Isoform-specific inhibition of FGFR signaling achieved by a de-novo-designed mini-protein

Park, Joon Sung; Choi, Jungyuen; Cao, Longxing; Mohanty, Jyotidarsini; Suzuki, Yoshihisa; Park, Andy; Baker, David; Schlessinger, Joseph; Lee, Sangwon

doi:10.1016/j.celrep.2022.111545

Isoform-specific inhibition of FGFR signaling achieved by a de-novo-designed mini-protein

Journal Article · 01 October 2022 · Cell Reports

DOI:https://doi.org/10.1016/j.celrep.2022.111545· OSTI ID:1902361

Park, Joon Sung; Choi, Jungyuen; Cao, Longxing; Mohanty, Jyotidarsini; Suzuki, Yoshihisa; Park, Andy; Baker, David; Schlessinger, Joseph; Lee, Sangwon

Research Organization:: Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)

Sponsoring Organization:: DOE - Office Of Science; NCI; NIH

OSTI ID:: 1902361

Journal Information:: Cell Reports, Journal Name: Cell Reports Journal Issue: (4) Vol. 41

Country of Publication:: United States

Language:: ENGLISH

References (51)

Structural Basis for FGF Receptor Dimerization and Activation Plotnikov, Alexander N.; Schlessinger, Joseph; Hubbard, Stevan R. Cell, Vol. 98, Issue 5 https://doi.org/10.1016/S0092-8674(00)80051-3	journal	September 1999
Acquired On-Target Clinical Resistance Validates FGFR4 as a Driver of Hepatocellular Carcinoma Hatlen, Megan A.; Schmidt-Kittler, Oleg; Sherwin, Cori Ann Cancer Discovery, Vol. 9, Issue 12 https://doi.org/10.1158/2159-8290.CD-19-0367	journal	December 2019
Molecular Insights into the Klotho-Dependent, Endocrine Mode of Action of Fibroblast Growth Factor 19 Subfamily Members Goetz, R.; Beenken, A.; Ibrahimi, O. A. Molecular and Cellular Biology, Vol. 27, Issue 9 https://doi.org/10.1128/MCB.02249-06	journal	March 2007
H3B-6527 Is a Potent and Selective Inhibitor of FGFR4 in FGF19-Driven Hepatocellular Carcinoma Joshi, Jaya Julie; Coffey, Heather; Corcoran, Erik Cancer Research, Vol. 77, Issue 24 https://doi.org/10.1158/0008-5472.CAN-17-1865	journal	December 2017
Crystal Structures of Two FGF-FGFR Complexes Reveal the Determinants of Ligand-Receptor Specificity Plotnikov, Alexander N.; Hubbard, Stevan R.; Schlessinger, Joseph Cell, Vol. 101, Issue 4 https://doi.org/10.1016/S0092-8674(00)80851-X	journal	May 2000
Heparan Sulfate-Dependent Signaling of Fibroblast Growth Factor 18 by Chondrocyte-Derived Perlecan Chuang, Christine Y.; Lord, Megan S.; Melrose, James Biochemistry, Vol. 49, Issue 26 https://doi.org/10.1021/bi1005199	journal	June 2010
NMR structure of the first Ig module of mouse FGFR1 Kiselyov, Vladislav V.; Bock, Elisabeth; Berezin, Vladimir Protein Science, Vol. 15, Issue 6 https://doi.org/10.1110/ps.062207906	journal	June 2006
Insights into the molecular basis for fibroblast growth factor receptor autoinhibition and ligand-binding promiscuity Olsen, Shaun K.; Ibrahimi, Omar A.; Raucci, Angela Proceedings of the National Academy of Sciences, Vol. 101, Issue 4 https://doi.org/10.1073/pnas.0307287101	journal	January 2004
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
The Fibroblast Growth Factor signaling pathway Ornitz, David M.; Itoh, Nobuyuki Wiley Interdisciplinary Reviews: Developmental Biology, Vol. 4, Issue 3 https://doi.org/10.1002/wdev.176	journal	March 2015
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Plasticity in Interactions of Fibroblast Growth Factor 1 (FGF1) N Terminus with FGF Receptors Underlies Promiscuity of FGF1 Beenken, Andrew; Eliseenkova, Anna V.; Ibrahimi, Omar A. Journal of Biological Chemistry, Vol. 287, Issue 5 https://doi.org/10.1074/jbc.M111.275891	journal	November 2011
Lenvatinib inhibits angiogenesis and tumor fibroblast growth factor signaling pathways in human hepatocellular carcinoma models Matsuki, Masahiro; Hoshi, Taisuke; Yamamoto, Yuji Cancer Medicine, Vol. 7, Issue 6 https://doi.org/10.1002/cam4.1517	journal	May 2018
Tissue-specific Expression of βKlotho and Fibroblast Growth Factor (FGF) Receptor Isoforms Determines Metabolic Activity of FGF19 and FGF21 Kurosu, Hiroshi; Choi, Mihwa; Ogawa, Yasushi Journal of Biological Chemistry, Vol. 282, Issue 37 https://doi.org/10.1074/jbc.M704165200	journal	July 2007
Antibody-based targeting of FGFR3 in bladder carcinoma and t(4;14)-positive multiple myeloma in mice Qing, Jing; Du, Xiangnan; Chen, Yongmei Journal of Clinical Investigation, Vol. 119, Issue 5 https://doi.org/10.1172/JCI38017	journal	May 2009
Co-receptor Requirements for Fibroblast Growth Factor-19 Signaling Wu, Xinle; Ge, Hongfei; Gupte, Jamila Journal of Biological Chemistry, Vol. 282, Issue 40 https://doi.org/10.1074/jbc.C700130200	journal	October 2007
Indirect recruitment of the signalling adaptor Shc to the fibroblast growth factor receptor 2 (FGFR2) Schüller, Annika C.; Ahmed, Zamal; Levitt, James A. Biochemical Journal, Vol. 416, Issue 2 https://doi.org/10.1042/BJ20080887	journal	November 2008
Receptor subtype discrimination using extensive shape complementary designed interfaces Dang, Luke T.; Miao, Yi; Ha, Andrew Nature Structural & Molecular Biology, Vol. 26, Issue 6 https://doi.org/10.1038/s41594-019-0224-z	journal	May 2019
Identification of a Therapeutic Strategy Targeting Amplified FGF19 in Liver Cancer by Oncogenomic Screening Sawey, Eric T.; Chanrion, Maia; Cai, Chunlin Cancer Cell, Vol. 19, Issue 3 https://doi.org/10.1016/j.ccr.2011.01.040	journal	March 2011
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Fibroblast growth factor 15 functions as an enterohepatic signal to regulate bile acid homeostasis Inagaki, Takeshi; Choi, Mihwa; Moschetta, Antonio Cell Metabolism, Vol. 2, Issue 4 https://doi.org/10.1016/j.cmet.2005.09.001	journal	October 2005
Structures of ligand-occupied β-Klotho complexes reveal a molecular mechanism underlying endocrine FGF specificity and activity Kuzina, Ekaterina S.; Ung, Peter Man-Un; Mohanty, Jyotidarsini Proceedings of the National Academy of Sciences, Vol. 116, Issue 16 https://doi.org/10.1073/pnas.1822055116	journal	April 2019
Roles of FGF19 in Liver Metabolism Kir, S.; Kliewer, S. A.; Mangelsdorf, D. J. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 76, Issue 0 https://doi.org/10.1101/sqb.2011.76.010710	journal	January 2011
FGF401, A First-In-Class Highly Selective and Potent FGFR4 Inhibitor for the Treatment of FGF19-Driven Hepatocellular Cancer Weiss, Andreas; Adler, Flavia; Buhles, Alexandra Molecular Cancer Therapeutics, Vol. 18, Issue 12 https://doi.org/10.1158/1535-7163.MCT-18-1291	journal	August 2019
First-in-Human Phase I Study of Fisogatinib (BLU-554) Validates Aberrant FGF19 Signaling as a Driver Event in Hepatocellular Carcinoma Kim, Richard D.; Sarker, Debashis; Meyer, Tim Cancer Discovery, Vol. 9, Issue 12 https://doi.org/10.1158/2159-8290.CD-19-0555	journal	October 2019
First Selective Small Molecule Inhibitor of FGFR4 for the Treatment of Hepatocellular Carcinomas with an Activated FGFR4 Signaling Pathway Hagel, M.; Miduturu, C.; Sheets, M. Cancer Discovery, Vol. 5, Issue 4 https://doi.org/10.1158/2159-8290.CD-14-1029	journal	March 2015
Cell Signaling by Receptor Tyrosine Kinases Lemmon, Mark A.; Schlessinger, Joseph Cell, Vol. 141, Issue 7 https://doi.org/10.1016/j.cell.2010.06.011	journal	June 2010
Shape Complementarity at Protein/Protein Interfaces Lawrence, Michael C.; Colman, Peter M. Journal of Molecular Biology, Vol. 234, Issue 4 https://doi.org/10.1006/jmbi.1993.1648	journal	December 1993
Structural basis by which alternative splicing modulates the organizer activity of FGF8 in the brain Olsen, S. K. Genes & Development, Vol. 20, Issue 2 https://doi.org/10.1101/gad.1365406	journal	January 2006
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation Spivak-Kroizman, T.; Lemmon, M. A.; Dikic, I. Cell, Vol. 79, Issue 6 https://doi.org/10.1016/0092-8674(94)90032-9	journal	December 1994
Targeting FGF19 inhibits tumor growth in colon cancer xenograft and FGF19 transgenic hepatocellular carcinoma models Desnoyers, L. R.; Pai, R.; Ferrando, R. E. Oncogene, Vol. 27, Issue 1 https://doi.org/10.1038/sj.onc.1210623	journal	June 2007
Design of protein-binding proteins from the target structure alone Cao, Longxing; Coventry, Brian; Goreshnik, Inna Nature, Vol. 605, Issue 7910 https://doi.org/10.1038/s41586-022-04654-9	journal	March 2022
Structural basis for fibroblast growth factor receptor 2 activation in Apert syndrome Ibrahimi, Omar A.; Eliseenkova, Anna V.; Plotnikov, Alexander N. Proceedings of the National Academy of Sciences, Vol. 98, Issue 13 https://doi.org/10.1073/pnas.121183798	journal	June 2001
Structures of β-klotho reveal a ‘zip code’-like mechanism for endocrine FGF signalling Lee, Sangwon; Choi, Jungyuen; Mohanty, Jyotidarsini Nature, Vol. 553, Issue 7689 https://doi.org/10.1038/nature25010	journal	January 2018
α-Klotho is a non-enzymatic molecular scaffold for FGF23 hormone signalling Chen, Gaozhi; Liu, Yang; Goetz, Regina Nature, Vol. 553, Issue 7689 https://doi.org/10.1038/nature25451	journal	January 2018
Receptor Specificity of the Fibroblast Growth Factor Family: THE COMPLETE MAMMALIAN FGF FAMILY Zhang, Xiuqin; Ibrahimi, Omar A.; Olsen, Shaun K. Journal of Biological Chemistry, Vol. 281, Issue 23 https://doi.org/10.1074/jbc.M601252200	journal	April 2006
Receptor Specificity of the Fibroblast Growth Factor Family Ornitz, David M.; Xu, Jingsong; Colvin, Jennifer S. Journal of Biological Chemistry, Vol. 271, Issue 25 https://doi.org/10.1074/jbc.271.25.15292	journal	June 1996
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444912001308	journal	March 2012
Targeting FGFR4 Inhibits Hepatocellular Carcinoma in Preclinical Mouse Models French, Dorothy M.; Lin, Benjamin C.; Wang, Manping PLoS ONE, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pone.0036713	journal	May 2012
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Ligand specificity and heparin dependence of fibroblast growth factor receptors 1 and 3. Ornitz, D. M.; Leder, P. Journal of Biological Chemistry, Vol. 267, Issue 23 https://doi.org/10.1016/S0021-9258(18)42001-7	journal	August 1992
Crystal Structure of a Ternary FGF-FGFR-Heparin Complex Reveals a Dual Role for Heparin in FGFR Binding and Dimerization Schlessinger, Joseph; Plotnikov, Alexander N.; Ibrahimi, Omar A. Molecular Cell, Vol. 6, Issue 3 https://doi.org/10.1016/S1097-2765(00)00073-3	journal	September 2000
A Mouse Model of Hepatocellular Carcinoma Nicholes, Katrina; Guillet, Susan; Tomlinson, Elizabeth The American Journal of Pathology, Vol. 160, Issue 6 https://doi.org/10.1016/S0002-9440(10)61177-7	journal	June 2002
Cellular signaling by fibroblast growth factor receptors Eswarakumar, V. P.; Lax, I.; Schlessinger, J. Cytokine & Growth Factor Reviews, Vol. 16, Issue 2 https://doi.org/10.1016/j.cytogfr.2005.01.001	journal	April 2005
Novel Recognition Motif on Fibroblast Growth Factor Receptor Mediates Direct Association and Activation of SNT Adapter Proteins Xu, Hong; Lee, Kyung W.; Goldfarb, Mitchell Journal of Biological Chemistry, Vol. 273, Issue 29 https://doi.org/10.1074/jbc.273.29.17987	journal	July 1998
FGF19 and Cancer Lin, Benjamin C.; Desnoyers, Luc R. Advances in Experimental Medicine and Biology https://doi.org/10.1007/978-1-4614-0887-1_12	book	January 2012
Heparin/Heparan Sulfate Domains in Binding and Signaling of Fibroblast Growth Factor 8b Loo, Britt-Marie; Salmivirta, Markku Journal of Biological Chemistry, Vol. 277, Issue 36 https://doi.org/10.1074/jbc.M204961200	journal	September 2002
Cell Signaling by Receptor Tyrosine Kinases Schlessinger, Joseph Cell, Vol. 103, Issue 2 https://doi.org/10.1016/S0092-8674(00)00114-8	journal	October 2000

Similar Records

De novo design of functional proteins: Toward artificial hydrogenases: De Novo Design of Functional Proteins

Journal Article · 2013 · Biopolymers · OSTI ID:1383174

De novo design of drug-binding proteins with predictable binding energy and specificity

Journal Article · 2024 · Science · OSTI ID:2582765

De novo protein design by deep network hallucination

Journal Article · 2021 · Nature · OSTI ID:1844737

Isoform-specific inhibition of FGFR signaling achieved by a de-novo-designed mini-protein

Citation Formats

References (51)

Similar Records

Related Subjects