Non-canonical Wnt signalling and N-cadherin related β-catenin signalling play a role in mechanically induced osteogenic cell fate

PLoS ONE

Volumn 4, Issue 4, 2009, Pages

  Arnsdorf, Emily J ^a,b   Tummala, Padmaja ^a   Jacobs, Christopher R ^a,b,c  

^a VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^b Stanford University   (United States)

^c Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; GUANOSINE TRIPHOSPHATASE; LYMPHOID ENHANCER FACTOR 1; NERVE CELL ADHESION MOLECULE; PROTEIN ROR2; RECEPTOR PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; T CELL FACTOR PROTEIN; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG; WNT PROTEIN; WNT5A PROTEIN; CADHERIN; CATNB PROTEIN, MOUSE; CDH2 PROTEIN, MOUSE; PROTEIN TYROSINE KINASE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA PROTEIN, MOUSE; ROR2 PROTEIN, MOUSE; SMALL INTERFERING RNA; WNT5A PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ASSAY; GENE TRANSLOCATION; GENETIC TRANSCRIPTION; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; OSCILLATION; OSTEOBLAST; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; BIOLOGICAL MODEL; BIOMECHANICS; BONE DEVELOPMENT; CELL JUNCTION; CELL LINE; CYTOLOGY; DRUG ANTAGONISM; GENETICS; MECHANICAL STRESS; MESENCHYMAL STEM CELL; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY;

ADHERENS JUNCTIONS; ANIMALS; BASE SEQUENCE; BETA CATENIN; BIOMECHANICS; CADHERINS; CELL DIFFERENTIATION; CELL LINE; MESENCHYMAL STEM CELLS; MICE; MODELS, BIOLOGICAL; OSTEOGENESIS; RECEPTOR PROTEIN-TYROSINE KINASES; RHO GTP-BINDING PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STRESS, MECHANICAL; WNT PROTEINS;

EID: 65549114494     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005388     Document Type: Article

References (84)

1. Turner CH (2006) Bone strength: current concepts. Ann N Y Acad Sci 1068: 429-46.
2. Carter DR, Beaupre GS, Giori NJ, Helms JA (1998) Mechanobiology of skeletal regeneration. Clin Orthop Relat Res 355: S41-55.
3. Carter DR, Orr TE, Fyhrie DP (1989) Relationships between loading history and femoral cancellous bone architecture. J Biomech 22: 231-44.
4. Brown TD, Pedersen DR, Gray ML, Brand RA, Rubin CT (1990) Toward an identification of mechanical parameters initiating periosteal remodeling: a combined experimental and analytic approach. J Biomech 23: 893-905.
5. Ruff C, Holt B, Trinkaus E (2006) Who's afraid of the big bad Wolff?: "Wolff's law" and bone functional adaptation. Am J Phys Anthropol 129: 484-98.
6. Wolff J (1986) The Law of Bone Remodeling. Berlin: Springer-Verlag.
7. Frost HM (1988) Vital biomechanics: proposed general concepts for skeletal adaptations to mechanical usage. Calcif Tissue Int 42: 145-56.
8. Dehority W, Halloran BP, Bikle DD, Curren T, Kostenuik PJ, et al. (1999) Bone and hormonal changes induced by skeletal unloading in the mature male rat. Am J Physiol 276: E62-9.
9. Lamb KJ, Lewthwaite JC, Lin JP, Simon D, Kavanagh E, et al. (2003) Diverse range of fixed positional deformities and bone growth restraint provoked by flaccid paralysis in embryonic chicks. Int J Exp Pathol 84: 191-9.
10. Frost HM (1987) The mechanostat: a proposed pathogenic mechanism of osteoporoses and the bone mass effects of mechanical and nonmechanical agents. Bone Miner 2: 73-85.
11. Krahl H, Michaelis U, Pieper HG, Quack G, Montag M (1994) Stimulation of bone growth through sports. A radiologic investigation of the upper extremities in professional tennis players. Am J Sports Med 22: 751-7.
12. Kitaori T, Ito H, Schwarz EM, Tsutsumi R, Yoshitomi H, et al. (2009) Stromal cell-derived factor 1/CXCR4 signaling is critical for the recruitment of mesenchymal stem cells to the fracture site during skeletal repair in a mouse model. Arthritis Rheum 60: 813-23.
13. Srinivasan S, Gross TS (2000) Canalicular fluid flow induced by bending of a long bone. Med Eng Phys 22: 127-33.
14. Steck R, Niederer P, Knothe Tate ML (2000) A finite difference model of load-induced fluid displacements within bone under mechanical loading. Med Eng Phys 22: 117-25.
15. Knothe Tate ML, Steck R, Forwood MR, Niederer P (2000) In vivo demonstration of load-induced fluid flow in the rat tibia and its potential implications for processes associated with functional adaptation. J Exp Biol 203: 2737-45.
16. Batra NN, Li YJ, Yellowley CE, You L, Malone AM, et al. (2005) Effects of short-term recovery periods on fluid-induced signaling in osteoblastic cells. J Biomech 38: 1909-17.
17. Saunders MM, You J, Zhou Z, Li Z, Yellowley CE, et al. (2003) Fluid flow-induced prostaglandin E2 response of osteoblastic ROS 17/2.8 cells is gap junction-mediated and independent of cytosolic calcium. Bone 32: 350-6.
18. Riddle RC, Taylor AF, Genetos DC, Donahue HJ (2006) MAP kinase and calcium signaling mediate fluid flow-induced human mesenchymal stem cell proliferation. Am J Physiol Cell Physiol 290: C776-84.
19. Triplett JW, O'Riley R, Tekulve K, Norvell SM, Pavalko FM (2007) Mechanical loading by fluid shear stress enhances IGF-1 receptor signaling in osteoblasts in a PKCzeta-dependent manner. Mol Cell Biomech 4: 13-25.
20. Kim CH, You L, Yellowley CE, Jacobs CR (2006) Oscillatory fluid flow-induced shear stress decreases osteoclastogenesis through RANKL and OPG signaling. Bone 39: 1043-7.
21. You J, Reilly GC, Zhen X, Yellowley CE, Chen Q, et al. (2001) 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: 13365-71.
22. Li YJ, Batra NN, You L, Meier SC, Coe IA, et al. (2004) Oscillatory fluid flow affects human marrow stromal cell proliferation and differentiation. J Orthop Res 22: 1283-9.
23. Arnsdorf EJ, Kwon RY, Jacobs CR (2009) Mechanically induced osteogenic differentiation - the role of RhoA, ROCKII and cytoskeletal dynamics. J Cell Sc 122: 546-53.
24. Chen Y, Whetstone HC, Youn A, Nadesan P, Chow EC, et al. (2007) Betacatenin signaling pathway is crucial for bone morphogenetic protein 2 to induce new bone formation. J Biol Chem 282: 526-33.
25. Baksh D, Tuan RS (2007) Canonical and non-canonical wnts differentially affect the development potential of primary isolate of human bone marrow mesenchymal stem cells. J Cell Physiol 212: 817-26.
26. Baksh D, Boland GM, Tuan RS (2007) Cross-talk between Wnt signaling pathways in human mesenchymal stem cells leads to functional antagonism during osteogenic differentiation. J Cell Biochem 101: 1109-24.
27. Morvan F, Boulukos K, Clement-Lacroix P, Roman Roman S, Suc-Royer I, et al. (2006) Deletion of a single allele of the Dkk1 gene leads to an increase in bone formation and bone mass. J Bone Miner Res 21: 934-45.
28. Rodda SJ, McMahon AP (2006) Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 133: 3231-44.
29. Wang FS, Ko JY, Lin CL, Wu HL, Ke HJ, et al. (2007) Knocking down dickkopf-1 alleviates estrogen deficiency induction of bone loss. A histomorphological study in ovariectomized rats. Bone 40: 485-92.
30. Semenov MV, He X (2006) LRP5 mutations linked to high bone mass diseases cause reduced LRP5 binding and inhibition by SOST. J Biol Chem 281: 38276-84.
31. Zou L, Zou X, Li H, Mygind T, Zeng Y, et al. (2006) Molecular mechanism of osteochondroprogenitor fate determination during bone formation. Adv Exp Med Biol 585: 431-41.
32. Krishnan V, Bryant HU, Macdougald OA (2006) Regulation of bone mass by Wnt signaling. J Clin Invest 116: 1202-9.
33. Spater D, Hill TP, Gruber M, Hartmann C (2006) Role of canonical Wnt-signalling in joint formation. Eur Cell Mater 12: 71-80.
34. Huang W, Yang S, Shao J, Li YP (2007) Signaling and transcriptional regulation in osteoblast commitment and differentiation. Front Biosci 12: 3068-92.
35. Zhong N, Gersch RP, Hadjiargyrou M (2006) Wnt signaling activation during bone regeneration and the role of Dishevelled in chondrocyte proliferation and differentiation. Bone 39: 5-16.
36. Bodine PV, Komm BS (2006) Wnt signaling and osteoblastogenesis. Rev Endocr Metab Disord 7: 33-9.
37. Baron R, Rawadi G, Roman-Roman S (2006) Wnt signaling: a key regulator of bone mass. Curr Top Dev Biol 76: 103-27.
38. Du SJ, Purcell SM, Christian JL, McGrew LL, Moon RT (1995) Identification of distinct classes and functional domains of Wnts through expression of wild-type and chimeric proteins in Xenopus embryos. Mol Cell Biol 15: 2625-34.
39. Kuhl M, Sheldahl LC, Park M, Miller JR, Moon RT (2000) The Wnt/Ca2+ pathway: a new vertebrate Wnt signaling pathway takes shape. Trends Genet 16: 279-83.
40. Toyofuku T, Hong Z, Kuzuya T, Tada M, Hori M (2000) Wnt/frizzled-2 signaling induces aggregation and adhesion among cardiac myocytes by increased cadherin-beta-catenin complex. J Cell Biol 150: 225-41.
41. Smith JC, Conlon FL, Saka Y, Tada M (2000) Xwnt11 and the regulation of gastrulation in Xenopus. Philos Trans R Soc Lond B Biol Sci 355: 923-30.
42. Katoh M, Katoh M (2006) Cross-talk of WNT and FGF signaling pathways at GSK3beta to regulate beta-catenin and SNAIL signaling cascades. Cancer Biol Ther 5: 1059-64.
43. Cadigan KM, Nusse R (1997) Wnt signaling: a common theme in animal development. Genes Dev 11: 3286-305.
44. Papkoff J, Rubinfeld B, Schryver B, Polakis P (1996) Wnt-1 regulates free pools of catenins and stabilizes APC-catenin complexes. Mol Cell Biol 16: 2128-34.
45. Taurin S, Sandbo N, Qin Y, Browning D, Dulin NO (2006) Phosphorylation of beta-catenin by cyclic AMP-dependent protein kinase. J Biol Chem 281: 9971-6.
46. Katoh Y, Katoh M(2005) Comparative genomics on Dkk1 orthologs. Int J Oncol 27: 275-9.
47. Reinhold MI, Naski MC (2007) Direct interactions of Runx2 and canonical Wnt signaling induce FGF18. J Biol Chem 282: 3653-63.
48. Chamorro MN, Schwartz DR, Vonica A, Brivanlou AH, Cho KR, et al. (2005) FGF-20 and DKK1 are transcriptional targets of beta-catenin and FGF-20 is implicated in cancer and development. Embo J 24: 73-84.
49. Shimokawa T, Furukawa Y, Sakai M, Li M, Miwa N, et al. (2003) Involvement of the FGF18 gene in colorectal carcinogenesis, as a novel downstream target of the beta-catenin/T-cell factor complex. Cancer Res 63: 6116-20.
50. He X, Semenov M, Tamai K, Zeng X (2004) LDL receptor-related proteins 5 and 6 in Wnt/beta-catenin signaling: arrows point the way. Development 131: 1663-77.
51. Boyden LM, Mao J, Belsky J, Mitzner L, Farhi A, et al. (2002) High bone density due to a mutation in LDL-receptor-related protein 5. N Engl J Med 346: 1513-21.
52. Gong Y, Slee RB, Fukai N, Rawadi G, Roman-Roman S, et al. (2001) LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 107: 513-23.
53. Gaur T, Lengner CJ, Hovhannisyan H, Bhat RA, Bodine PV, et al. (2005) Canonical WNT signaling promotes osteogenesis by directly stimulating Runx2 gene expression. J Biol Chem 280: 33132-40.
54. Goldring MB, Tsuchimochi K, Ijiri K (2006) The control of chondrogenesis. J Cell Biochem 97: 33-44.
55. Zhang C, Cho K, Huang Y, Lyons JP, Zhou X, et al. (2008) Inhibition of Wnt signaling by the osteoblast-specific transcription factor Osterix. PNAS 105: 6936-41.
56. Dong YF, Soung do Y, Schwarz EM, O'Keefe RJ, Drissi H (2006) Wnt induction of chondrocyte hypertrophy through the Runx2 transcription factor. J Cell Physiol 208: 77-86.
57. Kim JB, Leucht P, Lam K, Luppen C, Ten Berge D, et al. (2007) Bone regeneration is regulated by wnt signaling. J Bone Miner Res 22: 1913-23.
58. Nelson WJ, Nusse R (2004) Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303: 1483-7.
59. Wang Y, Volloch V, Pindrus MA, Blasioli DJ, Chen J, et al. (2007) Murine osteoblasts regulate mesenchymal stem cells via WNT and cadherin pathways: mechanism depends on cell-cell contact mode. J Tissue Eng Regen Med 1: 39-50.
60. Tuli R, Tuli S, Nandi S, Huang X, Manner PA, et al. (2003) Transforming growth factor-beta-mediated chondrogenesis of human mesenchymal progenitor cells involves N-cadherin and mitogen-activated protein kinase and Wnt signaling cross-talk. J Biol Chem 278: 41227-36.
61. Orsulic S, Huber O, Aberle H, Arnold S, Kemler R (1999) E-cadherin binding prevents beta-catenin nuclear localization and beta-catenin/ LEF-1-mediated transactivation. J Cell Sci 112: 1237-45.
62. Aberle H, Schwartz H, Kemler R (1996) Cadherin-catenin complex: protein interactions and their implications for cadherin function. J Cell Biochem 61: 514-23.
63. Katoh M (2005) WNT/PCP signaling pathway and human cancer. Oncol Rep 14: 1583-8.
64. 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: 483-95.
65. Woods A, Beier F (2006) RhoA/ROCK signaling regulates chondrogenesis in a context-dependent manner. J Biol Chem 281: 13134-40.
66. Woods A, Wang G, Beier F (2005) RhoA/ROCK signaling regulates Sox9 expression and actin organization during chondrogenesis. J Biol Chem 280: 11626-34.
67. Liu Y, Bhat RA, Seestaller-Wehr LM, Fukayama S, Mangine A, et al. (2007) The orphan receptor tyrosine kinase Ror2 promotes osteoblast differentiation and enhances ex vivo bone formation. Mol Endocrinol 21: 376-87.
68. Liu Y, Bodine PV, Billiard J (2007) Ror2, a novel modulator of osteogenesis. J Musculoskelet Neuronal Interact 7: 323-4.
69. Zhu S, Liu L, Korzh V, Gong Z, Low BC (2006) RhoA acts downstream of Wnt5 and Wnt11 to regulate convergence and extension movements by involving effectors Rho kinase and Diaphanous: use of zebrafish as an in vivo model for GTPase signaling. Cell Signal 18: 359-72.
70. Mikels AJ, Nusse R (2006) Purified Wnt5a protein activates or inhibits betacatenin-TCF signaling depending on receptor context. PLoS Biol 4: e115.
71. Jacobs CR, Yellowley CE, Davis BR, Zhou Z, Cimbala JM, et al. (1998) Differential effect of steady versus oscillating flow on bone cells. J Biomech 31: 969-76.
72. Ren XD, Schwartz MA (2000) Determination of GTP loading on Rho. Methods Enzymol 325: 264-72.
73. Hanai J, Gloy J, Karumanchi SA, Kale S, Tang J, et al. (2002) Endostatin is a potential inhibitor of Wnt signaling. JCB 158: 529-39.
74. Norvell SM, Alvarez M, Bidwell JP, Pavalko FM (2004) Fluid shear stress induces beta-catenin signaling in osteoblasts. Calcif Tissue Int 75: 396-404.
75. Pavalko FM, Norvell SM, Burr DB, Turner CH, Duncan RL, et al. (2003) A model for mechanotransduction in bone cells: the load-bearing mechanosomes. J Cell Biochem 88: 104-12.
76. Bain G, Muller T, Wang X, Papkoff J (2003) Activated beta-catenin induces osteoblast differentiation of C3H10T1/2 cells and participates in BMP2 mediated signal transduction. Biochem Biophys Res Commun 301: 84-91.
77. El-Tanani M, Barraclough R, Wilkinson MC, Rudland PS (2001) Metastasis-inducing dna regulates the expression of the osteopontin gene by binding the transcription factor Tcf-4. Cancer Res 61: 5619-29.
78. Muller T, Bain G, Wang X, Papkoff J (2002) Regulation of epithelial cell migration and tumor formation by beta-catenin signaling. Exp Cell Res 280: 119-33.
79. Oberlender SA, Tuan RS (1994) Expression and functional involvement of N-cadherin in embryonic limb chondrogenesis. Development 120: 177-87.
80. Oberlender SA, Tuan RS (1994) Spatiotemporal profile of N-cadherin expression in the developing limb mesenchyme. Cell Adhes Commun 2: 521-37.
81. Ganz A, Lambert M, Saez A, Silberzan P, Buguin A, et al. (2006) Traction forces exerted through N-cadherin contacts. Biol Cell 98: 721-30.
82. Haÿ E, Laplantine E, Geoffroy V, Frain M, Kohler T, et al. (2009) N-cadherin interacts with axin and LRP5 to negatively regulate Wnt/ beta-catenin signaling, osteoblast function, and bone formation. Mol Cell Biol 20: 953-64.
83. Wu X, Tu X, Joeng KS, Hilton MJ, Williams DA, et al. (2008) Rac1 activation controls nuclear localization of beta-catenin during canonical Wnt signaling. Cell 133: 340-53.
84. Woods A, Wang G, Dupuis H, Shao Z, Beier F (2007) Rac1 signaling stimulates N-cadherin expression, mesenchymal condensation, and chondrogenesis. J Biol Chem 282: 23500-8.