. Arnsdorf EJ, Tummala P, Kwon RY, Jacobs CR (2009b) Mechanically induced osteogenic differentiation-the role of RhoA, ROCKII and cytoskeletal dynamics. J Cell Sci 122: 546-553.
9. Aubert J, Dunstan H, Chambers I, Smith A (2002) Functional gene screening in embryonic stem cells implicates Wnt antagonism in neural differentiation. Nature Biotechnol 20: 1240-1245.
10. Axelrod JD, Miller JR, Shulman JM, Moon RT, Perrimon N (1998) Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes Dev 12: 2610-2622.
11. Babij P, Zhao W, Small C, Kharode Y, Yaworsky PJ, Bouxsein ML, Reddy PS, Bodine PV, Robinson JA, Bhat B, Marzolf J, Moran RA, Bex F (2003) High bone mass in mice expressing a mutant LRP5 gene. J Bone Miner Res 18: 960-974.
12. Bernatik O, Ganji RS, Dijksterhuis JP, Konik P, Cervenka I, Polonio T, Krejci P, Schulte G, Bryja V (2011) Sequential activation and inactivation of Dishevelled in the Wnt/beta-catenin pathway by casein kinases. J Biol Chem 286: 10396-10410.
13. Bigerelle M, Anselme K, Noël B, Ruderman I, Hardouin P, Iost A (2002) Improvement in the morphology of Ti-based surfaces: a new process to increase in vitro human osteoblast response. Biomaterials 23: 1563-1577.
14. Bigerelle M, Giljean S, Anselme K (2011) Existence of a typical threshold in the response of human mesenchymal stem cells to a peak and valley topography. Acta Biomater 7: 3302-3311.
15. Biggs MJ, Richards RG, Gadegaard N, McMurray RJ, Affrossman S, Wilkinson CD, Oreffo RO, Dalby MJ (2009) Interactions with nanoscale topography: adhesion quantification and signal transduction in cells of osteogenic and multipotent lineage. J Biomed Mater Res A 91: 195-208.
16. Boland GM, Perkins G, Hall DJ, Tuan RS (2004) Wnt 3a promotes proliferation and suppresses osteogenic differentiation of adult human mesenchymal stem cells. J Cell Biochem 93: 1210-1230.
17. Bornstein MM, Valderrama P, Jones AA, Wilson TG, Seibl R, Cochran DL (2008) Bone apposition around two different sandblasted and acid-etched titanium implant surfaces: a histomorphometric study in canine mandibles. Clin Oral Implants Res 19: 233-241.
18. Boutahar N, Guignandon A, Vico L, Lafage-Proust MH (2004) Mechanical strain on osteoblasts activates autophosphorylation of focal adhesion kinase and proline-rich tyrosine kinase 2 tyrosine sites involved in ERK activation. J Biol Chem 279: 30588-30599.
19. Boutros M, Mlodzik M (1999) Dishevelled: at the crossroads of divergent intracellular signaling pathways. Mech Dev 83: 27-37.
20. Boyan BD, Bonewald LF, Paschalis EP, Lohmann CH, Rosser J, Cochran DL, Dean DD, Schwartz Z, Boskey AL (2002) Osteoblast mediated mineral deposition in culture is dependent on surface mictotopography. Calcif Tiss Int 71: 519-529.
21. Boyden LM, Mao J, Belsky J, Mitzner L, Farhi A, Mitnick MA, Wu D, Insogna K, Lifton RP (2002) High bone density due to a mutation in LDL-receptor-related protein 5. N Engl J Med 346: 1513-1521.
22. Brånemark PI (1983) Osseointegration and its experimental background. J Prosthet Dent 50: 399-410.
23. Buser D, Broggini N, Wieland M, Schenk RK, Denzer AJ, Cochran DL, Hoffmann B, Lussi A, Steinemann SG (2004) Enhanced bone apposition to a chemically modified SLA titanium surface. J Dent Res 83: 529-533.
24. Cadigan KM, Nusse R (1997) Wnt signaling: a common theme in animal development. Genes Dev 11: 3286-3305.
25. Calzado-Martín A, Méndez-Vilas A, Multigner M, Saldaña L, González-Carrasco JL, González-Martín ML, Vilaboa N (2011) On the role of RhoA/ROCK signaling in contact guidance of bone-forming cells on anisotropic Ti6Al4V surfaces. Acta Biomater 7:1890-1901.
26. Cervenka I, Wolf J, Masek J, Krejci P, Wilcox WR, Kozubik A, Schulte G, Gutkind JS, Bryja V (2011) Mitogen-activated protein kinases promote WNT/beta-catenin signaling via phosphorylation of LRP6. Mol Cell Biol 31: 179-189.
27. Chang J, Sonoyama W, Wang Z, Jin Q, Zhang C, Krebsbach PH, Giannobile W, Shi S, Wang CY (2007) Noncanonical Wnt-4 signaling enhances bone regeneration of mesenchymal stem cells in craniofacial defects through activation of p38 MAPK. J Biol Chem 282: 30938-30948.
28. Chatterjee K, Lin-Gibson S, Wallace WE, Parekh SH, Lee YJ, Cicerone MT, Young MF, Simon CG Jr (2010) The effect of 3D hydrogel scaffold modulus on osteoblast differentiation and mineralization revealed by combinatorial screening. Biomaterials 31: 5051-5062.
29. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE (1997) Geometric control of cell life and death. Science 276: 1425-1428.
30. Chen M, Zhu M, Awad H, Li TF, Sheu TJ, Boyce BF, Chen D, O'Keefe RJ (2008) Inhibition of beta-catenin signaling causes defects in postnatal cartilage development. J Cell Sci 121: 1455-1465.
31. Chia IV, Costantini F (2005) Mouse axin and axin2/conductin proteins are functionally equivalent in vivo. Mol Cell Biol 25: 4371-4376.
32. Cho M, Park S, Gwak J, Kim DE, Yea SS, Shin JG, Oh S (2008) Bisindoylmaleimide I suppresses adipocyte differentiation through stabilization of intracellular beta-catenin protein. Biochem Biophys Res Commun 367: 195-200.
33. Chun JS, Oh H, Yang S, Park M (2008) Wnt signaling in cartilage development and degeneration. BMB Rep 41: 485-494.
34. Chung YS, Baylink DJ, Srivastava AK, Amaar Y, Tapia B, Kasukawa Y, Mohan S (2004) Effects of secreted frizzled-related protein 3 on osteoblasts in vitro. J Bone Miner Res 19: 1395-1402.
35. Clement-Lacroix P, Ai M, Morvan F, Roman-Roman S, Vayssiere B, Belleville C, Estrera K, Warman ML, Baron R, Rawadi G (2005) Lrp5-independent activation of Wnt signaling by lithium chloride increases bone formation and bone mass in mice. Proc Natl Acad Sci USA 102: 17406-17411.
36. Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480.
37. Coelho PG, Freire JN, Granato R, Marin C, Bonfante EA, Gil JN, Chuang SK, Suzuki M (2011) Bone mineral apposition rates at early implantation times around differently prepared titanium surfaces: a study in beagle dogs. Int J Oral Maxillofac Implants 26: 63-69.
38. Dalby MJ, Andar A, Nag A, Affrossman S, Tare R, McFarlane S, Oreffo RO (2008) Genomic expression of mesenchymal stem cells to altered nanoscale topographies. J R Soc Interface.5: 1055-1065.
39. De Boer J, Wang HJ, Van Blitterswijk C (2004) Effects of Wnt signaling on proliferation and differentiation of human mesenchymal stem cells. Tissue Eng 10: 393-401.
40. Doble BW, Patel S, Wood GA, Kockeritz LK, Woodgett JR (2007) Functional redundancy of GSK-3alpha and GSK-3beta in Wnt/beta-catenin signaling shown by using an allelic series of embryonic stem cell lines. Dev Cell 12: 957-971.
41. Donos N, Hamlet S, Lang NP, Salvi GE, Huynh-Ba G, Bosshardt DD, Ivanovski S (2011a) Gene expression profile of osseointegration of a hydrophilic compared with a hydrophobic microrough implant surface. Clin Oral Implants Res 22: 365-372.
42. 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. Clin Oral Implants Res 22: 390-398.
43. Dravid G, Ye Z, Hammond H, Chen G, Pyle A, Donovan P, Yu X, Cheng L (2005) Defining the role of Wnt/beta-catenin signaling in the survival, proliferation, and self-renewal of human embryonic stem cells. Stem Cells 23: 1489-1501.
44. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689.
45. Force T, Woodgett JR (2009) Unique and overlapping functions of GSK-3 isoforms in cell differentiation and proliferation and cardiovascular development. J Biol Chem 284: 9643-9647.
46. Freisinger CM, Schneider I, Westfall TA, Slusarski DC (2008) Calcium dynamics integrated into signalling pathways that influence vertebrate axial patterning. Philos Trans R Soc Lond B Biol Sci 363: 1377-1385.
47. Fromigue O, Hay E, Barbara A, Marie PJ (2010) Essential role of nuclear factor of activated T cells (NFAT)-mediated Wnt signaling in osteoblast differentiation induced by strontium ranelate. J Biol Chem 285: 25251-25258.
48. Fukuda T, Kokabu S, Ohte S, Sasanuma H, Kanomata K, Yoneyama K, Kato H, Akita M, Oda H, Katagiri T (2010) Canonical Wnts and BMPs cooperatively induce osteoblastic differentiation through a GSK3beta-dependent and beta-catenin-independent mechanism. Differentiation. 80: 46-52.
49. Gahlert M, Gudehus T, Eichhorn S, Steinhauser E, Kniha H, Erhardt W (2007) Biomechanical and histomorphometric comparison between zirconia implants with varying surface textures and a titanium implant in the maxilla of miniature pigs. Clin Oral Implants Res 18: 662-668.
50. Galli C, Passeri G, Ravanetti F, Elezi E, Pedrazzoni M, Macaluso GM (2010) Rough surface topography enhances the activation of Wnt/beta-catenin signaling in mesenchymal cells. J Biomed Mater Res A 95: 682-690.
51. Galli C, Macaluso GM, Piemontese M, Passeri G (2011) Titanium topography controls FoxO/beta-catenin signaling. J Dent Res 90: 360-364.
52. Gao C, Chen YG (2010) Dishevelled: The hub of Wnt signaling. Cell Signal 22: 717-727.
53. Germanier Y, Tosatti S, Broggini N, Textor M, Buser D (2006) Enhanced bone apposition around biofunctionalized sandblasted and acid-etched titanium implant surfaces. A histomorphometric study in miniature pigs. Clin Oral Implants Res 17: 251-257.
54. Glass DA 2nd, Bialek P, Ahn JD, Starbuck M, Patel MS, Clevers H, Taketo MM, Long F, McMahon AP, Lang RA, Karsenty G (2005) Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev Cell 8: 751-764.
55. Gong Y, Slee RB, Fukai N, Rawadi G, Roman-Roman S, Reginato AM, Wang H, Cundy T, Glorieux FH, Lev D, Zacharin M, Oexle K, Marcelino J, Suwairi W, Heeger S, Sabatakos G, Apte S, Adkins WN, Allgrove J, Arslan-Kirchner M, Batch JA, Beighton P, Black GC, Boles RG, Boon LM, Borrone C, Brunner HG, Carle GF, Dallapiccola B, De Paepe A, Floege B, Halfhide ML, Hall B, Hennekam RC, Hirose T, Jans A, Juppner H, Kim CA, Keppler-Noreuil K, Kohlschuetter A, LaCombe D, Lambert M, Lemyre E, Letteboer T, Peltonen L, Ramesar RS, Romanengo M, Somer H, Steichen-Gersdorf E, Steinmann B, Sullivan B, Superti-Furga A, Swoboda W, van den Boogaard MJ, Van Hul W, Vikkula M, Votruba M, Zabel B, Garcia T, Baron R, Olsen BR, Warman ML (2001) LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 107: 513-523.
56. Habas R, Dawid IB, He X (2003) Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. Genes Dev 17: 295-309.
57. Hamamura K, Swarnkar G, Tanjung N, Cho E, Li J, Na S, Yokota H (2012) RhoA-mediated signaling in mechanotransduction of osteoblasts. Connect Tissue Res, in press.
58. Hao J, Li TG, Qi X, Zhao DF, Zhao GQ.(2006). WNT/beta-catenin pathway up-regulates Stat3 and converges on LIF to prevent differentiation of mouse embryonic stem cells. Dev Biol 290: 81-91.
59. Hay E, Laplantine E, Geoffroy V, Frain M, Kohler T, Muller R, Marie PJ (2009) N-cadherin interacts with axin and LRP5 to negatively regulate Wnt/beta-catenin signaling, osteoblast function, and bone formation. Mol Cell Biol 29: 953-964.
60. Heath DJ, Chantry AD, Buckle CH, Coulton L, Shaughnessy JD Jr, Evans HR, Snowden JA, Stover DR, Vanderkerken K, Croucher PI (2009) Inhibiting Dickkopf-1 (Dkk1) removes suppression of bone formation and prevents the development of osteolytic bone disease in multiple myeloma. J Bone Miner Res 24: 425-436.
61. Hill TP, Später D, Taketo MM, Birchmeier W, Hartmann C (2005) Canonical Wnt/beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev Cell 8: 727-738.
62. Hoeppner LH, Secreto FJ, Westendorf JJ (2009) Wnt signaling as a therapeutic target for bone diseases. Expert Opin Ther Targets 13: 485-496.
63. Holmen SL, Giambernardi TA, Zylstra CR, Buckner-Berghuis BD, Resau JH, Hess JF, Glatt V, Bouxsein ML, Ai M, Warman ML, Williams BO (2004) Decreased BMD and limb deformities in mice carrying mutations in both Lrp5 and Lrp6. J Bone Miner Res 19: 2033-2040.
64. Hu S, Wang N (2006) Control of stress propagation in the cytoplasm by prestress and loading frequency. Mol Cell Biomech 3: 49-60.
65. Huang Y, Zhang X, Du K, Yang F, Shi Y, Huang J, Tang T, Chen D, Dai K (2012) Inhibition of beta-catenin signaling in chondrocytes induces delayed fracture healing in mice. J Orthop Res, in press.
66. Huelsken J, Vogel R, Brinkmann V, Erdmann B, Birchmeier C, Birchmeier W (2000) Requirement for beta-catenin in anterior-posterior axis formation in mice. J Cell Biol 148: 567-578.
67. Ingber DE (1993) Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J Cell Sci. 104: 613-627.
68. Ingber DE (2003) Tensegrity I. Cell structure and hierarchical systems biology. J Cell Sci 116: 1157-1173.
69. Isa ZM, Schneider GB, Zaharias R, Seabold D, Stanford CM (2006) Effects of fluoride-modified titanium surfaces on osteoblast proliferation and gene expression. Int J Oral Maxillofac Implants 21: 203-211.
70. Ivanovski S, Hamlet S, Salvi GE, Huynh-Ba G, Bosshardt DD, Lang NP, Donos N (2011) Transcriptional profiling of osseointegration in humans. Clin Oral Implants Res 22: 373-381.
71. Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21: 247-269.
72. Joeng KS, Schumacher CA, Zylstra-Diegel CR, Long F, Williams BO (2011) Lrp5 and Lrp6 redundantly control skeletal development in the mouse embryo. Dev Biol 359: 222-229.
73. Kämmerer PW, Gabriel M, Al-Nawas B, Scholz T, Kirchmaier CM, Klein MO (2012) Early implant healing: promotion of platelet activation and cytokine release by topographical, chemical and biomimetical titanium surface modifications in vitro. Clin Oral Implants Res 23: 504-510.
74. Kanno T, Takahashi T, Tsujisawa T, Ariyoshi W, Nishihara T (2007) Mechanical stress-mediated Runx2 activation is dependent on Ras/ERK1/2 MAPK signaling in osteoblasts. J Cell Biochem 101: 1266-1277.
75. Kato M, Patel MS, Levasseur R, Lobov I, Chang BH, Glass DA 2nd, Hartmann C, Li L, Hwang TH, Brayton CF, Lang RA, Karsenty G, Chan L (2002) Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J Cell Biol 157: 303-314.
76. Katoh Y, Katoh M (2005) Identification and characterization of rat Wnt1 and Wnt10b genes in silico. Int J Oncol 26: 841-845.
77. Kearney EM, Farrell E, Prendergast PJ, Campbell VA (2010) Tensile strain as a regulator of mesenchymal stem cell osteogenesis. Ann Biomed Eng 38:1767-1779.
78. Keller JC, Schneider GB, Stanford CM, Kellogg B (2003) Effects of implant microtopography on osteoblast cell attachment. Implant Dent 12: 175-181.
79. Kennell JA, MacDougald OA (2005) Wnt signaling inhibits adipogenesis through beta-catenin-dependent and-independent mechanisms. J Biol Chem 280: 24004-24010.
80. Kilian KA, Bugarija B, Lahn BT, Mrksich M (2010) Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci USA 107: 4872-4877.
81. Kim JB, Leucht P, Lam K, Luppen C, Ten Berge D, Nusse R, Helms JA (2007) Bone regeneration is regulated by wnt signaling. J Bone Miner Res 22: 1913-1923.
82. Kishida S, Yamamoto H, Hino S, Ikeda S, Kishida M, Kikuchi A (1999) DIX domains of Dvl and axin are necessary for protein interactions and their ability to regulate beta-catenin stability. Mol Cell Biol 19: 4414-4422.
83. Kokubu C, Heinzmann U, Kokubu T, Sakai N, Kubota T, Kawai M, Wahl MB, Galceran J, Grosschedl R, Ozono K, Imai K (2004) Skeletal defects in ringelschwanz mutant mice reveal that Lrp6 is required for proper somitogenesis and osteogenesis. Development 131: 5469-5480.
84. Krishnan V, Bryant HU, Macdougald OA (2006) Regulation of bone mass by Wnt signaling. J Clin Invest 116: 1202-1209.
85. Kuhl M (2004) The WNT/calcium pathway: biochemical mediators, tools and future requirements. Front Biosci 9: 967-974.
86. 2+/calmodulin-dependent protein kinase II is stimulated by Wnt and Frizzled homologs and promotes ventral cell fates in Xenopus. J Biol Chem 275: 12701-12711.
87. 2+pathway: a new vertebrate Wnt signaling pathway takes shape. Trends Genet 16: 279-283.
88. Lai HC, Zhuang LF, Liu X, Wieland M, Zhang ZY, Zhang ZY (2010) The influence of surface energy on early adherent events of osteoblast on titanium substrates. J Biomed Mater Res A 93: 289-296.
89. Lee YN, Gao Y, Wang HY (2008) Differential mediation of the Wnt canonical pathway by mammalian Dishevelleds-1,-2, and-3. Cell Signal 20: 443-452.
90. Li D, Zhou J, Chowdhury F, Cheng J, Wang N, Wang F (2011) Role of mechanical factors in fate decisions of stem cells. Regen Med 6: 229-240.
91. Li FQ, Singh AM, Mofunanya A, Love D, Terada N, Moon RT, Takemaru K (2007) Chibby promotes adipocyte differentiation through inhibition of beta-catenin signaling. Mol Cell Biol 27: 4347-4354.
92. Li X, Liu P, Liu W, Maye P, Zhang J, Zhang Y, Hurley M, Guo C, Boskey A, Sun L, Harris SE, Rowe DW, Ke HZ, Wu D (2005) Dkk2 has a role in terminal osteoblast differentiation and mineralized matrix formation. Nat Genet 37: 945-952.
93. Linez-Bataillon P, Monchau F, Bigerelle M, Hildebrand HF (2002) In vitro MC3T3 osteoblast adhesion with respect to surface roughness of Ti6Al4V substrates. Biomol Eng 19: 133-141.
94. Liu J, Jin T, Chang S, Czajka-Jakubowska A, Zhang Z, Nör JE, Clarkson BH (2010) The effect of novel fluorapatite surfaces on osteoblast-like cell adhesion, growth, and mineralization. Tissue Eng Part A 16: 2977-2986.
95. Liu J, Wang X, Jin Q, Jin T, Chang S, Zhang Z, Czajka-Jakubowska A, Giannobile WV, Nör JE, Clarkson BH (2012) The stimulation of adipose-derived stem cell differentiation and mineralization by ordered rod-like fluorapatite coatings. Biomaterials 33: 5036-5046.
96. Lossdorfer S, Schwartz Z, Wang L, Lohmann CH, Turner JD, Wieland M, Cochran DL, Boyan BD (2004) Microrough implant surface topographies increase osteogenesis by reducing osteoclast formation and activity. J Biomed Mater Res A 70: 361-369.
97. Lyashenko N, Winter M, Migliorini D, Biechele T, Moon RT, Hartmann C (2011) Differential requirement for the dual functions of β-catenin in embryonic stem cell self-renewal and germ layer formation. Nat Cell Biol 13: 753-761.
98. Martin BL, Kimelman D (2009) Wnt signaling and the evolution of embryonic posterior development. Curr Biol 19: R215-219.
99. Masaki C, Schneider GB, Zaharias R, Seabold D, Stanford C (2005) Effects of implant surface microtopography on osteoblast gene expression. Clin Oral Implants Res 16: 650-656.
100. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6: 483-495.
101. Mikels AJ, Nusse R (2006) Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol 4: e115.
102. Miki T, Yasuda SY, Kahn M (2011) Wnt/β-catenin signaling in embryonic stem cell self-renewal and somatic cell reprogramming. Stem Cell Rev 7: 836-846.
103. Milat F, Ng KW (2009) Is wnt-signalling the final common pathway leading to bone formation? Mol Cell Endocrinol 310: 52-62
104. Mosimann C, Hausmann G, Basler K (2009) Beta-catenin hits chromatin: regulation of Wnt target gene activation. Nat Rev Mol Cell Biol 10: 276-286.
105. Nusse R (2008) Wnt signaling and stem cell control. Cell Res 18: 523-527.
106. Oh S, Brammer KS, Li YS, Teng D, Engler AJ, Chien S, Jin S (2009) Stem cell fate dictated solely by altered nanotube dimension. Proc Natl Acad Sci USA 106: 2130-2135.
107. Olivares-Navarrete R, Hyzy S, Wieland M, Boyan BD, Schwartz Z (2010a) 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.
108. Olivares-Navarrete R, Hyzy SL, Hutton DL, Erdman CP, Wieland M, Boyan BD, Schwartz Z (2010b) Direct and indirect effects of microstructured titanium substrates on the induction of mesenchymal stem cell differentiation towards the osteoblast lineage. Biomaterials 31: 2728-2735.
109. Olivares-Navarrete R, Hyzy SL, Hutton DL, Dunn GR, Appert C, Boyan BD, Schwartz Z (2011a) Role of non-canonical Wnt signaling in osteoblast maturation on microstructured titanium surfaces. Acta Biomater 7: 2740-2750.
110. Olivares-Navarrete R, Hyzy SL, Park JH, Dunn GR, Haithcock DA, Wasilewski CE, Boyan BD, 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.
111. Pan WJ, Pang SZ, Huang T, Guo HY, Wu D, Li L (2004) Characterization of function of three domains in dishevelled-1: DEP domain is responsible for membrane translocation of dishevelled-1. Cell Res 14: 324-330.
112. Park JW (2011) Increased bone apposition on a titanium oxide surface incorporating phosphate and strontium. Clin Oral Implants Res 22: 230-234.
113. Pek YS, Wan AC, Ying JY (2010) The effect of matrix stiffness on mesenchymal stem cell differentiation in a 3D thixotropic gel. Biomaterials 31:385-391.
114. Pereira L, Yi F, Merrill BJ (2006) Repression of Nanog gene transcription by Tcf3 limits embryonic stem cell self-renewal. Mol Cell Biol 26: 7479-7491.
115. Ponik SM, Pavalko FM (2004) Formation of focal adhesions on fibronectin promotes fluid shear stress induction of COX-2 and PGE2 release in MC3T3-E1 osteoblasts. J Appl Physiol 97: 135-142.
116. Popelut A, Rooker SM, Leucht P, Medio M, Brunski JB, Helms JA (2010) The acceleration of implant osseointegration by liposomal Wnt3a. Biomaterials 31: 9173-9181.
117. Qiang YW, Barlogie B, Rudikoff S, Shaughnessy JD Jr (2008a) Dkk1-induced inhibition of Wnt signaling in osteoblast differentiation is an underlying mechanism of bone loss in multiple myeloma. Bone 42: 669-680.
118. Qiang YW, Chen Y, Stephens O, Brown N, Chen B, Epstein J, Barlogie B, Shaughnessy JD Jr (2008b) Myeloma-derived Dickkopf-1 disrupts Wnt-regulated osteoprotegerin and RANKL production by osteoblasts: a potential mechanism underlying osteolytic bone lesions in multiple myeloma. Blood 112: 196-207.
119. Qiang YW, Shaughnessy JD Jr, Yaccoby S (2008c) Wnt3a signaling within bone inhibits multiple myeloma bone disease and tumor growth. Blood 112: 374-382.
120. Ramires PA, Giuffrida A, Milella E (2002) Three-dimensional reconstruction of confocal laser microscopy images to study the behaviour of osteoblastic cells grown on biomaterials. Biomaterials 23: 397-406.
121. Rodda SJ, McMahon AP (2006) Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 133: 3231-3244.
122. Rossol-Allison J, Stemmle LN, Swenson-Fields KI, Kelly P, Fields PE, McCall SJ, Casey PJ, Fields TA (2009) Rho GTPase activity modulates Wnt3a/beta-catenin signaling. Cell Signal 21: 1559-1568.
123. Rupp F, Scheideler L, Olshanska N, de Wild M, Wieland M, Geis-Gerstorfer J (2006) Enhancing surface free energy and hydrophilicity through chemical modification of microstructured titanium implant surfaces. J Biomed Mater Res A 76: 323-334.
124. Salasznyk RM, Klees RF, Williams WA, Boskey A, Plopper GE (2007) Focal adhesion kinase signaling pathways regulate the osteogenic differentiation of human mesenchymal stem cells. Exp Cell Res. 313: 22-37.
125. Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou AH (2004) Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Natural Med 10: 55-63.
126. Sawakami K, Robling AG, Ai M, Pitner ND, Liu D, Warden SJ, Li J, Maye P, Rowe DW, Duncan RL, Warman ML, Turner CH (2006) The Wnt co-receptor LRP5 is essential for skeletal mechanotransduction but not for the anabolic bone response to parathyroid hormone treatment. J Biol Chem 281: 23698-23711.
127. Schlessinger K, Hall A, Tolwinski N (2009) Wnt signaling pathways meet Rho GTPases. Genes Dev 23: 265-277.
128. Schneider GB, Perinpanayagam H, Clegg M, Zaharias R, Seabold D, Keller J, Stanford C (2003) Implant surface roughness affects osteoblast gene expression. J Dent Res 82: 372-376.
129. Schneider GB, Zaharias R, Seabold D, Keller J, Stanford C (2004) Differentiation of preosteoblasts is affected by implant surface microtopographies. J Biomed Mater Res A 69: 462-468.
130. Schwartz Z, Olivares-Navarrete R, Wieland M, Cochran DL, Boyan BD (2009) Mechanisms regulating increased production of osteoprotegerin by osteoblasts cultured on microstructured titanium surfaces. Biomaterials 30: 3390-3396.
131. Schwarz F, Ferrari D, Herten M, Mihatovic I, Wieland M, Sager M, Becker J (2007) Effects of surface hydrophilicity and microtopography on early stages of soft and hard tissue integration at non-submerged titanium implants: an immunohistochemical study in dogs. J Periodontol 78: 2171-2184.
132. 2+flux, PKC, and CamKII in vertebrate embryos. J Cell Biol 161: 769-777.
133. Singla DK, Schneider DJ, LeWinter MM, Sobel BE (2006). wnt3a but not wnt11 supports self-renewal of embryonic stemcells. Biochem Biophys Res Commun 345: 789-795.
134. Smith PG, Deng L, Fredberg JJ, Maksym GN (2003) Mechanical strain increases cell stiffness through cytoskeletal filament reorganization. Am J Physiol Lung Cell Mol Physiol 285: L456-463.
135. Sokol SY (2011) Maintaining embryonic stem cell pluripotency with Wnt signaling. Development. 138: 4341-4350.
136. Sonderegger S, Pollheimer J, Knofler M (2010). Wnt signaling in implantation, decidualisation and placental differentiation: review. Placenta 31: 839-847.
137. Stamenovic D, Coughlin MF (1999) The role of prestress and architecture of the cytoskeleton and deformability of cytoskeletal filaments in mechanics of adherent cells: a quantitative analysis. J Theor Biol 201: 63-74.
138. Stamenovic D, Mijailovich SM, Tolic-Norrelykke IM, Chen J, Wang N (2002) Cell prestress. II. Contribution of microtubules. Am J Physiol Cell Physiol 282: C617-624.
139. Takao Y, Yokota T, Koide H. (2007). Beta-catenin upregulates Nanog expression through interaction with Oct-3/4 in embryonic stem cells. Biochem Biophys Res Commun 353: 699-705.
140. Takemaru K, Yamaguchi S, Lee YS, Zhang Y, Carthew RW, Moon RT (2003) Chibby, a nuclear beta-catenin-associated antagonist of the Wnt/Wingless pathway. Nature 422: 905-909.
141. Tanneberger K, Pfister AS, Kriz V, Bryja V, Schambony A, Behrens J (2011) Structural and functional characterization of the Wnt inhibitor APC membrane recruitment 1 (Amer1). J Biol Chem 286: 19204-19214.
142. Tu X, Joeng KS, Nakayama KI, Nakayama K, Rajagopal J, Carroll TJ, McMahon AP, Long F (2007) Noncanonical Wnt signaling through G protein-linked PKCdelta activation promotes bone formation. Dev Cell 12:113-127.
143. Turm H, Grisaru-Granvosky S, Maoz M, Offermanns S, Bar-Shavit R (2010) DVL as a scaffold protein capturing classical GPCRs. Commun Integr Biol 3: 495-498.
144. Tutter AV, Fryer CJ, Jones KA (2001) Chromatin-specific regulation of LEF-1-beta-catenin transcription activation and inhibition in vitro. Genes Dev 15: 3342-3354.
145. Van Amerongen R, Mikels A, Nusse R (2008) Alternative wnt signaling is initiated by distinct receptors. Sci Signal 1: re9.
146. Van Amerongen R, Nusse R (2009) Towards an integrated view of Wnt signaling in development. Development 136: 3205-3214.
147. Van der Horst G, van der Werf SM, Farih-Sips H, van Bezooijen RL, Lowik CW, Karperien M (2005) Downregulation of Wnt signaling by increased expression of Dickkopf-1 and-2 is a prerequisite for late-stage osteoblast differentiation of KS483 cells. J Bone Miner Res 20: 1867-1877.
148. Van Steenberghe D, Branemark PI, Quirynen M, De Mars G, Naert I (1991) The rehabilitation of oral defects by osseointegrated implants. J Clin Periodontol 18: 488-493.
149. Van Tienen FH, Laeremans H, van der Kallen CJ, Smeets HJ (2009) Wnt5b stimulates adipogenesis by activating PPARgamma, and inhibiting the beta-catenin dependent Wnt signaling pathway together with Wnt5a. Biochem Biophys Res Commun 387: 207-211.
150. Verheyen EM, Gottardi CJ (2010) Regulation of Wnt/beta-catenin signaling by protein kinases. Dev Dyn 239: 34-44.
151. Vlacic-Zischke J, Hamlet SM, Friis T, Tonetti MS, Ivanovski S (2011) The influence of surface microroughness and hydrophilicity of titanium on the up-regulation of TGFbeta/BMP signalling in osteoblasts. Biomaterials 32: 665-671.
152. 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.
153. Wang B, Du T, Wang Y, Yang C, Zhang S, Cao X (2011) Focal adhesion kinase signaling pathway is involved in mechanotransduction in MG-63 cells. Biochem Biophys Res Commun 410: 671-676.
154. Wang J, de Groot K, van Blitterswijk C, de Boer J (2009a) Electrolytic deposition of lithium into calcium phosphate coatings. Dent Mater 25: 353-359.
155. Wang N, Butler JP, Ingber DE (1993) Mechanotransduction across the cell surface and through the cytoskeleton. Science 260: 1124-1127.
156. Wang N, Ingber DE (1994) Control of cytoskeletal mechanics by extracellular matrix, cell shape, and mechanical tension. Biophys J 66: 2181-2189.
157. Wang N, Tolic-Norrelykke IM, Chen J, Mijailovich SM, Butler JP, Fredberg JJ, Stamenovic D (2002) Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. Am J Physiol Cell Physiol 282: C606-C616.
158. Wang N, Tytell JD, Ingber DE (2009b) Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 10: 75-82.
159. Wennerberg A, Albrektsson T (2010) On implant surfaces: a review of current knowledge and opinions. Int J Oral Maxillofac Implants 25: 63-74.
160. Wharton KA Jr (2003) Runnin' with the Dvl: proteins that associate with Dsh/Dvl and their significance to Wnt signal transduction. Dev Biol 253: 1-17.
161. Williams BO, Insogna KL (2009) Where Wnts went: the exploding field of Lrp5 and Lrp6 signaling in bone. J Bone Miner Res. 24:171-178.
162. Wozniak MA, Chen CS (2009) Mechanotransduction in development: a growing role for contractility. Nat Rev Mol Cell Biol 10: 34-43.
163. Xu W, Kimelman D (2007) Mechanistic insights from structural studies of beta-catenin and its binding partners. J Cell Sci 120: 3337-3344.
164. Young SR, Gerard-O'Riley R, Kim JB, Pavalko FM (2009) Focal adhesion kinase is important for fluid shear stress-induced mechanotransduction in osteoblasts. J Bone Miner Res. 24: 411-424.
165. Young SR, Hum JM, Rodenberg E, Turner CH, Pavalko FM (2011) Non-overlapping functions for Pyk2 and FAK in osteoblasts during fluid shear stress-induced mechanotransduction. PLoS One 6: e16026.
166. Yang F, Yang D, Tu J, Zheng Q, Cai L, Wang L (2011) Strontium enhances osteogenic differentiation of mesenchymal stem cells and in vivo bone formation by activating Wnt/catenin signaling. Stem Cells 29: 981-991.
167. Zhang C, Cho K, Huang Y, Lyons JP, Zhou X, Sinha K, McCrea PD, de Crombrugghe B (2008) Inhibition of Wnt signaling by the osteoblast-specific transcription factor Osterix. Proc Natl Acad Sci USA 105: 6936-6941.