Proline to arginine mutations in FGF receptors 1 and 3 result in Pfeiffer and Muenke craniosynostosis syndromes through enhancement of FGF binding affinity

Ibrahimi, O. A.

doi:10.1093/hmg/ddh011

Cited by 128Craniofacial Disorders and TreatmentsFibroblast Growth Factor ResearchConnective tissue disorders research

Proline to arginine mutations in FGF receptors 1 and 3 result in Pfeiffer and Muenke craniosynostosis syndromes through enhancement of FGF binding affinity

Ibrahimi, O. A.·2003·Human Molecular Genetics

DOI 10.1093/hmg/ddh011

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Abstract

Identical proline-->arginine gain-of-function mutations in fibroblast growth factor receptor (FGFR) 1 (Pro252Arg), FGFR2 (Pro253Arg) and FGFR3 (Pro250Arg), result in type I Pfeiffer, Apert and Muenke craniosynostosis syndromes, respectively. Here, we characterize the effects of proline-->arginine mutations in FGFR1c and FGFR3c on ligand binding using surface plasmon resonance and X-ray crystallography. Both Pro252Arg FGFR1c and Pro250Arg FGFR3c exhibit an enhancement in ligand binding in comparison to their respective wild-type receptors. Interestingly, binding of both mutant receptors to FGF9 was notably enhanced and implicates FGF9 as a potential pathophysiological ligand for mutant FGFRs in mediating craniosynostosis. The crystal structure, of Pro252Arg FGFR1c in complex with FGF2, demonstrates that the enhanced ligand binding is due to an additional set of receptor-ligand hydrogen bonds, similar to those gain-of-function interactions that occur in the Apert syndrome Pro253Arg FGFR2c-FGF2 crystal structure. However, unlike the Apert syndrome Pro253Arg FGFR2c mutant, neither the Pfeiffer syndrome Pro250Arg FGFR1c mutant nor the Muenke syndrome Pro250Arg FGFR3c mutant bound appreciably to FGF7 or FGF10. This observation provides a potential explanation for why the limb phenotypes, observed in type I Pfeiffer and Muenke syndromes, are less severe than the limb abnormalities observed in Apert syndrome. Hence, although analogous proline-->arginine mutations in FGFR1-3 act through a common structural mechanism to result in gain-of-function, differences in the primary sequence among FGFRs result in varying effects on ligand binding specificity.

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The Pro250Arg substitution is equivalent to the Apert Pro253Arg substitution in FGFR2 and also causes ligand-dependent gain-of-function.
“The Pro250Arg substitution is the exact equivalent to the Apert Pro253Arg substitution in FGFR2, and also causes liganddependent gain-of-function.24”
From Craniosynostosis (2011) · cites this paper as [24]
Gain-of-function mutations in FGFR1 are associated with myeloproliferative disorders leading to leukemia.
“Gain-of-function mutations in FGFR1 are associated with myeloproliferative disorders leading to leukemia, as well as hereditary conditions leading to skeletal and craniofacial abnormalities, both of which are common in DS78–80.”
From Trisomy 21 causes changes in the circulating proteome indicative of chronic autoinflammation (2017) · cites this paper as [78]
Gain-of-function mutations in FGFR1 are associated with hereditary conditions leading to skeletal and craniofacial abnormalities.
“Gain-of-function mutations in FGFR1 are associated with myeloproliferative disorders leading to leukemia, as well as hereditary conditions leading to skeletal and craniofacial abnormalities, both of which are common in DS78–80.”
From Trisomy 21 causes changes in the circulating proteome indicative of chronic autoinflammation (2017) · cites this paper as [78]
Myeloproliferative disorders leading to leukemia and hereditary skeletal/craniofacial abnormalities are common in Down syndrome.
“Gain-of-function mutations in FGFR1 are associated with myeloproliferative disorders leading to leukemia, as well as hereditary conditions leading to skeletal and craniofacial abnormalities, both of which are common in DS78–80.”
From Trisomy 21 causes changes in the circulating proteome indicative of chronic autoinflammation (2017) · cites this paper as [78]

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Authors: Ibrahimi, O. A.
Affiliations: New York University (US)
Corresponding author: Ibrahimi, O. A.
ORCID: Ibrahimi, O. A.
Venue: Human Molecular Genetics
Publisher: Oxford University Press (OUP)
Published: 2003-10-28
Volume: 13
Issue: 1
Pages: 69-78
ISSN: 0964-6906 (ISSN-L)
1460-2083
DOI: 10.1093/hmg/ddh011
OpenAlex: W2161638912
Cited by: 128
References: 64
Citations by year: 2026: 4 · 2024: 2 · 2023: 3 · 2022: 3 · 2021: 3 · 2020: 4 · 2019: 3 · 2018: 1 · 2017: 6 · 2016: 4 · 2015: 5 · 2014: 7 · 2013: 9 · 2012: 11
FWCI: 5.66
Type: journal article
Language: en
Open access: closed
Locations: Human Molecular Genetics (publishedVersion)
PubMed (publishedVersion)
Funders: Howard Hughes Medical Institute
U.S. Department of Energy
National Heart, Lung, and Blood Institute (HL 52622, R01HL052622)
National Institute of Dental and Craniofacial Research (DE13686, R01DE013686)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Craniofacial Disorders and Treatments
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fibroblast Growth Factor Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Connective tissue disorders research
Keywords: fibroblast growth factor receptor, FGFR1, FGFR3, FGFR2, gain-of-function mutations, craniosynostosis, Pfeiffer syndrome, Muenke syndrome, Apert syndrome, FGF9, FGF2, ligand binding affinity, ligand specificity, limb malformations
MeSH terms: Amino Acids, Chromatography, Craniosynostoses, Fibroblast Growth Factors, Humans, Hydrogen Bonding, Ligands, Protein Binding, Point Mutation, Receptors, Fibroblast Growth Factor, Crystallography, X-Ray, Surface Plasmon Resonance, Protein Structure, Quaternary, Fibroblast Growth Factor 9

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Proline to arginine mutations in FGF receptors 1 and 3 result in Pfeiffer and Muenke craniosynostosis syndromes through enhancement of FGF binding affinity

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