Insights Into the Molecular Basis for FGF Receptor Autoinhibition and Ligand Binding Promiscuity

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Authors
Olsen, S.K.
Ibrahimi, O.A.
Raucci, A.
Zhang, F.
Eliseenkova, A.V.
Yayon, A.
Basilico, C.
Linhardt, Robert J.
Schlessinger, J.
Mohammadi, M.
Issue Date
2004
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Article
Language
ENG
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Biology , Chemistry and chemical biology , Chemical and biological engineering , Biomedical engineering
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Abstract
The prototypical fibroblast growth factor receptor (FGFR) extracellular domain consists of three Ig domains (D1-D3) of which the two membrane-proximal D2 and D3 domains and the interconnecting D2-D3 linker bear the determinants of ligand binding and specificity. In contrast, D1 and the D1-D2 linker are thought to play autoinhibitory roles in FGFR regulation. Here, we report the crystal structure of the three-Ig form of FGFR3c in complex with FGF1, an FGF that binds promiscuously to each of the seven principal FGFRs. In this structure, D1 and the D1-D2 linker are completely disordered, demonstrating that these regions are dispensable for FGF binding. Real-time binding experiments using surface plasmon resonance show that relative to two-Ig form, the three-Ig form of FGFR3c exhibits lower affinity for both FGF1 and heparin. Importantly, we demonstrate that this autoinhibition is mediated by intramolecular interactions of D1 and the D1-D2 linker with the minimal FGF and heparin-binding D2-D3 region. As in the FGF1-FGFR2c structure, but not the FGF1-FGFR1c structure, the alternatively spliced betaC'-betaE loop is ordered and interacts with FGF1 in the FGF1-FGFR3c structure. However, in contrast to the FGF1-FGFR2c structure in which the betaC'-betaE loop interacts with the beta-trefoil core region of FGF1, in the FGF1-FGFR3c structure, this loop interacts extensively with the N-terminal region of FGF1, underscoring the importance of the FGF1 N terminus in conferring receptor-binding affinity and promiscuity. Importantly, comparison of the three FGF1-FGFR structures shows that the flexibility of the betaC'-betaE loop is a major determinant of ligand-binding specificity and promiscuity.
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Proceedings of the National Academy of Sciences USA, 101, 935-940
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Full Citation
Insights Into the Molecular Basis for FGF Receptor Autoinhibition and Ligand Binding Promiscuity, S. K. Olsen, O. A. Ibrahimi, A. Raucci, F. Zhang, A. V. Eliseenkova, A. Yayon, C. Basilico, R. J. Linhardt, J. Schlessinger, M. Mohammadi, Proceedings of the National Academy of Sciences USA, 101, 935-940, 2004.
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