Unliganded fibroblast growth factor receptor 1 forms density-independent dimers

Journal of Biological Chemistry

Volumn 290, Issue 40, 2015, Pages 24166-24177

  Comps Agrar, Laëtitia ^a   Dunshee, Diana Ronai ^a   Eaton, Dan L ^a   Sonoda, Junichiro ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; CELL CULTURE; CELL MEMBRANES; CELLS; DIMERIZATION; ENERGY TRANSFER; ENZYME ACTIVITY; FIBROBLASTS; GROWTH KINETICS; LIGANDS;

EPIDERMAL GROWTH FACTOR RECEPTORS; EXTRACELLULAR DOMAINS; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTORS; INTRACELLULAR SIGNALING; PATHOGENIC MUTATION; RESONANCE ENERGY TRANSFER; TRANS-MEMBRANE DOMAINS;

CYTOLOGY;

DIMER; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FGFR1 PROTEIN, HUMAN; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 21; KLB PROTEIN, HUMAN; LIGAND; MEMBRANE PROTEIN; PROTEIN BINDING;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL DENSITY; CELL SURFACE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DIMERIZATION; FLOW CYTOMETRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; LIGAND BINDING; MEMBRANE STRUCTURE; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; CELL MEMBRANE; CHEMISTRY; CHLOROCEBUS AETHIOPS; COS CELL LINE; DNA MUTATIONAL ANALYSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; METABOLISM; MUTATION; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; STRUCTURE ACTIVITY RELATION;

ANIMALS; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; DNA MUTATIONAL ANALYSIS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROBLAST GROWTH FACTORS; FLOW CYTOMETRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; LIGANDS; MEMBRANE PROTEINS; MUTATION; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84943302962     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.681395     Document Type: Article

References (58)

1. Lemmon, M. A., and Schlessinger, J. (2010) Cell signaling by receptor-tyrosine kinases. Cell 141, 1117-1134
2. Mohammadi, M., and Olsen., S. K., and Ibrahimi, O. A. (2005) Structural basis for fibroblast growth factor receptor activation. Cytokine Growth Factor Rev. 16, 107-137
3. Beenken, A., and Mohammadi, M. (2009) The FGF family: biology, pathophysiology, and therapy. Nat. Rev. DrugDiscov. 8, 235-253
4. Goetz, R., and Mohammadi, M. (2013) Exploring mechanisms of FGF signalling through the lens of structural biology. Nat. Rev. Mol. Cell Biol. 14, 166-180
5. Itoh, N, and Ornitz, D. M. (2004) Evolution of the Fgf and Fgfr gene families. Trends Genet. 20, 563-569
6. Itoh, N, and Ornitz, D. M. (2011) Fibroblast growth factors: from molecular evolution to roles in development, metabolism, and disease. J. Biochem 149, 121-130
7. Beenken, A., and Mohammadi, M. (2012) The structural biology of the FGF19 subfamily. Adv. Exp. Med. Biol. 728, 1-24
8. Kuro-o, M. (2012) Klotho and βKlotho. Adv. Exp. Med. Biol. 728, 25-40
9. Kurosu, H., Choi, M., Ogawa, Y., Dickson, A. S., Goetz, R., Eliseenkova, A. V., Mohammadi, M., Rosenblatt, K. P., Kliewer, S. A., and Kuro-o, M. (2007) 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
10. Kharitonenkov, A., and Dunbar., J. D., Bina, H. A., Bright, S., Moyers, J. S., Zhang, C, Ding, L., Micanovic, R., Mehrbod, S. F., Knierman, M. D., Hale, J. E., Coskun, T., and Shanafelt, A. B. (2008) FGF-21/FGF-21 receptor interaction and activation is determined by βKlotho. J. Cell Physiol. 215, 1-7
11. Kolumam, G., and Chen., M. Z., Tong, R., Zavala-Solorio, J., Kates, L., van Bruggen, N, Ross, J., Wyatt, S. K., Gandham, V. D., Carano, R. A., Dunshee, D. R., Wu, A. L., Haley, B., Anderson, K., Warming, S., Rairdan, X. Y., Lewin-Koh, N, Zhang, Y., Gutierrez, J., Baruch, A., Gelzleichter, T. R., Stevens, D., Rajan, S., Bainbridge, T. W., Vernes, J. M., Meng, Y. G., Ziai, J., Soriano, R. H., Brauer, M. J., Chen, Y., Stawicki, S., Kim, H. S., CompsAgrar, L., Luis, E., Spiess, C, Wu, Y., Ernst, J. A., McGuinness, O. P., Peterson, A. S., and Sonoda, J. (2015) Sustained brown fat stimulation and insulin sensitization by a humanized bispecific antibody agonist for fibroblast growth factor receptor 1/βKlotho complex. EBioMedicine 2, 730-743
12. Turner, N, and Grose, R. (2010) Fibroblast growth factor signalling: from development to cancer. Nat. Rev. Cancer 10, 116-129
13. White, K. E., and Cabral., J. M., Davis, S. I., Fishburn, T., Evans, W. E., Ichikawa, S., Fields, J., Yu, X., Shaw, N.J., McLellan, N.J., McKeown, C, Fitzpatrick, D., Yu, K., Ornitz, D. M., and Econs, M. J. (2005) Mutations that cause osteoglophonic dysplasia define novel roles for FGFR1 in bone elongation. Am. J. Hum. Genet. 76, 361-367
14. Kelleher, F. C, O'Sullivan, H., Smyth, E., McDermott, R., and Viterbo, A. (2013) Fibroblast growth factor receptors, developmental corruption and malignant disease. Carcinogenesis 34, 2198-2205
15. Du, X., Xie, Y., Xian, C. J., and Chen, L. (2012) Role of FGFs/FGFRs in skeletal development and bone regeneration. J. Cell Physiol. 227, 3731-3743
16. Zhang, J., and Li, Y. (2014) Fibroblast growth factor 21, the endocrine FGF pathway and novel treatments for metabolic syndrome. Drug Discov. Today 19, 579-589
17. Wu, A. L., Kolumam, G., Stawicki, S., Chen, Y., Li, J., Zavala-Solorio, J., Phamluong, K., Feng, B., Li, L., Marsters, S., Kates, L., van Bruggen, N, Leabman, M., Wong, A., West, D., Stern, H., Luis, E., Kim, H. S., Yansura, D., Peterson, A. S., Filvaroff, E., Wu, Y., and Sonoda, J. (2011) Amelioration of type 2 diabetes by antibody-mediated activation of fibroblast growth factor receptor 1. Sci. Transl. Med. 3, 113ra126
18. Lee, P. L., and Johnson., D. E., Cousens, L. S., Fried, V. A., and Williams, L. T. (1989) Purification and complementary DNA cloning of a receptor for basic fibroblast growth factor. Science 245, 57-60
19. Kiselyov, V. V., Bock, E., Berezin, V., and Poulsen, F. M. (2006) NMR structure of the first Ig module of mouse FGFR1. Protein Sci. 15, 1512-1515
20. Olsen, S. K., and Ibrahimi., O. A., Raucci, A., Zhang, F., Eliseenkova, A. V., Yayon, A., Basilico, C, and Linhardt., R. J., Schlessinger, J., and Mohammadi, M. (2004) Insights into the molecular basis for fibroblast growth factor receptor autoinhibition and ligand-binding promiscuity. Proc. Natl. Acad. Sci. U.S.A. 101, 935-940
21. Plotnikov, A. N, Hubbard, S. R., Schlessinger, J., and Mohammadi, M. (2000) Crystal structures of two FGF-FGFR complexes reveal the determinants of ligand-receptor specificity. Cell 101, 413-424
22. Plotnikov, A. N, Schlessinger, J., and Hubbard., S. R., and Mohammadi, M. (1999) Structural basis for FGF receptor dimerization and activation. Cell 98, 641-650
23. Schlessinger, J., Plotnikov, A. N, Ibrahimi, O. A., Eliseenkova, A. V., Yeh, B. K., Yayon, A., Linhardt, R. J., and Mohammadi, M. (2000) 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
24. Bocharov, E. V., and Lesovoy., D. M., Goncharuk, S. A., Goncharuk, M. V., Hristova, K., and Arseniev, A. S. (2013) Structure of FGFR3 transmembrane domain dimer: implications for signaling and human pathologies. Structure 21, 2087-2093
25. Chen, L., Placone, J., Novicky, L., and Hristova, K. (2010) The extracellular domain of fibroblast growth factor receptor 3 inhibits ligand-independent dimerization. Sci. Signal 3, ra86
26. Lin, C. C, Melo, F. A., Ghosh, R., Suen, K. M., Stagg, L. J., Kirkpatrick, J., Arold, S. T., Ahmed, Z., and Ladbury, J. E. (2012) Inhibition of basal FGF receptor signaling by dimeric Grb2. Cell 149, 1514-1524
27. Belov, A. A., and Mohammadi, M. (2012) Grb2, a double-edged sword of receptor-tyrosine kinase signaling. Sci. Signal. 5, pe49
28. Yie, J., Wang, W., Deng, L., Tam, L. T., Stevens, J., Chen, M. M., Li, Y., Xu, J., Lindberg, R., Hecht, R., Véniant, M., Chen, C, and Wang, M. (2012) Understanding the physical interactions in the FGF21/FGFR/β-Klotho complex: structural requirements and implications in FGF21 signaling. Chem. Biol. Drug Des. 79, 398-410
29. Maurel, D., Comps-Agrar, L., Brock, C, and Rives., M. L., Bourrier, E., Ayoub, M. A., Bazin, H., Tinel, N., Durroux, T., Prézeau, L., Trinquet, E., and Pin, J. P. (2008) Cell-surface protein-protein interaction analysis with time-resolved FRET and snap-tag technologies: application to GPCR oligomerization. Nat. Methods 5, 561-567
30. Monnier, C, Tu, H., Bourrier, E., Vol, C, Lamarque, L., Trinquet, E., Pin, J. P., and Rondard, P. (2011) Trans-activation between 7TM domains: implication in heterodimeric GABAB receptor activation. EMBO J. 30, 32-42
31. Doumazane, E., Scholler, P., Zwier, J. M., Trinquet, E., Rondard, P., and Pin, J. P. (2011) A new approach to analyze cell surface protein complexes reveals specific heterodimeric metabotropic glutamate receptors. FASEB J. 25, 66-77
32. Comps-Agrar, L., Kniazeff, J., Brock, C, Trinquet, E., and Pin, J. P. (2012) Stability of GABAB receptor oligomers revealed by dual TR-FRET and drug-induced cell surface targeting. FASEB J. 26, 3430-3439
33. Keppler, A., Gendreizig, S., Gronemeyer, T., Pick, H., Vogel, H., and Johnsson, K. (2003) A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat. Biotechnol. 21, 86-89
34. George, N., Pick, H., Vogel, H., Johnsson, N., and Johnsson, K. (2004) Specific labeling of cell surface proteins with chemically diverse compounds. J. Am. Chem. Soc. 126, 8896-8897
35. Selvin, P. R. (2002) Principles and biophysical applications of lanthanide-based probes. Annu. Rev. Biophys. Biomol. Struct. 31, 275-302
36. Zwier, J. M., Bazin, H., Lamarque, L., and Mathis, G. (2014) Luminescent lanthanide cryptates: from the bench to the bedside. Inorg. Chem. 53, 1854-1866
37. Mathis, G. (1995) Probing molecular interactions with homogeneous techniques based on rare earth cryptates and fluorescence energy transfer. Clin. Chem. 41, 1391-1397
38. Arkhipov, A., Shan, Y., Das, R., Endres, N. F., Eastwood, M. P., Wemmer, D. E., Kuriyan, J., and Shaw, D. E. (2013) Architecture and membrane interactions of the EGF receptor. Cell 152, 557-569
39. Endres, N. F., Das, R., Smith, A. W., Arkhipov, A., Kovacs, E., Huang, Y., Pelton, J. G., Shan, Y., Shaw, D. E., Wemmer, D. E., Groves, J. T., and Kuriyan, J. (2013) Conformational coupling across the plasma membrane in activation of the EGF receptor. Cell 152, 543-556
40. Chung, I., Akita, R., Vandlen, R., Toomre, D., Schlessinger, J., and Mellman, I. (2010) Spatial control of EGF receptor activation by reversible dimerization on living cells. Nature 464, 783-787
41. Haugsten, E. M., Wiedlocha, A., Olsnes, S., and Wesche, J. (2010) Roles of fibroblast growth factor receptors in carcinogenesis. Mol. Cancer Res. 8, 1439-1452
42. Li, E., and Hristova, K. (2006) Role of receptor-tyrosine kinase transmembrane domains in cell signaling and human pathologies. Biochemistry 45, 6241-6251
43. Rand, V., Huang, J., Stockwell, T., Ferriera, S., Buzko, O., Levy, S., Busam, D., Li, K., Edwards, J. B., Eberhart, C, and Murphy., K. M., Tsiamouri, A., Beeson, K., Simpson, A. J., Venter, J. C, Riggins, G. J., and Strausberg, R. L. (2005) Sequence survey of receptor-tyrosine kinases reveals mutations in glioblastomas. Proc. Natl. Acad. Sci. U.S.A. 102, 14344-14349
44. Jones, D. T., Hutter, B., Jäger, N., Korshunov, A., Kool, M., Warnatz, H. J., Zichner, T., Lambert, S. R., Ryzhova, M., Quang, D. A., Fontebasso, A. M., Stütz, A. M., Hutter, S., Zuckermann, M., Sturm, D., Gronych, J., Lasitschka, B., Schmidt, S., Seker-Cin, H., Witt, H., Sultan, M., Ralser, M., Northcott, P. A., Hovestadt, V., Bender, S., Pfaff, E., Stark, S., Faury, D., Schwartzentruber, J., Majewski, J., Weber, U. D., Zapatka, M., Raeder, B., Schlesner, M., Worth, C. L., Bartholomae, C. C, von Kalle, C, Imbusch, C. D., Radomski, S., Lawerenz, C, van Sluis, P., Koster, J., Volckmann, R., Versteeg, R., Lehrach, H., Monoranu, C, Winkler, B., Unterberg, A., Herold-Mende, C, Milde, T., Kulozik, A. E., Ebinger, M., Schuhmann, M. U., Cho, Y. J., Pomeroy, S. L., von Deimling, A., Witt, O., Taylor, M. D., Wolf, S., Karajannis, M. A., Eberhart, C. G., Scheurlen, W., Hasselblatt, M., Ligon, K. L., Kieran, M. W., Korbel, J. O., Yaspo, M. L., Brors, B., Felsberg, J., Reifenberger, G., Collins, V. P., Jabado, N., Eils, R., Lichter, P., and Pfister, S. M. (2013) Recurrent somatic alterations of FGFR1 and NTRK2 in pilocytic astrocytoma. Nat. Genet. 45, 927-932
45. Lew, E. D., and Furdui., C. M., Anderson, K. S., and Schlessinger, J. (2009) The precise sequence of FGF receptor autophosphorylation is kinetically driven and is disrupted by oncogenic mutations. Sci. Signal 2, ra6
46. Webster, M. K., and D'Avis., P. Y., Robertson, S. C, and Donoghue, D. J. (1996) Profound ligand-independent kinase activation of fibroblast growth factor receptor 3 by the activation loop mutation responsible for a lethal skeletal dysplasia, thanatophoric dysplasia type II. Mol. Cell. Biol. 16, 4081-4087
47. Kan, M., Wang, F., To, B., Gabriel, J. L., and McKeehan, W. L. (1996) Divalent cations and heparin/heparan sulfate cooperate to control assembly and activity of the fibroblast growth factor receptor complex. J. Biol. Chem. 271, 26143-26148
48. Wang, F., Kan, M., McKeehan, K., Jang, J. H, Feng, S., and McKeehan, W. L. (1997) A homeo-interaction sequence in the ectodomain of the fibroblast growth factor receptor. J. Biol. Chem. 272, 23887-23895
49. McKeehan, W. L., Wang, F., and Kan, M. (1998) The heparan sulfatefibroblast growth factor family: diversity of structure and function. Prog. Nucleic Acid Res. Mol. Biol. 59, 135-176
50. Ballinger, M. D., Shyamala, V., Forrest, L. D., Deuter-Reinhard, M., Doyle, L. V., and Wang., J. X., Panganiban-Lustan, L., Stratton, J. R., Apell, G., and Winter., J. A., Doyle, M. V, Rosenberg, S., and Kavanaugh, W. M. (1999) Semirational design of a potent, artificial agonist of fibroblast growth factor receptors. Nat Biotechnol. 17, 1199-1204
51. Welm, B. E., and Freeman., K. W., Chen, M., Contreras, A., Spencer, D.M., and Rosen, J. M. (2002) Inducible dimerization of FGFR1: development of a mouse model to analyze progressive transformation of the mammary gland. J. Cell Biol. 157, 703-714
52. Lemmon, M. A., Schlessinger, J., and Ferguson, K. M. (2014) The EGFR family: not so prototypical receptor-tyrosine kinases. Cold Spring Harb. Perspect. Biol. 6, a020768
53. Ming, A.Y., Yoo, E., Vorontsov, E.N., Altamentova, S.M., Kilkenny, D.M., and Rocheleau, J. V. (2012) Dynamics and Distribution of Klothoβ (KLB) and fibroblast growth factor receptor-1 (FGFR1) in living cells reveal the fibroblast growth factor-21 (FGF21)-induced receptor complex. J. Biol. Chem. 287, 19997-20006
54. Sarabipour, S., and Hristova, K. (2015) FGFR3 unliganded dimer stabilization by the juxtamembrane domain. J. Mol. Biol. 427, 1705-1714
55. Placone, J., and Hristova, K. (2012) Direct assessment of the effect of the Gly380Arg achondroplasia mutation on FGFR3 dimerization using quantitative imaging FRET. PLoS ONE 7, e46678
56. Mohammadi, M., and Olsen., S. K., and Goetz, R. (2005) A protein canyon in the FGF-FGF receptor dimer selects from an a la carte menu of heparan sulfate motifs. Curr. Opin. Struct. Biol. 15, 506-516
57. Gao, G., and Goldfarb, M. (1995) Heparin can activate a receptor-tyrosine kinase. EMBO J. 14, 2183-2190
58. Ogawa, Y., Kurosu, H., Yamamoto, M., Nandi, A., and Rosenblatt., K. P., Goetz, R., Eliseenkova, A. V., Mohammadi, M., and Kuro-o, M. (2007) βKlotho is required for metabolic activity of fibroblast growth factor 21. Proc. Natl. Acad. Sci. U.S.A. 104, 7432-7437