Fibroblast growth factor and canonical WNT/β-catenin signaling cooperate in suppression of chondrocyte differentiation in experimental models of FGFR signaling in cartilage

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1852, Issue 5, 2015, Pages 839-850

  Buchtova, Marcela ^a,b   Oralova, Veronika ^b   Aklian, Anie ^c   Masek, Jan ^d   Vesela, Iva ^a   Ouyang, Zhufeng ^e   Obadalova, Tereza ^d   Konecna, Zaneta ^d   Spoustova, Tereza ^d   Pospisilova, Tereza ^d   Matula, Petr ^d   Varecha, Miroslav ^d   Balek, Lukas ^d   Gudernova, Iva ^d   Jelinkova, Iva ^d   Duran, Ivan ^f   Cervenkova, Iveta ^d   Murakami, Shunichi ^e   Kozubik, Alois ^d,g   Dvorak, Petr ^d   Bryja, Vitezslav ^d,g   Krejci, Pavel ^d,h   more..

^a UNIVERSITY OF VETERINARY AND PHARMACEUTICAL SCIENCES   (Czech Republic)

^b INSTITUTE OF ANIMAL PHYSIOLOGY AND GENETICS   (Czech Republic)

^c CEDARS SINAI MEDICAL CENTER   (United States)

^d MASARYK UNIVERSITY   (Czech Republic)

^e CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g INSTITUTE OF BIOPHYSICS   (Czech Republic)

^h ST ANNE S UNIVERSITY HOSPITAL   (Czech Republic)

Author keywords

Cartilage; Chondrocyte; Differentiation; FGFR3; Fibroblast growth factor receptor; WNT

Indexed keywords

BETA CATENIN; COLLAGEN; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; GUANOSINE TRIPHOSPHATASE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN CDC42; PROTEOGLYCAN; FIBROBLAST GROWTH FACTOR 2; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; LRP6 PROTEIN, MOUSE; TRANSCRIPTOME; WNT PROTEIN; WNT3A PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARTILAGE; CARTILAGE CELL; CELL ADHESION; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL SHAPE; CELL STRUCTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME INDUCTION; EXPERIMENTAL MOUSE; EXTRACELLULAR MATRIX; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSFECTION; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; LIMB; LIMB BUD; MOUSE; NONHUMAN; ORGAN CULTURE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TURNOVER TIME; WESTERN BLOTTING; WNT SIGNALING PATHWAY; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; DRUG POTENTIATION; EMBRYOLOGY; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

ANIMALS; BETA CATENIN; BLOTTING, WESTERN; CARTILAGE; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELLS, CULTURED; CHONDROCYTES; DRUG SYNERGISM; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTORS; HEK293 CELLS; HUMANS; LIMB BUDS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-6; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; RATS; RECEPTORS, FIBROBLAST GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTOME; WNT PROTEINS; WNT3A PROTEIN;

EID: 84922439626     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2014.12.020     Document Type: Article

References (61)

1. Provot S., Schipani E. Molecular mechanisms of endochondral bone development. Biochem. Biophys. Res. Commun. 2005, 328(3):658-665.
2. Colvin J.S., Bohne B.A., Harding G.W., McEwen D.G., Ornitz D.M. Skeletal overgrowth and deafness in mice lacking fibroblast growth factor receptor 3. Nat. Genet. 1996, 12(4):390-397.
3. Waller D.K., Correa A., Vo T.M., Wang Y., Hobbs C., et al. The population-based prevalence of achondroplasia and thanatophoric dysplasia in selected regions of the US. Am. J. Med. Genet. A 2008, 146A:2385-2389.
4. Foldynova-Trantirkova S., Wilcox W.R., Krejci Sixteen years and counting: the current understanding of fibroblast growth factor receptor 3 (FGFR3) signaling in skeletal dysplasias. Hum. Mutat. 2012, 33(1):29-41.
5. Kronenberg H.M. PTHrP and skeletal development. Ann. NY Acad. Sci. 2006, 1068:1-13.
6. Naski M.C., Colvin J.S., Coffin J.D., Ornitz D.M. Repression of hedgehog signaling and BMP4 expression in growth plate cartilage by fibroblast growth factor receptor 3. Development 1998, 125:4977-4988.
7. Chen L., Adar R., Yang X., Monsonego E.O., Li C., et al. Gly369Cys mutation in mouse FGFR3 causes achondroplasia by affecting both chondrogenesis and osteogenesis. J. Clin. Invest. 1999, 104(11):1517-1525.
8. Li C., Chen L., Iwata T., Kitagawa M., Fu X.Y., Deng C.X. A Lys644Glu substitution in fibroblast growth factor receptor 3 (FGFR3) causes dwarfism in mice by activation of STATs and ink4 cell cycle inhibitors. Hum. Mol. Genet. 1999, 8:35-44.
9. Yamanaka Y., Tanaka H., Koike M., Nishimura R., Seino Y. PTHrP rescues ATDC5 cells from apoptosis induced by FGF receptor 3 mutation. J. Bone Miner. Res. 2003, 18:1395-1403.
10. Krejci P., Aklian A., Kaucka M., Sevcikova E., Prochazkova J., et al. Receptor tyrosine kinases activate canonical WNT/beta-catenin signaling via MAP kinase/LRP6 pathway and direct beta-catenin phosphorylation. PLoS ONE 2012, 7(4):e35826.
11. Tamai K., Zeng X., Liu C., Zhang X., Harada Y., et al. A mechanism for Wnt coreceptor activation. Mol. Cell 2004, 13(1):149-156.
12. Andrade A.C., Nilsson O., Barnes K.M., Baron J. Wnt gene expression in the post-natal growth plate: regulation with chondrocyte differentiation. Bone 2007, 40(5):1361-1369.
13. Dong Y.F., Soung do Y., Schwarz E.M., O'Keefe R.J., Drissi H. Wnt induction of chondrocyte hypertrophy through the runx2 transcription factor. J. Cell. Physiol. 2006, 208(1):77-86.
14. Guo X., Mak K.K., Taketo M.M., Yang Y. The Wnt/beta-catenin pathway interacts differentially with PTHrP signaling to control chondrocyte hypertrophy and final maturation. PLoS ONE 2009, 4(6):e6067.
15. Mukhopadhyay K., Lefebvre V., Zhou G., Garofalo S., Kimura J.H., de Crombrugghe B. Use of a new rat chondrosarcoma cell line to delineate a 119-base pair chondrocyte-specific enhancer element and to define active promoter segments in the mouse pro-alpha 1(II) collagen gene. J. Biol. Chem. 1995, 270(46):27711-27719.
16. Krejci P., Bryja V., Pachernik J., Hampl A., Pogue R., et al. FGF2 inhibits proliferation and alters the cartilage-like phenotype of RCS cells. Exp. Cell Res. 2004, 297(1):152-164.
17. Rozenblatt-Rosen O., Mosonego-Ornan E., Sadot E., Madar-Shapiro L., Sheinin Y., et al. Induction of chondrocyte growth arrest by FGF: transcriptional and cytoskeletal alterations. J. Cell Sci. 2002, 115:553-562.
18. Daniels K., Reiter R., Solursh M. Micromass cultures of limb and other mesenchyme. Methods Cell Biol. 1996, 51:237-247.
19. Gay S.W., Kosher R.A. Uniform cartilage differentiation in micromass cultures prepared from a relatively homogeneous population of chondrogenic progenitor cells of the chick limb bud: effect of prostaglandins. J. Exp. Zool. 1984, 232(2):317-326.
20. Niehrs C., Shen J. Regulation of Lrp6 phosphorylation. Cell. Mol. Life Sci. 2010, 67:2551-2562.
21. Wolf J., Palmby T.R., Gavard J., Williams B.O., Gutkind J.S. Multiple PPPS/TP motifs act in a combinatorial fashion to transduce Wnt signaling through LRP6. FEBS Lett. 2008, 582:255-261.
22. Cervenka I., Wolf J., Masek J., Krejci P., Wilcox W.R., et al. Mitogen-activated protein kinases promote WNT/beta-catenin signaling via phosphorylation of LRP6. Mol. Cell. Biol. 2011, 31(1):179-189.
23. de Frutos C.A., Vega S., Manzanares M., Flores J.M., Huertas H., et al. Snail1 is a transcriptional effector of FGFR3 signaling during chondrogenesis and achondroplasias. Dev. Cell 2007, 13(6):872-883.
24. Lefebvre V., Huang W., Harley V.R., Goodfellow P.N., de Crombrugghe B. SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene. Mol. Cell. Biol. 1997, 4:2336-2346.
25. Pogue R., Lyons K. BMP signaling in the cartilage growth plate. Curr. Top. Dev. Biol. 2006, 76:1-48.
26. Vortkamp A., Lee K., Lanske B., Segre G.V., Kronenberg H.M., Tabin C.J. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 1996, 273(5275):613-622.
27. Wu S., Morrison A., Sun H., De Luca F. Nuclear factor-kappaB (NF-kappaB) p65 interacts with Stat5b in growth plate chondrocytes and mediates the effects of growth hormone on chondrogenesis and on the expression of insulin-like growth factor-1 and bone morphogenetic protein-2. J. Biol. Chem. 2011, 286(28):24726-24734.
28. Mello M.A., Tuan R.S. High density micromass cultures of embryonic limb bud mesenchymal cells: an in vitro model of endochondral skeletal development. In Vitro Cell. Dev. Biol. Anim. 1999, 35:262-269.
29. Sahni M., Ambrosetti D.C., Mansukhani A., Gertner R., Levy D., Basilico C. FGF signaling inhibits chondrocyte proliferation and regulates bone development through the STAT-1 pathway. Genes Dev. 1999, 13(11):1361-1366.
30. Krejci P., Masri B., Fontaine V., Mekikian P.B., Weis M., et al. Interaction of fibroblast growth factor and C-natriuretic peptide signaling in regulation of chondrocyte proliferation and extracellular matrix homeostasis. J. Cell Sci. 2005, 118(Pt 21):5089-5100.
31. Krejci P., Prochazkova J., Smutny J., Chlebova K., Lin P., et al. FGFR3 signaling induces a reversible senescence phenotype in chondrocytes similar to oncogene-induced premature senescence. Bone 2010, 47(1):102-110.
32. Malfait A.M., Liu R.Q., Ijiri K., Komiya S., Tortorella M.D. Inhibition of ADAM-TS4 and ADAM-TS5 prevents aggrecan degradation in osteoarthritic cartilage. J. Biol. Chem. 2002, 277(25):22201-22208.
33. Rodríguez-Manzaneque J.C., Westling J., Thai S.N., Luque A., Knauper V., et al. ADAMTS1 cleaves aggrecan at multiple sites and is differentially inhibited by metalloproteinase inhibitors. Biochem. Biophys. Res. Commun. 2002, 293(1):501-508.
34. Caterson B., Flannery C.R., Hughes C.E., Little C.B. Mechanisms involved in cartilage proteoglycan catabolism. Matrix Biol. 2000, 19(4):333-344.
35. Maeda M., Hasegawa H., Hyodo T., Ito S., Asano E., et al. ARHGAP18, a GTPase-activating protein for RhoA, controls cell shape, spreading, and motility. Mol. Biol. Cell 2011, 22(20):3840-3852.
36. Tang Y.A., Wen W.L., Chang J.W., Wei T.T., Tan Y.H., et al. A novel histone deacetylase inhibitor exhibits antitumor activity via apoptosis induction, F-actin disruption and gene acetylation in lung cancer. PLoS ONE 2010, 5(9):e12417.
37. Wong K., Ren X.R., Huang Y.Z., Xie Y., et al. Signal transduction in neuronal migration: roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell 2001, 107(2):209-221.
38. Tcherkezian J., Triki I., Stenne R., Danek E.I., Lamarche-Vane N. The human orthologue of CdGAP is a phosphoprotein and a GTPase-activating protein for Cdc42 and Rac1 but not RhoA. Biol. Cell. 2006, 98(8):445-456.
39. Kaibuchi K., Kuroda S., Amano M. Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu. Rev. Biochem. 1999, 68:459-486.
40. Narumiya S. The small GTPase Rho: cellular functions and signal transduction. J. Biochem. 1996, 120(2):215-228.
41. Schoenwaelder S.M., Burridge K. Bidirectional signaling between the cytoskeleton and integrins. Curr. Opin. Cell Biol. 1999, 11(2):274-286.
42. Nakamura K., Nishimura J., Hirano K., Ibayashi S., Fujishima M., Kanaide H. Hydroxyfasudil, an active metabolite of fasudil hydrochloride, relaxes the rabbit basilar artery by disinhibition of myosin light chain phosphatase. J. Cereb. Blood Flow Metab. 2001, 21(7):876-885.
43. Uehata M., Ishizaki T., Satoh H., Ono T., Kawahara T., et al. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 1997, 389(6654):990-994.
44. Diez M., Musri M.M., Ferrer E., Barbera J.A., Peinado V.I. Endothelial progenitor cells undergo an endothelial-to-mesenchymal transition-like process mediated by TGFbetaRI. Cardiovasc. Res. 2010, 88(3):502-511.
45. Kanazawa Y., Doi Y., Kudo H., Fujimoto S. Immunolocalization of fibronectin and its receptors integrin alpha 3 and alpha 5 subunits in the rat limb development. J. Electron. Microsc. (Tokyo) 1998, 47(1):87-92.
46. Mirza A., Foster L., Valentine H., Welch I., West C.M., Pritchard S. Investigation of the epithelial to mesenchymal transition markers S100A4, vimentin and Snail1 in gastroesophageal junction tumors. Dis. Esophagus 2012, 10.1111/j.1442-2050.2012.01435.x.
47. Sagi B., Maraghechi P., Urban V.S., Hegyi B., Szigeti A., et al. Positional identity of murine mesenchymal stem cells resident in different organs is determined in the postsegmentation mesoderm. Stem Cells Dev. 2012, 21(5):814-828.
48. Dailey L., Laplantine E., Priore R., Basilico C. A network of transcriptional and signaling events is activated by FGF to induce chondrocyte growth arrest and differentiation. J. Cell Biol. 2003, 161(6):1053-1066.
49. Horton W.A., Hood O.J., Machado M.A., Ahmed S., Griffey E.S. Abnormal ossification in thanatophoric dysplasia. Bone 1988, 9(1):53-61.
50. Chen L., Li C., Qiao W., Xu X., Deng C. A Ser(365)->Cys mutation of fibroblast growth factor receptor 3 in mouse downregulates Ihh/PTHrP signals and causes severe achondroplasia. Hum. Mol. Genet. 2001, 10:457-465.
51. Ornoy A., Adomian G.E., Eteson D.J., Burgeson R.E., Rimoin D.L. The role of mesenchyme-like tissue in the pathogenesis of thanatophoric dysplasia. Am. J. Med. Genet. 1985, 21(4):613-630.
52. Weizmann S., Tong A., Reich A., Genina O., Yayon A., Monsonego-Ornan E. FGF upregulates osteopontin in epiphyseal growth plate chondrocytes: implications for endochondral ossification. Matrix Biol. 2005, 24(8):520-529.
53. Kumar D., Lassar A.B. The transcriptional activity of Sox9 in chondrocytes is regulated by RhoA signaling and actin polymerization. Mol. Cell. Biol. 2009, 29(15):4262-4273.
54. Wang G., Woods A., Sabari S., Pagnotta L., Stanton L.A., Beier F. RhoA/ROCK signaling suppresses hypertrophic chondrocyte differentiation. J. Biol. Chem. 2004, 279(13):13205-13214.
55. Hill T.P., Spater D., Taketo M.M., Birchmeier W., Hartmann C. Canonical Wnt/beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev. Cell 2005, 8(5):727-738.
56. Ning B., Wang P., Pei X., Kang Y., Song J., et al. Dual function of beta-catenin in articular cartilage growth and degeneration at different stages of postnatal cartilage development. Int. Orthop. 2012, 36(3):655-664.
57. Tamamura Y., Otani T., Kanatani N., Koyama E., Kitagaki J., et al. Developmental regulation of Wnt/beta-catenin signals is required for growth plate assembly, cartilage integrity, and endochondral ossification. J. Biol. Chem. 2005, 280(19):19185-19195.
58. Zawel L., Dai J.L., Buckhaults P., Zhou S., Kinzler K.W., et al. Human Smad3 and Smad4 are sequence-specific transcription activators. Mol. Cell 1998, 1(4):611-617.
59. Horiguchi K., Shirakihara T., Nakano A., Imamura T., Miyazono K., Saitoh M. Role of Ras signaling in the induction of snail by transforming growth factor-beta. J. Biol. Chem. 2009, 284(1):245-253.
60. Lefebvre V., Zhou G., Mukhopadhyay K., Smith C.N., Zhang Z., et al. An 18-base-pair sequence in the mouse proalpha1(II) collagen gene is sufficient for expression in cartilage and binds nuclear proteins that are selectively expressed in chondrocytes. Mol. Cell. Biol. 1996, 16(8):4512-4523.
61. Sasaki H., Hui C., Nakafuku M., Kondoh H. A binding site for Gli proteins is essential for HNF-3beta floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 1997, 124(7):1313-1322.