Fibroblast growth factor signalling in osteoarthritis and cartilage repair.

Animals Cartilage, Articular / metabolism Clinical Trials as Topic Disease Progression Fibroblast Growth Factors / metabolism Homeostasis / physiology Humans Mice Models, Animal Osteoarthritis / metabolism Receptor, Fibroblast Growth Factor, Type 1 / antagonists & inhibitors Receptor, Fibroblast Growth Factor, Type 3 / agonists Signal Transduction / physiology

Journal

Nature reviews. Rheumatology
ISSN: 1759-4804
Titre abrégé: Nat Rev Rheumatol
Pays: United States
ID NLM: 101500080

Informations de publication

Date de publication:
10 2020
Historique:
accepted: 02 07 2020
pubmed: 19 8 2020
medline: 28 1 2021
entrez: 19 8 2020
Statut: ppublish

Résumé

Regulated fibroblast growth factor (FGF) signalling is a prerequisite for the correct development and homeostasis of articular cartilage, as evidenced by the fact that aberrant FGF signalling contributes to the maldevelopment of joints and to the onset and progression of osteoarthritis. Of the four FGF receptors (FGFRs 1-4), FGFR1 and FGFR3 are strongly implicated in osteoarthritis, and FGFR1 antagonists, as well as agonists of FGFR3, have shown therapeutic efficacy in mouse models of spontaneous and surgically induced osteoarthritis. FGF18, a high affinity ligand for FGFR3, is the only FGF-based drug currently in clinical trials for osteoarthritis. This Review covers the latest advances in our understanding of the molecular mechanisms that regulate FGF signalling during normal joint development and in the pathogenesis of osteoarthritis. Strategies for FGF signalling-based treatment of osteoarthritis and for cartilage repair in animal models and clinical trials are also introduced. An improved understanding of FGF signalling from a structural biology perspective, and of its roles in skeletal development and diseases, could unlock new avenues for discovery of modulators of FGF signalling that can slow or stop the progression of osteoarthritis.

Identifiants

DOI: 10.1038/s41584-020-0469-2 PMID: 32807927
pubmed: 32807927
doi: 10.1038/s41584-020-0469-2
pii: 10.1038/s41584-020-0469-2
doi:

Substances chimiques

fibroblast growth factor 18 0
Fibroblast Growth Factors 62031-54-3
Receptor, Fibroblast Growth Factor, Type 1 EC 2.7.10.1
Receptor, Fibroblast Growth Factor, Type 3 EC 2.7.10.1

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

547-564

Références

Huey, D. J., Hu, J. C. & Athanasiou, K. A. Unlike bone, cartilage regeneration remains elusive. Science 338, 917–921 (2012).
pubmed: 23161992 pmcid: 4327988 doi: 10.1126/science.1222454
Zhang, Y. & Jordan, J. M. Epidemiology of osteoarthritis. Clin. Geriatr. Med. 26, 355–369 (2010).
pubmed: 20699159 pmcid: 2920533 doi: 10.1016/j.cger.2010.03.001
Allen, K. D. & Golightly, Y. M. State of the evidence. Curr. Opin. Rheumatol. 27, 276–283 (2015).
pubmed: 25775186 pmcid: 4405030 doi: 10.1097/BOR.0000000000000161
Wallace, I. J. et al. Knee osteoarthritis has doubled in prevalence since the mid-20th century. Proc. Natl Acad. Sci. USA 114, 9332–9336 (2017).
pubmed: 28808025 doi: 10.1073/pnas.1703856114
Martel-Pelletier, J. et al. Osteoarthritis. Nat. Rev. Dis. Prim. 2, 16072 (2016).
pubmed: 27734845 doi: 10.1038/nrdp.2016.72
Roemer, F. W. et al. Presence of MRI-detected joint effusion and synovitis increases the risk of cartilage loss in knees without osteoarthritis at 30-month follow-up: the MOST study. Ann. Rheum. Dis. 70, 1804–1809 (2011).
pubmed: 21791448 pmcid: 3496084 doi: 10.1136/ard.2011.150243
Liu-Bryan, R. & Terkeltaub, R. Emerging regulators of the inflammatory process in osteoarthritis. Nat. Rev. Rheumatol. 11, 35–44 (2015).
pubmed: 25266449 doi: 10.1038/nrrheum.2014.162
Hunter, D. J. & Bierma-Zeinstra, S. Osteoarthritis. Lancet 393, 1745–1759 (2019).
doi: 10.1016/S0140-6736(19)30417-9
Bijlsma, J. W., Berenbaum, F. & Lafeber, F. P. Osteoarthritis: an update with relevance for clinical practice. Lancet 377, 2115–2126 (2011).
pubmed: 21684382 doi: 10.1016/S0140-6736(11)60243-2
Kwon, H. et al. Surgical and tissue engineering strategies for articular cartilage and meniscus repair. Nat. Rev. Rheumatol. 15, 550–570 (2019).
pubmed: 31296933 pmcid: 7192556 doi: 10.1038/s41584-019-0255-1
Tiku, M. L. & Sabaawy, H. E. Cartilage regeneration for treatment of osteoarthritis: a paradigm for nonsurgical intervention. Ther. Adv. Musculoskelet. Dis. 7, 76–87 (2015).
pubmed: 26029269 pmcid: 4426098 doi: 10.1177/1759720X15576866
Mastbergen, S. C., Saris, D. B. & Lafeber, F. P. Functional articular cartilage repair: here, near, or is the best approach not yet clear? Nat. Rev. Rheumatol. 9, 277–290 (2013).
pubmed: 23507899 doi: 10.1038/nrrheum.2013.29 pmcid: 23507899
Chijimatsu, R. & Saito, T. Mechanisms of synovial joint and articular cartilage development. Cell. Mol. Life Sci. 76, 3939–3952 (2019).
pubmed: 31201464 doi: 10.1007/s00018-019-03191-5 pmcid: 31201464
Ellman, M. B. et al. Fibroblast growth factor control of cartilage homeostasis. J. Cell. Biochem. 114, 735–742 (2013).
pubmed: 23060229 pmcid: 3690116 doi: 10.1002/jcb.24418
Su, N., Jin, M. & Chen, L. Role of FGF/FGFR signaling in skeletal development and homeostasis: learning from mouse models. Bone Res. 2, 14003 (2014).
pubmed: 26273516 pmcid: 4472122 doi: 10.1038/boneres.2014.3
Ornitz, D. M. & Marie, P. J. Fibroblast growth factor signaling in skeletal development and disease. Genes Dev. 29, 1463–1486 (2015).
pubmed: 26220993 pmcid: 4526732 doi: 10.1101/gad.266551.115
Beenken, A. & Mohammadi, M. The FGF family: biology, pathophysiology and therapy. Nat. Rev. Drug. Discov. 8, 235–253 (2009).
pubmed: 19247306 pmcid: 3684054 doi: 10.1038/nrd2792
Itoh, N. & Ornitz, D. M. Fibroblast growth factors: from molecular evolution to roles in development, metabolism and disease. J. Biochem. 149, 121–130 (2011).
pubmed: 20940169 doi: 10.1093/jb/mvq121 pmcid: 20940169
Goetz, R. et al. Molecular insights into the klotho-dependent, endocrine mode of action of fibroblast growth factor 19 subfamily members. Mol. Cell Biol. 27, 3417–3428 (2007).
pubmed: 17339340 pmcid: 1899957 doi: 10.1128/MCB.02249-06
Belov, A. A. & Mohammadi, M. Molecular mechanisms of fibroblast growth factor signaling in physiology and pathology. Cold Spring Harb. Perspect. Biol. 5, a015958 (2013).
pubmed: 23732477 pmcid: 3660835 doi: 10.1101/cshperspect.a015958
Plotnikov, A. N., Schlessinger, J., Hubbard, S. R. & Mohammadi, M. Structural basis for FGF receptor dimerization and activation. Cell 98, 641–650 (1999).
pubmed: 10490103 doi: 10.1016/S0092-8674(00)80051-3 pmcid: 10490103
Mohammadi, M., Olsen, S. K. & Ibrahimi, O. A. Structural basis for fibroblast growth factor receptor activation. Cytokine Growth Factor Rev. 16, 107–137 (2005).
pubmed: 15863029 doi: 10.1016/j.cytogfr.2005.01.008 pmcid: 15863029
Stauber, D. J., DiGabriele, A. D. & Hendrickson, W. A. Structural interactions of fibroblast growth factor receptor with its ligands. Proc. Natl Acad. Sci. USA 97, 49–54 (2000).
pubmed: 10618369 doi: 10.1073/pnas.97.1.49 pmcid: 10618369
Kalinina, J. et al. The alternatively spliced acid box region plays a key role in FGF receptor autoinhibition. Structure 20, 77–88 (2012).
pubmed: 22244757 pmcid: 3378326 doi: 10.1016/j.str.2011.10.022
Olsen, S. K. et al. Insights into the molecular basis for fibroblast growth factor receptor autoinhibition and ligand-binding promiscuity. Proc. Natl Acad. Sci. USA 101, 935–940 (2004).
pubmed: 14732692 doi: 10.1073/pnas.0307287101 pmcid: 14732692
Fantl, W. J., Johnson, D. E. & Williams, L. T. Signalling by receptor tyrosine kinases. Annu. Rev. Biochem. 62, 453–481 (1993).
pubmed: 7688944 doi: 10.1146/annurev.bi.62.070193.002321 pmcid: 7688944
Givol, D. & Yayon, A. Complexity of FGF receptors: genetic basis for structural diversity and functional specificity. FASEB J. 6, 3362–3369 (1992).
pubmed: 1464370 doi: 10.1096/fasebj.6.15.1464370 pmcid: 1464370
Ornitz, D. M. et al. Receptor specificity of the fibroblast growth factor family. J. Biol. Chem. 271, 15292–15297 (1996).
pubmed: 8663044 doi: 10.1074/jbc.271.25.15292 pmcid: 8663044
Zhang, X. et al. Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J. Biol. Chem. 281, 15694–15700 (2006).
pubmed: 16597617 pmcid: 2080618 doi: 10.1074/jbc.M601252200
Schlessinger, J. et al. Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol. Cell 6, 743–750 (2000).
pubmed: 11030354 doi: 10.1016/S1097-2765(00)00073-3
Asada, M. et al. Glycosaminoglycan affinity of the complete fibroblast growth factor family. Biochim. Biophys. Acta 1790, 40–48 (2009).
pubmed: 18835578 doi: 10.1016/j.bbagen.2008.09.001
Sarrazin, S., Lamanna, W. C. & Esko, J. D. Heparan sulfate proteoglycans. Cold Spring Harb. Perspect. Biol. 3, a004952 (2011).
pubmed: 21690215 pmcid: 3119907 doi: 10.1101/cshperspect.a004952
Goetz, R. et al. Conversion of a paracrine fibroblast growth factor into an endocrine fibroblast growth factor. J. Biol. Chem. 287, 29134–29146 (2012).
pubmed: 22733815 pmcid: 3436551 doi: 10.1074/jbc.M112.342980
Goetz, R. & Mohammadi, M. Exploring mechanisms of FGF signalling through the lens of structural biology. Nat. Rev. Mol. Cell Biol. 14, 166–180 (2013).
pubmed: 23403721 pmcid: 3695728 doi: 10.1038/nrm3528
Itoh, N., Ohta, H. & Konishi, M. Endocrine FGFs: evolution, physiology, pathophysiology, and pharmacotherapy. Front. Endocrinol. 6, 154 (2015).
doi: 10.3389/fendo.2015.00154
Beenken, A. & Mohammadi, M. The structural biology of the FGF19 subfamily. Adv. Exp. Med. Biol. 728, 1–24 (2012).
pubmed: 22396159 pmcid: 3682411 doi: 10.1007/978-1-4614-0887-1_1
Kurosu, H. et al. Regulation of fibroblast growth factor-23 signaling by klotho. J. Biol. Chem. 281, 6120–6123 (2006).
pubmed: 16436388 pmcid: 2637204 doi: 10.1074/jbc.C500457200
Urakawa, I. et al. Klotho converts canonical FGF receptor into a specific receptor for FGF23. Nature 444, 770–774 (2006).
pubmed: 17086194 doi: 10.1038/nature05315
Goetz, R. et al. Isolated C-terminal tail of FGF23 alleviates hypophosphatemia by inhibiting FGF23-FGFR-klotho complex formation. Proc. Natl Acad. Sci. USA 107, 407–412 (2010).
pubmed: 19966287 doi: 10.1073/pnas.0902006107
Henrissat, B. & Davies, G. Structural and sequence-based classification of glycoside hydrolases. Curr. Opin. Struct. Biol. 7, 637–644 (1997).
pubmed: 9345621 doi: 10.1016/S0959-440X(97)80072-3
Chen, G. et al. α-Klotho is a non-enzymatic molecular scaffold for FGF23 hormone signalling. Nature 553, 461–466 (2018).
pubmed: 29342138 pmcid: 6007875 doi: 10.1038/nature25451
Ogawa, Y. et al. βKlotho is required for metabolic activity of fibroblast growth factor 21. Proc. Natl Acad. Sci. USA 104, 7432–7437 (2007).
pubmed: 17452648 doi: 10.1073/pnas.0701600104
Kurosu, H. et al. Tissue-specific expression of βklotho and fibroblast growth factor (FGF) receptor isoforms determines metabolic activity of FGF19 and FGF21. J. Biol. Chem. 282, 26687–26695 (2007).
pubmed: 17623664 pmcid: 2496965 doi: 10.1074/jbc.M704165200
Makarenkova, H. P. et al. Differential interactions of FGFs with heparan sulfate control gradient formation and branching morphogenesis. Sci. Signal. 2, ra55 (2009).
pubmed: 19755711 pmcid: 2884999 doi: 10.1126/scisignal.2000304
Zinkle, A. & Mohammadi, M. Structural biology of the FGF7 subfamily. Front. Genet. 10, 102 (2019).
pubmed: 30809251 pmcid: 6379346 doi: 10.3389/fgene.2019.00102
Huang, Z. et al. Uncoupling the mitogenic and metabolic functions of FGF1 by tuning FGF1-FGF receptor dimer stability. Cell Rep. 20, 1717–1728 (2017).
pubmed: 28813681 pmcid: 5821125 doi: 10.1016/j.celrep.2017.06.063
Zinkle, A. & Mohammadi, M. A threshold model for receptor tyrosine kinase signaling specificity and cell fate determination. F1000Research 7, 872 (2018).
doi: 10.12688/f1000research.14143.1
Scotet, E. & Houssaint, E. The choice between alternative IIIb and IIIc exons of the FGFR-3 gene is not strictly tissue-specific. Biochim. Biophys. Acta 1264, 238–242 (1995).
pubmed: 7495869 doi: 10.1016/0167-4781(95)00156-B
Murgue, B., Tsunekawa, S., Rosenberg, I., de Beaumont, M. & Podolsky, D. K. Identification of a novel variant form of fibroblast growth factor receptor 3 (FGFR3 IIIb) in human colonic epithelium. Cancer Res. 54, 5206–5211 (1994).
pubmed: 7923141
Plotnikov, A. N., Hubbard, S. R., Schlessinger, J. & Mohammadi, M. Crystal structures of two FGF-FGFR complexes reveal the determinants of ligand-receptor specificity. Cell 101, 413–424 (2000).
pubmed: 10830168 doi: 10.1016/S0092-8674(00)80851-X
Yeh, B. K. et al. Structural basis by which alternative splicing confers specificity in fibroblast growth factor receptors. Proc. Natl Acad. Sci. USA 100, 2266–2271 (2003).
pubmed: 12591959 doi: 10.1073/pnas.0436500100
Olsen, S. K. et al. Structural basis by which alternative splicing modulates the organizer activity of FGF8 in the brain. Genes Dev. 20, 185–198 (2006).
pubmed: 16384934 pmcid: 1356110 doi: 10.1101/gad.1365406
Liu, Y. et al. Regulation of receptor binding specificity of FGF9 by an autoinhibitory homodimerization. Structure 25, 1325–1336.e3 (2017).
pubmed: 28757146 pmcid: 5587394 doi: 10.1016/j.str.2017.06.016
Ornitz, D. M. & Itoh, N. The fibroblast growth factor signaling pathway. Wiley Interdiscip. Rev. Dev. Biol. 4, 215–266 (2015).
pubmed: 25772309 pmcid: 4393358 doi: 10.1002/wdev.176
Bae, J. H. et al. Asymmetric receptor contact is required for tyrosine autophosphorylation of fibroblast growth factor receptor in living cells. Proc. Natl Acad. Sci. USA 107, 2866–2871 (2010).
pubmed: 20133753 doi: 10.1073/pnas.0914157107
Chen et al. Molecular basis for receptor tyrosine kinase A-loop tyrosine transphosphorylation. Nat. Chem. Biol. 16, 267–277 (2020).
pubmed: 31959966 pmcid: 7040854 doi: 10.1038/s41589-019-0455-7
Mohammadi, M., Schlessinger, J. & Hubbard, S. R. Structure of the FGF receptor tyrosine kinase domain reveals a novel autoinhibitory mechanism. Cell 86, 577–587 (1996).
pubmed: 8752212 doi: 10.1016/S0092-8674(00)80131-2
Chen, H. et al. A molecular brake in the kinase hinge region regulates the activity of receptor tyrosine kinases. Mol. Cell 27, 717–730 (2007).
pubmed: 17803937 pmcid: 2094128 doi: 10.1016/j.molcel.2007.06.028
Eswarakumar, V. P., Lax, I. & Schlessinger, J. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev. 16, 139–149 (2005).
pubmed: 15863030 doi: 10.1016/j.cytogfr.2005.01.001
Mohammadi, M. et al. A tyrosine-phosphorylated carboxy-terminal peptide of the fibroblast growth factor receptor (Flg) is a binding site for the SH2 domain of phospholipase C-gamma 1. Mol. Cell Biol. 11, 5068–5078 (1991).
pubmed: 1656221 pmcid: 361508 doi: 10.1128/MCB.11.10.5068
Peters, K. G., Werner, S., Chen, G. & Williams, L. T. Two FGF receptor genes are differentially expressed in epithelial and mesenchymal tissues during limb formation and organogenesis in the mouse. Development 114, 233–243 (1992).
pubmed: 1315677
Newton, A. C. Protein kinase C: structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions. Chem. Rev. 101, 2353–2364 (2001).
pubmed: 11749377 doi: 10.1021/cr0002801
Rosse, C. et al. PKC and the control of localized signal dynamics. Nat. Rev. Mol. Cell Biol. 11, 103–112 (2010).
pubmed: 20094051 doi: 10.1038/nrm2847
Igumenova, T. I. Dynamics and membrane interactions of protein kinase C. Biochemistry 54, 4953–4968 (2015).
pubmed: 26214365 pmcid: 4979571 doi: 10.1021/acs.biochem.5b00565
Turner, N. & Grose, R. Fibroblast growth factor signalling: from development to cancer. Nat. Rev. Cancer 10, 116–129 (2010).
pubmed: 20094046 doi: 10.1038/nrc2780
Shin, E. Y. et al. Basic fibroblast growth factor stimulates activation of Rac1 through a p85 βPIX phosphorylation-dependent pathway. J. Biol. Chem. 279, 1994–2004 (2004).
pubmed: 14557270 doi: 10.1074/jbc.M307330200
Lee, J. G. & Kay, E. P. FGF-2-induced wound healing in corneal endothelial cells requires Cdc42 activation and Rho inactivation through the phosphatidylinositol 3-kinase pathway. Invest. Ophthalmol. Vis. Sci. 47, 1376–1386 (2006).
pubmed: 16565371 doi: 10.1167/iovs.05-1223
Schlessinger, J. Phospholipase Cγ activation and phosphoinositide hydrolysis are essential for embryonal development. Proc. Natl Acad. Sci. USA 94, 2798–2799 (1997).
pubmed: 9096299 doi: 10.1073/pnas.94.7.2798
Ellis, M. V. et al. Catalytic domain of phosphoinositide-specific phospholipase C (PLC). Mutational analysis of residues within the active site and hydrophobic ridge of PLCδ1. J. Biol. Chem. 273, 11650–11659 (1998).
pubmed: 9565585 doi: 10.1074/jbc.273.19.11650
Kolch, W. et al. Protein kinase Cα activates RAF-1 by direct phosphorylation. Nature 364, 249–252 (1993).
pubmed: 8321321 doi: 10.1038/364249a0
Bunney, T. D. et al. Structural and functional integration of the PLCγ interaction domains critical for regulatory mechanisms and signaling deregulation. Structure 20, 2062–2075 (2012).
pubmed: 23063561 pmcid: 3532599 doi: 10.1016/j.str.2012.09.005
Hajicek, N., Charpentier, T. H., Rush, J. R., Harden, T. K. & Sondek, J. Autoinhibition and phosphorylation-induced activation of phospholipase C-γ isozymes. Biochemistry 52, 4810–4819 (2013).
pubmed: 23777354 doi: 10.1021/bi400433b
Poulin, B., Sekiya, F. & Rhee, S. G. Intramolecular interaction between phosphorylated tyrosine-783 and the C-terminal Src homology 2 domain activates phospholipase C-γ1. Proc. Natl Acad. Sci. USA 102, 4276–4281 (2005).
pubmed: 15764700 doi: 10.1073/pnas.0409590102
Huang, Z. et al. Two FGF receptor kinase molecules act in concert to recruit and transphosphorylate phospholipase Cγ. Mol. Cell 61, 98–110 (2016).
pubmed: 26687682 doi: 10.1016/j.molcel.2015.11.010
Wang, J. K., Xu, H., Li, H. C. & Goldfarb, M. Broadly expressed SNT-like proteins link FGF receptor stimulation to activators of Ras. Oncogene 13, 721–729 (1996).
pubmed: 8761293
Kouhara, H. et al. A lipid-anchored Grb2-binding protein that links FGF-receptor activation to the Ras/MAPK signaling pathway. Cell 89, 693–702 (1997).
doi: 10.1016/S0092-8674(00)80252-4
Hadari, Y. R., Kouhara, H., Lax, I. & Schlessinger, J. Binding of Shp2 tyrosine phosphatase to FRS2 is essential for fibroblast growth factor-induced PC12 cell differentiation. Mol. Cell Biol. 18, 3966–3973 (1998).
pubmed: 9632781 pmcid: 108981 doi: 10.1128/MCB.18.7.3966
Gotoh, N. Regulation of growth factor signaling by FRS2 family docking/scaffold adaptor proteins. Cancer Sci. 99, 1319–1325 (2008).
pubmed: 18452557 doi: 10.1111/j.1349-7006.2008.00840.x
Xu, H., Lee, K. W. & Goldfarb, M. Novel recognition motif on fibroblast growth factor receptor mediates direct association and activation of SNT adapter proteins. J. Biol. Chem. 273, 17987–17990 (1998).
pubmed: 9660748 doi: 10.1074/jbc.273.29.17987
Ong, S. H. et al. FRS2 proteins recruit intracellular signaling pathways by binding to diverse targets on fibroblast growth factor and nerve growth factor receptors. Mol. Cell Biol. 20, 979–989 (2000).
pubmed: 10629055 pmcid: 85215 doi: 10.1128/MCB.20.3.979-989.2000
Cha, J. Y., Maddileti, S., Mitin, N., Harden, T. K. & Der, C. J. Aberrant receptor internalization and enhanced FRS2-dependent signaling contribute to the transforming activity of the fibroblast growth factor receptor 2 IIIb C3 isoform. J. Biol. Chem. 284, 6227–6240 (2009).
pubmed: 19103595 pmcid: 2649112 doi: 10.1074/jbc.M803998200
Dhalluin, C. et al. Structural basis of SNT PTB domain interactions with distinct neurotrophic receptors. Mol. Cell 6, 921–929 (2000).
pubmed: 11090629 pmcid: 5155437 doi: 10.1016/S1097-2765(05)00087-0
Chardin, P. et al. Human Sos1: a guanine nucleotide exchange factor for Ras that binds to GRB2. Science 260, 1338–1343 (1993).
pubmed: 8493579 doi: 10.1126/science.8493579
Li, N. et al. Guanine-nucleotide-releasing factor hSos1 binds to Grb2 and links receptor tyrosine kinases to Ras signalling. Nature 363, 85–88 (1993).
pubmed: 8479541 doi: 10.1038/363085a0
Simon, J. A. & Schreiber, S. L. Grb2 SH3 binding to peptides from Sos: evaluation of a general model for SH3-ligand interactions. Chem. Biol. 2, 53–60 (1995).
pubmed: 9383403 doi: 10.1016/1074-5521(95)90080-2
Schaeper, U. et al. Coupling of Gab1 to c-Met, Grb2, and Shp2 mediates biological responses. J. Cell Biol. 149, 1419–1432 (2000).
pubmed: 10871282 pmcid: 2175135 doi: 10.1083/jcb.149.7.1419
Ong, S. H. et al. Stimulation of phosphatidylinositol 3-kinase by fibroblast growth factor receptors is mediated by coordinated recruitment of multiple docking proteins. Proc. Natl Acad. Sci. USA 98, 6074–6079 (2001).
pubmed: 11353842 doi: 10.1073/pnas.111114298
Lock, L. S., Royal, I., Naujokas, M. A. & Park, M. Identification of an atypical Grb2 carboxyl-terminal SH3 domain binding site in Gab docking proteins reveals Grb2-dependent and -independent recruitment of Gab1 to receptor tyrosine kinases. J. Biol. Chem. 275, 31536–31545 (2000).
pubmed: 10913131 doi: 10.1074/jbc.M003597200
Lamothe, B. et al. The docking protein Gab1 is an essential component of an indirect mechanism for fibroblast growth factor stimulation of the phosphatidylinositol 3-kinase/Akt antiapoptotic pathway. Mol. Cell Biol. 24, 5657–5666 (2004).
pubmed: 15199124 pmcid: 480891 doi: 10.1128/MCB.24.13.5657-5666.2004
Rodrigues, G. A., Falasca, M., Zhang, Z., Ong, S. H. & Schlessinger, J. A novel positive feedback loop mediated by the docking protein Gab1 and phosphatidylinositol 3-kinase in epidermal growth factor receptor signaling. Mol. Cell Biol. 20, 1448–1459 (2000).
pubmed: 10648629 pmcid: 85307 doi: 10.1128/MCB.20.4.1448-1459.2000
Faes, S. & Dormond, O. PI3K and AKT: unfaithful partners in cancer. Int. J. Mol. Sci. 16, 21138–21152 (2015).
pubmed: 26404259 pmcid: 4613246 doi: 10.3390/ijms160921138
Birge, R. B., Kalodimos, C., Inagaki, F. & Tanaka, S. Crk and CrkL adaptor proteins: networks for physiological and pathological signaling. Cell Commun. Signal. 7, 13 (2009).
pubmed: 19426560 pmcid: 2689226 doi: 10.1186/1478-811X-7-13
Seo, J. H., Suenaga, A., Hatakeyama, M., Taiji, M. & Imamoto, A. Structural and functional basis of a role for CRKL in a fibroblast growth factor 8-induced feed-forward loop. Mol. Cell Biol. 29, 3076–3087 (2009).
pubmed: 19307307 pmcid: 2681998 doi: 10.1128/MCB.01686-08
Park, T. J. & Curran, T. Essential roles of Crk and CrkL in fibroblast structure and motility. Oncogene 33, 5121–5132 (2014).
pubmed: 24166500 doi: 10.1038/onc.2013.453
Park, T., Koptyra, M. & Curran, T. Fibroblast growth requires CT10 regulator of kinase (Crk) and Crk-like (CrkL). J. Biol. Chem. 291, 26273–26290 (2016).
pubmed: 27807028 pmcid: 5159491 doi: 10.1074/jbc.M116.764613
Collins, T. N. et al. Crk proteins transduce FGF signaling to promote lens fiber cell elongation. eLife 7, e32586 (2018).
pubmed: 29360039 pmcid: 5818251 doi: 10.7554/eLife.32586
Kao, S., Jaiswal, R. K., Kolch, W. & Landreth, G. E. Identification of the mechanisms regulating the differential activation of the MAPK cascade by epidermal growth factor and nerve growth factor in PC12 cells. J. Biol. Chem. 276, 18169–18177 (2001).
pubmed: 11278445 doi: 10.1074/jbc.M008870200
Manser, E., Leung, T., Salihuddin, H., Zhao, Z. S. & Lim, L. A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature 367, 40–46 (1994).
pubmed: 8107774 doi: 10.1038/367040a0
Zugasti, O. et al. Raf-MEK-Erk cascade in anoikis is controlled by Rac1 and Cdc42 via Akt. Mol. Cell Biol. 21, 6706–6717 (2001).
pubmed: 11533257 pmcid: 99815 doi: 10.1128/MCB.21.19.6706-6717.2001
Lu, W., Gong, D., Bar-Sagi, D. & Cole, P. A. Site-specific incorporation of a phosphotyrosine mimetic reveals a role for tyrosine phosphorylation of SHP-2 in cell signaling. Mol. Cell 8, 759–769 (2001).
pubmed: 11684012 doi: 10.1016/S1097-2765(01)00369-0 pmcid: 11684012
Araki, T., Nawa, H. & Neel, B. G. Tyrosyl phosphorylation of Shp2 is required for normal ERK activation in response to some, but not all, growth factors. J. Biol. Chem. 278, 41677–41684 (2003).
pubmed: 12923167 doi: 10.1074/jbc.M306461200 pmcid: 12923167
Dance, M., Montagner, A., Salles, J. P., Yart, A. & Raynal, P. The molecular functions of Shp2 in the Ras/mitogen-activated protein kinase (ERK1/2) pathway. Cell Signal. 20, 453–459 (2008).
pubmed: 17993263 doi: 10.1016/j.cellsig.2007.10.002 pmcid: 17993263
Hanafusa, H., Torii, S., Yasunaga, T. & Nishida, E. Sprouty1 and Sprouty2 provide a control mechanism for the Ras/MAPK signalling pathway. Nat. Cell Biol. 4, 850–858 (2002).
pubmed: 12402043 doi: 10.1038/ncb867 pmcid: 12402043
Hanafusa, H., Torii, S., Yasunaga, T., Matsumoto, K. & Nishida, E. Shp2, an SH2-containing protein-tyrosine phosphatase, positively regulates receptor tyrosine kinase signaling by dephosphorylating and inactivating the inhibitor Sprouty. J. Biol. Chem. 279, 22992–22995 (2004).
pubmed: 15031289 doi: 10.1074/jbc.M312498200 pmcid: 15031289
Ornitz, D. M. & Marie, P. J. Fibroblast growth factors in skeletal development. Curr. Top. Dev. Biol. 133, 195–234 (2019).
pubmed: 30902253 doi: 10.1016/bs.ctdb.2018.11.020 pmcid: 30902253
Du, X., Xie, Y., Xian, C. J. & Chen, L. Role of FGFs/FGFRs in skeletal development and bone regeneration. J. Cell. Physiol. 227, 3731–3743 (2012).
pubmed: 22378383 doi: 10.1002/jcp.24083 pmcid: 22378383
Muenke, M. et al. A common mutation in the fibroblast growth factor receptor 1 gene in Pfeiffer syndrome. Nat. Genet. 8, 269–274 (1994).
pubmed: 7874169 doi: 10.1038/ng1194-269 pmcid: 7874169
White, K. E. et al. Mutations that cause osteoglophonic dysplasia define novel roles for FGFR1 in bone elongation. Am. J. Hum. Genet. 76, 361–367 (2005).
pubmed: 15625620 doi: 10.1086/427956 pmcid: 15625620
Wilkie, A. O. et al. Apert syndrome results from localized mutations of FGFR2 and is allelic with Crouzon syndrome. Nat. Genet. 9, 165–172 (1995).
pubmed: 7719344 doi: 10.1038/ng0295-165 pmcid: 7719344
Meyers, G. A. et al. FGFR2 exon IIIa and IIIc mutations in Crouzon, Jackson-Weiss, and Pfeiffer syndromes: evidence for missense changes, insertions, and a deletion due to alternative RNA splicing. Am. J. Hum. Genet. 58, 491–498 (1996).
pubmed: 8644708 pmcid: 1914562
Park, W. J. et al. Novel FGFR2 mutations in Crouzon and Jackson-Weiss syndromes show allelic heterogeneity and phenotypic variability. Hum. Mol. Genet. 4, 1229–1233 (1995).
pubmed: 8528214 doi: 10.1093/hmg/4.7.1229 pmcid: 8528214
Pulleyn, L. J. et al. Spectrum of craniosynostosis phenotypes associated with novel mutations at the fibroblast growth factor receptor 2 locus. Eur. J. Hum. Genet. 4, 283–291 (1996).
pubmed: 8946174 doi: 10.1159/000472215 pmcid: 8946174
Przylepa, K. A. et al. Fibroblast growth factor receptor 2 mutations in Beare-Stevenson cutis gyrata syndrome. Nat. Genet. 13, 492–494 (1996).
pubmed: 8696350 doi: 10.1038/ng0896-492 pmcid: 8696350
Merrill, A. E. et al. Bent bone dysplasia-FGFR2 type, a distinct skeletal disorder, has deficient canonical FGF signaling. Am. J. Hum. Genet. 90, 550–557 (2012).
pubmed: 22387015 pmcid: 3309195 doi: 10.1016/j.ajhg.2012.02.005
Robertson, S. C. et al. Activating mutations in the extracellular domain of the fibroblast growth factor receptor 2 function by disruption of the disulfide bond in the third immunoglobulin-like domain. Proc. Natl Acad. Sci. USA 95, 4567–4572 (1998).
pubmed: 9539778 doi: 10.1073/pnas.95.8.4567 pmcid: 9539778
Muenke, M. et al. A unique point mutation in the fibroblast growth factor receptor 3 gene (FGFR3) defines a new craniosynostosis syndrome. Am. J. Hum. Genet. 60, 555–564 (1997).
pubmed: 9042914 pmcid: 1712518
Tavormina, P. L. et al. Thanatophoric dysplasia (types I and II) caused by distinct mutations in fibroblast growth factor receptor 3. Nat. Genet. 9, 321–328 (1995).
pubmed: 7773297 doi: 10.1038/ng0395-321 pmcid: 7773297
Ye, X. et al. Mutation screening of candidate genes in patients with nonsyndromic sagittal craniosynostosis. Plast. Reconstr. Surg. 137, 952–961 (2016).
pubmed: 26910679 pmcid: 4770826 doi: 10.1097/01.prs.0000479978.75545.ee
Barroso, E. et al. Mild isolated craniosynostosis due to a novel FGFR3 mutation, p.Ala334Thr. Am. J. Med. Genet. A 155A, 3050–3053 (2011).
pubmed: 22038757 doi: 10.1002/ajmg.a.34199 pmcid: 22038757
Rousseau, F. et al. Missense FGFR3 mutations create cysteine residues in thanatophoric dwarfism type I (TD1). Hum. Mol. Genet. 5, 509–512 (1996).
pubmed: 8845844 doi: 10.1093/hmg/5.4.509 pmcid: 8845844
Shiang, R. et al. Mutations in the transmembrane domain of FGFR3 cause the most common genetic form of dwarfism, achondroplasia. Cell 78, 335–342 (1994).
pubmed: 7913883 doi: 10.1016/0092-8674(94)90302-6 pmcid: 7913883
Bellus, G. A. et al. A recurrent mutation in the tyrosine kinase domain of fibroblast growth factor receptor 3 causes hypochondroplasia. Nat. Genet. 10, 357–359 (1995).
pubmed: 7670477 doi: 10.1038/ng0795-357 pmcid: 7670477
Wilkes, D. et al. A recurrent mutation, ala391glu, in the transmembrane region of FGFR3 causes Crouzon syndrome and acanthosis nigricans. J. Med. Genet. 33, 744–748 (1996).
pubmed: 8880573 pmcid: 1050727 doi: 10.1136/jmg.33.9.744
Sarabipour, S. & Hristova, K. Mechanism of FGF receptor dimerization and activation. Nat. Commun. 7, 10262 (2016).
pubmed: 26725515 pmcid: 4725768 doi: 10.1038/ncomms10262
Sarabipour, S. & Hristova, K. FGFR3 unliganded dimer stabilization by the juxtamembrane domain. J. Mol. Biol. 427, 1705–1714 (2015).
pubmed: 25688803 pmcid: 4380549 doi: 10.1016/j.jmb.2015.02.013
Li, E., You, M. & Hristova, K. FGFR3 dimer stabilization due to a single amino acid pathogenic mutation. J. Mol. Biol. 356, 600–612 (2006).
pubmed: 16384584 doi: 10.1016/j.jmb.2005.11.077 pmcid: 16384584
Di Rocco, F. et al. FGFR3 mutation causes abnormal membranous ossification in achondroplasia. Hum. Mol. Genet. 23, 2914–2925 (2014).
pubmed: 24419316 doi: 10.1093/hmg/ddu004 pmcid: 24419316
Kannan, K. & Givol, D. FGF receptor mutations: dimerization syndromes, cell growth suppression, and animal models. IUBMB Life 49, 197–205 (2000).
pubmed: 10868910 doi: 10.1080/713803609 pmcid: 10868910
Naski, M. C., Wang, Q., Xu, J. & Ornitz, D. M. Graded activation of fibroblast growth factor receptor 3 by mutations causing achondroplasia and thanatophoric dysplasia. Nat. Genet. 13, 233–237 (1996).
pubmed: 8640234 doi: 10.1038/ng0696-233 pmcid: 8640234
Agochukwu, N. B., Solomon, B. D., Doherty, E. S. & Muenke, M. Palatal and oral manifestations of Muenke syndrome (FGFR3-related craniosynostosis). J. Craniofac. Surg. 23, 664–668 (2012).
pubmed: 22565872 pmcid: 3361570 doi: 10.1097/SCS.0b013e31824db8bb
Grillo, L. et al. Increased FGF3 and FGF4 gene dosage is a risk factor for craniosynostosis. Gene 534, 435–439 (2014).
pubmed: 24120895 doi: 10.1016/j.gene.2013.09.120 pmcid: 24120895
Hardelin, J. P. & Dode, C. The complex genetics of Kallmann syndrome: KAL1, FGFR1, FGF8, PROKR2, PROK2, et al. Sex. Dev. 2, 181–193 (2008).
pubmed: 18987492 doi: 10.1159/000152034 pmcid: 18987492
Larsson, T. et al. A novel recessive mutation in fibroblast growth factor-23 causes familial tumoral calcinosis. J. Clin. Endocrinol. Metab. 90, 2424–2427 (2005).
pubmed: 15687325 doi: 10.1210/jc.2004-2238 pmcid: 15687325
Rodriguez-Zabala, M. et al. FGF9 mutation causes craniosynostosis along with multiple synostoses. Hum. Mutat. 38, 1471–1476 (2017).
pubmed: 28730625 doi: 10.1002/humu.23292 pmcid: 28730625
Rohmann, E. et al. Mutations in different components of FGF signaling in LADD syndrome. Nat. Genet. 38, 414–417 (2006).
pubmed: 16501574 doi: 10.1038/ng1757 pmcid: 16501574
Tang, L. et al. A point mutation in Fgf9 impedes joint interzone formation leading to multiple synostoses syndrome. Hum. Mol. Genet. 26, 1280–1293 (2017).
pubmed: 28169396 doi: 10.1093/hmg/ddx029 pmcid: 28169396
Tekin, M. et al. Homozygous mutations in fibroblast growth factor 3 are associated with a new form of syndromic deafness characterized by inner ear agenesis, microtia, and microdontia. Am. J. Hum. Genet. 80, 338–344 (2007).
pubmed: 17236138 doi: 10.1086/510920 pmcid: 17236138
Wu, X. L. et al. Multiple synostoses syndrome is due to a missense mutation in exon 2 of FGF9 gene. Am. J. Hum. Genet. 85, 53–63 (2009).
pubmed: 19589401 pmcid: 2706969 doi: 10.1016/j.ajhg.2009.06.007
Chefetz, I. et al. A novel homozygous missense mutation in FGF23 causes familial tumoral calcinosis associated with disseminated visceral calcification. Hum. Genet. 118, 261–266 (2005).
pubmed: 16151858 doi: 10.1007/s00439-005-0026-8 pmcid: 16151858
Araya, K. et al. A novel mutation in fibroblast growth factor 23 gene as a cause of tumoral calcinosis. J. Clin. Endocrinol. Metab. 90, 5523–5527 (2005).
pubmed: 16030159 doi: 10.1210/jc.2005-0301 pmcid: 16030159
Abbasi, F. et al. A new missense mutation in FGF23 gene in a male with hyperostosis-hyperphosphatemia syndrome (HHS). Gene 542, 269–271 (2014).
pubmed: 24680727 doi: 10.1016/j.gene.2014.03.052 pmcid: 24680727
ADHR Consortium. Autosomal dominant hypophosphataemic rickets is associated with mutations in FGF23. Nat. Genet. 26, 345–348 (2000).
doi: 10.1038/81664
White, K. E. et al. Autosomal-dominant hypophosphatemic rickets (ADHR) mutations stabilize FGF-23. Kidney Int. 60, 2079–2086 (2001).
pubmed: 11737582 doi: 10.1046/j.1523-1755.2001.00064.x pmcid: 11737582
Gribaa, M. et al. An autosomal dominant hypophosphatemic rickets phenotype in a Tunisian family caused by a new FGF23 missense mutation. J. Bone Miner. Metab. 28, 111–115 (2010).
pubmed: 19655082 doi: 10.1007/s00774-009-0111-5 pmcid: 19655082
Shimada, T. et al. Mutant FGF-23 responsible for autosomal dominant hypophosphatemic rickets is resistant to proteolytic cleavage and causes hypophosphatemia in vivo. Endocrinology 143, 3179–3182 (2002).
pubmed: 12130585 doi: 10.1210/endo.143.8.8795 pmcid: 12130585
Ornitz, D. M. FGF signaling in the developing endochondral skeleton. Cytokine Growth Factor Rev. 16, 205–213 (2005).
pubmed: 15863035 pmcid: 3083241 doi: 10.1016/j.cytogfr.2005.02.003
Long, F. & Ornitz, D. M. Development of the endochondral skeleton. Cold Spring Harb. Perspect. Biol. 5, a008334 (2013).
pubmed: 23284041 pmcid: 3579395 doi: 10.1101/cshperspect.a008334
Sheeba, C. J., Andrade, R. P., Duprez, D. & Palmeirim, I. Comprehensive analysis of fibroblast growth factor receptor expression patterns during chick forelimb development. Int. J. Dev. Biol. 54, 1517–1526 (2010).
pubmed: 21302260 doi: 10.1387/ijdb.092887cs pmcid: 21302260
Orr-Urtreger, A., Givol, D., Yayon, A., Yarden, Y. & Lonai, P. Developmental expression of two murine fibroblast growth factor receptors, flg and bek. Development 113, 1419–1434 (1991).
pubmed: 1667382 pmcid: 1667382
Moon, A. M., Boulet, A. M. & Capecchi, M. R. Normal limb development in conditional mutants of Fgf4. Development 127, 989–996 (2000).
pubmed: 10662638 pmcid: 1780036
Mariani, F. V., Ahn, C. P. & Martin, G. R. Genetic evidence that FGFs have an instructive role in limb proximal-distal patterning. Nature 453, 401–405 (2008).
pubmed: 18449196 pmcid: 2631409 doi: 10.1038/nature06876
Jin, L., Wu, J., Bellusci, S. & Zhang, J.-S. Fibroblast growth factor 10 and vertebrate limb development. Front. Genet. 9, 705 (2019).
pubmed: 30687387 pmcid: 6338048 doi: 10.3389/fgene.2018.00705
Delezoide, A. L. et al. Spatio-temporal expression of FGFR 1, 2 and 3 genes during human embryo-fetal ossification. Mech. Dev. 77, 19–30 (1998).
pubmed: 9784595 doi: 10.1016/S0925-4773(98)00133-6 pmcid: 9784595
Eswarakumar, V. P. et al. The IIIc alternative of Fgfr2 is a positive regulator of bone formation. Development 129, 3783–3793 (2002).
pubmed: 12135917 pmcid: 12135917
Jacob, A. L., Smith, C., Partanen, J. & Ornitz, D. M. Fibroblast growth factor receptor 1 signaling in the osteo-chondrogenic cell lineage regulates sequential steps of osteoblast maturation. Dev. Biol. 296, 315–328 (2006).
pubmed: 16815385 pmcid: 2077084 doi: 10.1016/j.ydbio.2006.05.031
Lazarus, J. E., Hegde, A., Andrade, A. C., Nilsson, O. & Baron, J. Fibroblast growth factor expression in the postnatal growth plate. Bone 40, 577–586 (2007).
pubmed: 17169623 doi: 10.1016/j.bone.2006.10.013 pmcid: 17169623
Partanen, J. et al. FGFR-4, a novel acidic fibroblast growth factor receptor with a distinct expression pattern. EMBO J. 10, 1347–1354 (1991).
pubmed: 1709094 pmcid: 452793 doi: 10.1002/j.1460-2075.1991.tb07654.x
Cool, S., Jackson, R., Pincus, P., Dickinson, I. & Nurcombe, V. Fibroblast growth factor receptor 4 (FGFR4) expression in newborn murine calvaria and primary osteoblast cultures. Int. J. Dev. Biol. 46, 519–523 (2002).
pubmed: 12141439 pmcid: 12141439
Karolak, M. R., Yang, X. & Elefteriou, F. FGFR1 signaling in hypertrophic chondrocytes is attenuated by the Ras-GAP neurofibromin during endochondral bone formation. Hum. Mol. Genet. 24, 2552–2564 (2015).
pubmed: 25616962 pmcid: 4383864 doi: 10.1093/hmg/ddv019
Hung, I. H., Yu, K., Lavine, K. J. & Ornitz, D. M. FGF9 regulates early hypertrophic chondrocyte differentiation and skeletal vascularization in the developing stylopod. Dev. Biol. 307, 300–313 (2007).
pubmed: 17544391 pmcid: 2267922 doi: 10.1016/j.ydbio.2007.04.048
Karuppaiah, K. et al. FGF signaling in the osteoprogenitor lineage non-autonomously regulates postnatal chondrocyte proliferation and skeletal growth. Development 143, 1811–1822 (2016).
pubmed: 27052727 pmcid: 4874483 doi: 10.1242/dev.131722
Ohbayashi, N. et al. FGF18 is required for normal cell proliferation and differentiation during osteogenesis and chondrogenesis. Genes Dev. 16, 870–879 (2002).
pubmed: 11937494 pmcid: 186331 doi: 10.1101/gad.965702
Longobardi, L. et al. Synovial joints: from development to homeostasis. Curr. Osteoporos. Rep. 13, 41–51 (2015).
pubmed: 25431159 pmcid: 4306636 doi: 10.1007/s11914-014-0247-7
Lovinescu, I., Koyama, E. & Pacifici, M. Roles of FGF-10 on the development of diathrodial limb joints. Penn Dent. J. 103, 5–9 (2003).
pubmed: 15481582 pmcid: 15481582
Yan, D. et al. Fibroblast growth factor receptor 1 is principally responsible for fibroblast growth factor 2-induced catabolic activities in human articular chondrocytes. Arthritis Res. Ther. 13, R130 (2011).
pubmed: 21835001 pmcid: 3239372 doi: 10.1186/ar3441
Chen, T. M., Chen, Y. H., Sun, H. S. & Tsai, S. J. Fibroblast growth factors: potential novel targets for regenerative therapy of osteoarthritis. Chin. J. Physiol. 62, 2–10 (2019).
pubmed: 30942193 doi: 10.4103/CJP.CJP_23_19 pmcid: 30942193
Hagan, A. S. et al. Generation and validation of novel conditional flox and inducible Cre alleles targeting fibroblast growth factor 18 (Fgf18). Dev. Dyn. 248, 882–893 (2019).
pubmed: 31290205 pmcid: 7029619 doi: 10.1002/dvdy.85
Malemud, C. J. Growth hormone, VEGF and FGF: involvement in rheumatoid arthritis. Clin. Chim. Acta 375, 10–19 (2007).
pubmed: 16893535 doi: 10.1016/j.cca.2006.06.033 pmcid: 16893535
Glyn-Jones, S. et al. Osteoarthritis. Lancet 386, 376–387 (2015).
pubmed: 25748615 doi: 10.1016/S0140-6736(14)60802-3 pmcid: 25748615
Loeser, R. F., Collins, J. A. & Diekman, B. O. Ageing and the pathogenesis of osteoarthritis. Nat. Rev. Rheumatol. 12, 412–420 (2016).
pubmed: 27192932 pmcid: 4938009 doi: 10.1038/nrrheum.2016.65
Daouti, S. et al. Development of comprehensive functional genomic screens to identify novel mediators of osteoarthritis. Osteoarthr. Cartilage 13, 508–518 (2005).
doi: 10.1016/j.joca.2005.02.003
Im, H. J. et al. Basic fibroblast growth factor stimulates matrix metalloproteinase-13 via the molecular cross-talk between the mitogen-activated protein kinases and protein kinase Cδ pathways in human adult articular chondrocytes. J. Biol. Chem. 282, 11110–11121 (2007).
pubmed: 17311929 pmcid: 2895271 doi: 10.1074/jbc.M609040200
Weng, T. et al. Genetic inhibition of fibroblast growth factor receptor 1 in knee cartilage attenuates the degeneration of articular cartilage in adult mice. Arthritis Rheum. 64, 3982–3992 (2012).
pubmed: 22833219 pmcid: 3690192 doi: 10.1002/art.34645
Xu, W. et al. A novel fibroblast growth factor receptor 1 inhibitor protects against cartilage degradation in a murine model of osteoarthritis. Sci. Rep. 6, 24042 (2016).
pubmed: 27041213 pmcid: 4819196 doi: 10.1038/srep24042
Tang, J. et al. Fibroblast growth factor receptor 3 inhibits osteoarthritis progression in the knee joints of adult mice. Arthritis Rheumatol. 68, 2432–2443 (2016).
pubmed: 27159076 doi: 10.1002/art.39739
Zhou, S. et al. Conditional deletion of Fgfr3 in chondrocytes leads to osteoarthritis-like defects in temporomandibular joint of adult mice. Sci. Rep. 6, 24039 (2016).
pubmed: 27041063 pmcid: 4819201 doi: 10.1038/srep24039
Kuang, L. et al. FGFR3 deficiency enhances CXCL12-dependent chemotaxis of macrophages via upregulating CXCR7 and aggravates joint destruction in mice. Ann. Rheum. Dis. 79, 112–122 (2020).
pubmed: 31662319 doi: 10.1136/annrheumdis-2019-215696
Klag, K. A. & Horton, W. A. Advances in treatment of achondroplasia and osteoarthritis. Hum. Mol. Genet. 25, R2–R8 (2016).
pubmed: 26443596 doi: 10.1093/hmg/ddv419
Kisand, K., Tamm, A. E., Lintrop, M. & Tamm, A. O. New insights into the natural course of knee osteoarthritis: early regulation of cytokines and growth factors, with emphasis on sex-dependent angiogenesis and tissue remodeling. A pilot study. Osteoarthr. Cartilage 26, 1045–1054 (2018).
doi: 10.1016/j.joca.2018.05.009
Im, H. J. et al. Basic fibroblast growth factor accelerates matrix degradation via a neuro-endocrine pathway in human adult articular chondrocytes. J. Cell. Physiol. 215, 452–463 (2008).
pubmed: 17960584 pmcid: 2893571 doi: 10.1002/jcp.21317
Vincent, T. L., McLean, C. J., Full, L. E., Peston, D. & Saklatvala, J. FGF-2 is bound to perlecan in the pericellular matrix of articular cartilage, where it acts as a chondrocyte mechanotransducer. Osteoarthr. Cartilage 15, 752–763 (2007).
doi: 10.1016/j.joca.2007.01.021
Muddasani, P., Norman, J. C., Ellman, M., van Wijnen, A. J. & Im, H. J. Basic fibroblast growth factor activates the MAPK and NFκB pathways that converge on Elk-1 to control production of matrix metalloproteinase-13 by human adult articular chondrocytes. J. Biol. Chem. 282, 31409–31421 (2007).
pubmed: 17724016 doi: 10.1074/jbc.M706508200
Nummenmaa, E., Hamalainen, M., Moilanen, T., Vuolteenaho, K. & Moilanen, E. Effects of FGF-2 and FGF receptor antagonists on MMP enzymes, aggrecan, and type II collagen in primary human OA chondrocytes. Scand. J. Rheumatol. 44, 321–330 (2015).
pubmed: 25743336 doi: 10.3109/03009742.2014.1000372
Chong, K. W. et al. Fibroblast growth factor 2 drives changes in gene expression following injury to murine cartilage in vitro and in vivo. Arthritis Rheum. 65, 2346–2355 (2013).
pubmed: 23740825 pmcid: 3992838 doi: 10.1002/art.38039
Sawaji, Y., Hynes, J., Vincent, T. & Saklatvala, J. Fibroblast growth factor 2 inhibits induction of aggrecanase activity in human articular cartilage. Arthritis Rheum. 58, 3498–3509 (2008).
pubmed: 18975307 doi: 10.1002/art.24025
Tang, Z. F. & Li, H. Y. Effects of fibroblast growth factors 2 and low intensity pulsed ultrasound on the repair of knee articular cartilage in rabbits. Eur. Rev. Med. Pharmacol. Sci. 22, 2447–2453 (2018).
pubmed: 29762847
Cuevas, P., Burgos, J. & Baird, A. Basic fibroblast growth factor (FGF) promotes cartilage repair in vivo. Biochem. Biophys. Res. Commun. 156, 611–618 (1988).
pubmed: 3190672 doi: 10.1016/S0006-291X(88)80887-8
Chia, S. L. et al. Fibroblast growth factor 2 is an intrinsic chondroprotective agent that suppresses ADAMTS-5 and delays cartilage degradation in murine osteoarthritis. Arthritis Rheum. 60, 2019–2027 (2009).
pubmed: 19565481 doi: 10.1002/art.24654
Burt, P. M., Xiao, L., Doetschman, T. & Hurley, M. M. Ablation of low-molecular-weight FGF2 isoform accelerates murine osteoarthritis while loss of high-molecular-weight FGF2 isoforms offers protection. J. Cell. Physiol. 234, 4418–4431 (2019).
pubmed: 30144364 doi: 10.1002/jcp.27230
Li, R. et al. Upregulation of fibroblast growth factor 1 in the synovial membranes of patients with late stage osteoarthritis. Genet. Mol. Res. 14, 11191–11199 (2015).
pubmed: 26400350 doi: 10.4238/2015.September.22.13
El-Seoudi, A. et al. Catabolic effects of FGF-1 on chondrocytes and its possible role in osteoarthritis. J. Cell Commun. Signal. 11, 255–263 (2017).
pubmed: 28343287 pmcid: 5559396 doi: 10.1007/s12079-017-0384-8
Uchii, M. et al. Role of fibroblast growth factor 8 (FGF8) in animal models of osteoarthritis. Arthritis Res. Ther. 10, R90 (2008).
pubmed: 18699993 pmcid: 2575604 doi: 10.1186/ar2474
Rockel, J. S. et al. Hedgehog inhibits β-catenin activity in synovial joint development and osteoarthritis. J. Clin. Invest. 126, 1649–1663 (2016).
pubmed: 27018594 pmcid: 4855923 doi: 10.1172/JCI80205
Mori, Y. et al. Identification of fibroblast growth factor-18 as a molecule to protect adult articular cartilage by gene expression profiling. J. Biol. Chem. 289, 10192–10200 (2014).
pubmed: 24577103 pmcid: 3974988 doi: 10.1074/jbc.M113.524090
Ellsworth, J. L. et al. Fibroblast growth factor-18 is a trophic factor for mature chondrocytes and their progenitors. Osteoarthr. Cartilage 10, 308–320 (2002).
doi: 10.1053/joca.2002.0514
Moore, E. E. et al. Fibroblast growth factor-18 stimulates chondrogenesis and cartilage repair in a rat model of injury-induced osteoarthritis. Osteoarthr. Cartilage 13, 623–631 (2005).
doi: 10.1016/j.joca.2005.03.003
Zhou, S. et al. Exogenous fibroblast growth factor 9 attenuates cartilage degradation and aggravates osteophyte formation in post-traumatic osteoarthritis. Osteoarthr. Cartilage 24, 2181–2192 (2016).
doi: 10.1016/j.joca.2016.07.005
Sun, Y. et al. Analysis of meniscal degeneration and meniscal gene expression. BMC Musculoskelet. Disord. 11, 19 (2010).
pubmed: 20109188 pmcid: 2828422 doi: 10.1186/1471-2474-11-19
Li, Z. C. et al. Fibroblast growth factor-21 concentration in serum and synovial fluid is associated with radiographic bone loss of knee osteoarthritis. Scand. J. Clin. Lab. Invest. 75, 121–125 (2015).
pubmed: 25549692 doi: 10.3109/00365513.2014.992942
Bianchi, A. et al. Fibroblast growth factor 23 drives MMP13 expression in human osteoarthritic chondrocytes in a Klotho-independent manner. Osteoarthr. Cartilage 24, 1961–1969 (2016).
doi: 10.1016/j.joca.2016.06.003
Meo Burt, P., Xiao, L. & Hurley, M. M. FGF23 regulates Wnt/β-catenin signaling-mediated osteoarthritis in mice overexpressing high-molecular-weight FGF2. Endocrinology 159, 2386–2396 (2018).
pubmed: 29718273 pmcid: 6457004 doi: 10.1210/en.2018-00184
Kim, J. H., Lee, M. C., Seong, S. C., Park, K. H. & Lee, S. Enhanced proliferation and chondrogenic differentiation of human synovium-derived stem cells expanded with basic fibroblast growth factor. Tissue Eng. Part A 17, 991–1002 (2011).
pubmed: 21091327 doi: 10.1089/ten.tea.2010.0277
Li, J. & Pei, M. Optimization of an in vitro three-dimensional microenvironment to reprogram synovium-derived stem cells for cartilage tissue engineering. Tissue Eng. Part A 17, 703–712 (2011).
pubmed: 20929284 doi: 10.1089/ten.tea.2010.0339
Chen, X. et al. Integration capacity of human induced pluripotent stem cell-derived cartilage. Tissue Eng. Part A 25, 437–445 (2018).
pubmed: 30129877 doi: 10.1089/ten.tea.2018.0133
Gigout, A. et al. Sprifermin (rhFGF18) enables proliferation of chondrocytes producing a hyaline cartilage matrix. Osteoarthr. Cartilage 25, 1858–1867 (2017).
doi: 10.1016/j.joca.2017.08.004
Meloni, G. R. et al. Recombinant human FGF18 preserves depth-dependent mechanical inhomogeneity in articular cartilage. Eur. Cell Mater. 38, 23–34 (2019).
pubmed: 31393594 pmcid: 7273689 doi: 10.22203/eCM.v038a03
Sennett, M. L. et al. Sprifermin treatment enhances cartilage integration in an in vitro repair model. J. Orthop. Res. 36, 2648–2656 (2018).
pubmed: 29761549 pmcid: 7241943 doi: 10.1002/jor.24048
Barr, L., Getgood, A., Guehring, H., Rushton, N. & Henson, F. M. The effect of recombinant human fibroblast growth factor-18 on articular cartilage following single impact load. J. Orthop. Res. 32, 923–927 (2014).
pubmed: 24719286 doi: 10.1002/jor.22622
Yao, X. et al. Fibroblast growth factor 18 exerts anti-osteoarthritic effects through PI3K-AKT signaling and mitochondrial fusion and fission. Pharmacol. Res. 139, 314–324 (2019).
pubmed: 30273654 doi: 10.1016/j.phrs.2018.09.026
Howard, D., Wardale, J., Guehring, H. & Henson, F. Delivering rhFGF-18 via a bilayer collagen membrane to enhance microfracture treatment of chondral defects in a large animal model. J. Orthop. Res. 33, 1120–1127 (2015).
pubmed: 25721940 doi: 10.1002/jor.22882 pmcid: 25721940
Power, J., Hernandez, P., Guehring, H., Getgood, A. & Henson, F. Intra-articular injection of rhFGF-18 improves the healing in microfracture treated chondral defects in an ovine model. J. Orthop. Res. 32, 669–676 (2014).
pubmed: 24436147 doi: 10.1002/jor.22580 pmcid: 24436147
Eckstein, F., Wirth, W., Guermazi, A., Maschek, S. & Aydemir, A. Brief report: intraarticular sprifermin not only increases cartilage thickness, but also reduces cartilage loss: location-independent post hoc analysis using magnetic resonance imaging. Arthritis Rheumatol. 67, 2916–2922 (2015).
pubmed: 26138203 pmcid: 5061102 doi: 10.1002/art.39265
Lohmander, L. S. et al. Intraarticular sprifermin (recombinant human fibroblast growth factor 18) in knee osteoarthritis: a randomized, double-blind, placebo-controlled trial. Arthritis Rheumatol. 66, 1820–1831 (2014).
pubmed: 24740822 doi: 10.1002/art.38614
Hochberg, M. C. et al. Effect of intra-articular sprifermin vs placebo on femorotibial joint cartilage thickness in patients with osteoarthritis: the FORWARD randomized clinical trial. JAMA 322, 1360–1370 (2019).
pubmed: 31593273 pmcid: 6784851 doi: 10.1001/jama.2019.14735
Sanghani, A., Chimutengwende-Gordon, M., Adesida, A. & Khan, W. Applications of stem cell therapy for physeal injuries. Curr. Stem Cell Res. Ther. 8, 451–455 (2013).
pubmed: 24016322 doi: 10.2174/1574888X1130800063 pmcid: 24016322
Chung, R. & Xian, C. J. Recent research on the growth plate: mechanisms for growth plate injury repair and potential cell-based therapies for regeneration. J. Mol. Endocrinol. 53, T45–T61 (2014).
pubmed: 25114207 doi: 10.1530/JME-14-0062 pmcid: 25114207
Henson, F. M., Bowe, E. A. & Davies, M. E. Promotion of the intrinsic damage-repair response in articular cartilage by fibroblastic growth factor-2. Osteoarthr. Cartilage 13, 537–544 (2005).
doi: 10.1016/j.joca.2005.02.007
Cucchiarini, M., Schetting, S., Terwilliger, E. F., Kohn, D. & Madry, H. rAAV-mediated overexpression of FGF-2 promotes cell proliferation, survival, and α-SMA expression in human meniscal lesions. Gene Ther. 16, 1363–1372 (2009).
pubmed: 19641531 doi: 10.1038/gt.2009.91 pmcid: 19641531
Schmidt, L., Taiyab, A., Melvin, V. S., Jones, K. L. & Williams, T. Increased FGF8 signaling promotes chondrogenic rather than osteogenic development in the embryonic skull. Dis. Model. Mech. 11, dmm.031526 (2018).
doi: 10.1242/dmm.031526
Dai, J. et al. The effect of co-culturing costal chondrocytes and dental pulp stem cells combined with exogenous FGF9 protein on chondrogenesis and ossification in engineered cartilage. Biomaterials 33, 7699–7711 (2012).
pubmed: 22841919 doi: 10.1016/j.biomaterials.2012.07.020 pmcid: 22841919
Tan, Q. et al. A novel FGFR1-binding peptide attenuates the degeneration of articular cartilage in adult mice. Osteoarthr. Cartilage 26, 1733–1743 (2018).
doi: 10.1016/j.joca.2018.08.012
Mobasheri, A. et al. The role of metabolism in the pathogenesis of osteoarthritis. Nat. Rev. Rheumatol. 13, 302–311 (2017).
pubmed: 28381830 doi: 10.1038/nrrheum.2017.50 pmcid: 28381830
Makower, A. M., Wroblewski, J. & Pawlowski, A. Effects of IGF-I, rGH, FGF, EGF and NCS on DNA-synthesis, cell proliferation and morphology of chondrocytes isolated from rat rib growth cartilage. Cell Biol. Int. Rep. 13, 259–270 (1989).
pubmed: 2706688 doi: 10.1016/0309-1651(89)90148-3 pmcid: 2706688

Auteurs

Yangli Xie (Y)

Department of Wound Repair and Rehabilitation Medicine, State Key Laboratory of Trauma, Burns and Combined Injury, Daping Hospital, Army Medical University, Chongqing, China.
ORCID: 0000-0002-2865-1126

Allen Zinkle (A)

Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY, USA.
Columbia University, New York, NY, USA.

Lin Chen (L)

Department of Wound Repair and Rehabilitation Medicine, State Key Laboratory of Trauma, Burns and Combined Injury, Daping Hospital, Army Medical University, Chongqing, China. linchen70@163.com.
ORCID: 0000-0001-7764-9412

Moosa Mohammadi (M)

Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY, USA. moosa.mohammadi@nyulangone.org.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Effectiveness of Virtual Yoga for Chronic Low Back Pain: A Randomized Clinical Trial.

Hallie Tankha, Devyn Gaskins, Amanda Shallcross et al.
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Fibroblast growth factor signalling in...
questionsmedicales.fr › Appareil locomoteur › Squelette › Articulations › Cartilage articulaire › Fibroblast growth factor signalling in...
questionsmedicales.fr › Environnement et santé publique › Santé publique › Méthodes épidémiologiques › Caractéristiques des études épidémiologiques › Études cliniques comme sujet › Essais cliniques comme sujet › Fibroblast growth factor signalling in...
questionsmedicales.fr › États, signes et symptômes pathologiques › Processus pathologiques › Caractéristiques de la maladie › Évolution de la maladie › Fibroblast growth factor signalling in...
questionsmedicales.fr › Facteurs biologiques › Protéines et peptides de signalisation intercellulaire › Facteurs de croissance fibroblastique › Fibroblast growth factor signalling in...
questionsmedicales.fr › Phénomènes physiologiques › Homéostasie › Fibroblast growth factor signalling in...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Fibroblast growth factor signalling in...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Fibroblast growth factor signalling in...
questionsmedicales.fr › Techniques d'investigation › Modèles animaux › Fibroblast growth factor signalling in...
questionsmedicales.fr › Maladies ostéomusculaires › Arthrose › Fibroblast growth factor signalling in...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Récepteurs de surface cellulaire › Récepteurs peptidiques › Récepteur facteur croissance › Récepteur facteur croissance fibroblaste › Récepteur FGFR1 › Fibroblast growth factor signalling in...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines tumorales › Protéines oncogènes › Protéines proto-oncogènes › Récepteur de type 3 des facteurs de croissance fibroblastique › Fibroblast growth factor signalling in...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Transduction du signal › Fibroblast growth factor signalling in...