Coupling of transmembrane helix orientation to membrane release of the Juxtamembrane Region in FGFR3

Biochemistry

Volumn 53, Issue 30, 2014, Pages 5000-5007

  Tamagaki, Hiroko ^a   Furukawa, Yusuke ^a   Yamaguchi, Ritsuko ^a   Hojo, Hironobu ^a   Aimoto, Saburo ^a   Smith, Steven O ^b   Sato, Takeshi ^a  

^a OSAKA UNIVERSITY   (Japan)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CHEMICAL ACTIVATION; ENZYME ACTIVITY; FOURIER TRANSFORM INFRARED SPECTROSCOPY;

FIBROBLAST GROWTH FACTOR RECEPTORS; MEMBRANE SURFACE; PROTEIN TYROSINE KINASE; RECEPTOR ACTIVATION; RECEPTOR KINASE; TRANSMEMBRANE HELICES; TRANSMEMBRANES; TRANSPHOSPHORYLATION;

ENZYME INHIBITION;

AMINO ACID SEQUENCE; CELL MEMBRANE; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 3;

EID: 84905686652     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500327q     Document Type: Article

References (45)

1. Eswarakumar, V. P., Lax, I., and Schlessinger, J. (2005) Cellular signaling by fibroblast growth factor receptors Cytokine Growth Factor Rev. 16, 139-149
2. Plotnikov, A. N., Schlessinger, J., Hubbard, S. R., and Mohammadi, M. (1999) Structural basis for FGF receptor dimerization and activation Cell 98, 641-650
3. 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
4. Bae, J. H., Boggon, T. J., Tome, F., Mandiyan, V., Lax, I., and Schlessinger, J. (2010) Asymmetric receptor contact is required for tyrosine autophosphorylation of fibroblast growth factor receptor in living cells Proc. Natl. Acad. Sci. U. S. A. 107, 2866-2871
5. Chen, H. B., Xu, C. F., Ma, J. H., Eliseenkova, A. V., Li, W. Q., Pollock, P. M., Pitteloud, N., Miller, W. T., Neubert, T. A., and Mohammadi, M. (2008) A crystallographic snapshot of tyrosine trans-phosphorylation in action Proc. Natl. Acad. Sci. U. S. A. 105, 19660-19665
6. Mohammadi, M., Olsen, S. K., and Ibrahimi, O. A. (2005) Structural basis for fibroblast growth factor receptor activation Cytokine Growth Factor Rev. 16, 107-137
7. Endres, N. F., Das, R., Smith, A. W., Arkhipov, A., Kovacs, E., Huang, Y. J., Pelton, J. G., Shan, Y. B., 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
8. Arkhipov, A., Shan, Y. B., 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
9. Macdonald-Obermann, J. L. and Pike, L. J. (2009) The intracellular juxtamembrane domain of the epidermal growth factor (EGF) receptor is responsible for the allosteric regulation of EGF binding J. Biol. Chem. 284, 13570-13576
10. Macdonald-Obermann, J. L. and Pike, L. J. (2009) Palmitoylation of the EGF receptor impairs signal transduction and abolishes high-affinity ligand binding Biochemistry 48, 2505-2513
11. Matsushita, C., Tamagaki, H., Miyazawa, Y., Aimoto, S., Smith, S. O., and Sato, T. (2013) Transmembrane helix orientation influences membrane binding of the intracellular juxtamembrane domain in Neu receptor peptides Proc. Natl. Acad. Sci. U. S. A. 110, 1646-1651
12. Meyers, G. A., Orlow, S. J., Munro, I. R., Przylepa, K. A., and Jabs, E. W. (1995) Fibroblast growth factor receptor 3 (FGFR3) transmembrane mutation in crouzon-syndrome with acanthosis nigricans Nat. Genet. 11, 462-464
13. van Rhijn, B. W. G., van Tilborg, A. A. G., Lurkin, I., Bonaventure, J., de Vries, A., Thiery, J. P., van der Kwast, T. H., Zwarthoff, E. C., and Radvanyi, F. (2002) Novel fibroblast growth factor receptor 3 (FGFR3) mutations in bladder cancer previously identified in non-lethal skeletal disorders Eur. J. Hum. Genet. 10, 819-824
14. Li, E., You, M., and Hristova, K. (2006) FGFR3 dimer stabilization due to a single amino acid pathogenic mutation J. Mol. Biol. 356, 600-612
15. Chen, F. H., Degnin, C., Laederich, M., Horton, W. A., and Hristova, K. (2011) The A391E mutation enhances FGFR3 activation in the absence of ligand Biochim. Biophys. Acta, Biomembr. 1808, 2045-2050
16. Shiang, R., Thompson, L. M., Zhu, Y. Z., Church, D. M., Fielder, T. J., Bocian, M., Winokur, S. T., and Wasmuth, J. J. (1994) Mutations in the transmembrane domain of FGFR3 cause the most common genetic form of dwarfism, achondroplasia Cell 78, 335-342
17. You, M., Li, E., and Hristova, K. (2006) The achondroplasia mutation does not alter the dimerization energetics of the fibroblast growth factor receptor 3 transmembrane domain Biochemistry 45, 5551-5556
18. 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
19. Sato, T., Kawakami, T., Akaji, K., Konishi, H., Mochizuki, K., Fujiwara, T., Akutsu, H., and Aimoto, S. (2002) Synthesis of a membrane protein with two transmembrane regions J. Pept. Sci. 8, 172-180
20. Dawson, P. E., Muir, T. W., Clark-Lewis, I., and Kent, S. B. H. (1994) Synthesis of proteins by native chemical ligation Science 266, 776-779
21. Sato, T., Saito, Y., and Aimoto, S. (2005) Synthesis of the C-terminal region of opioid receptor like 1 in an SDS micelle by the native chemical ligation: Effect of thiol additive and SDS concentration on ligation efficiency J. Pept. Sci. 11, 410-416
22. Golebiewska, U., Gambhir, A., Hangyas-Mihalyne, G., Zaitseva, I., Radler, J., and McLaughlin, S. (2006) Membrane-bound basic peptides sequester multivalent (PIP2), but not monovalent (PS), acidic lipids Biophys. J. 91, 588-599
23. Smith, S. O., Smith, C., Shekar, S., Peersen, O., Ziliox, M., and Aimoto, S. (2002) Transmembrane interactions in the activation of the Neu receptor tyrosine kinase Biochemistry 41, 9321-9332
24. Liu, W., Eilers, M., Patel, A. B., and Smith, S. O. (2004) Helix packing moments reveal diversity and conservation in membrane protein structure J. Mol. Biol. 337, 713-729
25. Bechinger, B., Ruysschaert, J. M., and Goormaghtigh, E. (1999) Membrane helix orientation from linear dichroism of infrared attenuated total reflection spectra Biophys. J. 76, 552-563
26. Ben-Tal, N., Honig, B., Peitzsch, R. M., Denisov, G., and McLaughlin, S. (1996) Binding of small basic peptides to membranes containing acidic lipids: Theoretical models and experimental results Biophys. J. 71, 561-575
27. 2H NMR study Biochemistry 44, 1004-1012
28. 2H solid-state NMR Biophys. J. 86, 3709-3721
29. Muhle-Goll, C., Hoffmann, S., Afonin, S., Grage, S. L., Polyansky, A. A., Windisch, D., Zeitler, M., Burck, J., and Ulrich, A. S. (2012) Hydrophobic matching controls the tilt and stability of the dimeric platelet-derived growth factor receptor (PDGFR) beta transmembrane segment J. Biol. Chem. 287, 26178-26186
30. Lewis, B. A. and Engelman, D. M. (1983) Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles J. Mol. Biol. 166, 211-217
31. Liu, W., Crocker, E., Constantinescu, S. N., and Smith, S. O. (2005) Helix packing and orientation in the transmembrane dimer of gp55-P of the spleen focus forming virus Biophys. J. 89, 1194-1202
32. Sato, T., Pallavi, P., Golebiewska, U., McLaughlin, S., and Smith, S. O. (2006) Structure of the membrane reconstituted transmembrane-juxtamembrane peptide EGFR(622-660) and its interaction with Ca2+/calmodulin Biochemistry 45, 12704-12714
33. Sternberg, M. J. and Gullick, W. J. (1990) A sequence motif in the transmembrane region of growth factor receptors with tyrosine kinase activity mediates dimerization Protein Eng. 3, 245-248
34. Reddy, T., Manrique, S., Buyan, A., Hall, B. A., Chetwynd, A., and Sansom, M. S. (2014) Primary and secondary dimer interfaces of the fibroblast growth factor receptor 3 transmembrane domain: Characterization via multiscale molecular dynamics simulations Biochemistry 53, 323-332
35. Hubbard, S. R. (2004) Juxtamembrane autoinhibition in receptor tyrosine kinases Nat. Rev. Mol. Cell Biol. 5, 464-471
36. McLaughlin, S., Smith, S. O., Hayman, M. J., and Murray, D. (2005) An electrostatic engine model for autoinhibition and activation of the epidermal growth factor receptor (EGFR/ErbB) family J. Gen. Physiol. 126, 41-53
37. Sengupta, P., Bosis, E., Nachliel, E., Gutman, M., Smith, S. O., Mihalyne, G., Zaitseva, I., and McLaughlin, S. (2009) EGFR juxtamembrane domain, membranes, and calmodulin: Kinetics of their interaction Biophys. J. 96, 4887-4895
38. Michailidis, I. E., Rusinova, R., Georgakopoulos, A., Chen, Y. B., Iyengar, R., Robakis, N. K., Logothetis, D. E., and Baki, L. (2011) Phosphatidylinositol-4,5-bisphosphate regulates epidermal growth factor receptor activation Pfluegers Arch., Eur. J. Physiol. 461, 387-397
39. Martin-Nieto, J. and Villalobo, A. (1998) The human epidermal growth factor receptor contains a juxtamembrane calmodulin-binding site Biochemistry 37, 227-236
40. Mendrola, J. M., Berger, M. B., King, M. C., and Lemmon, M. A. (2002) The single transmembrane domains of ErbB receptors self-associate in cell membranes J. Biol. Chem. 277, 4704-4712
41. Russ, W. P. and Engelman, D. M. (2000) The GxxxG motif: A framework for transmembrane helix-helix association J. Mol. Biol. 296, 911-919
42. Adamian, L. and Liang, J. (2002) Interhelical hydrogen bonds and spatial motifs in membrane proteins: Polar clamps and serine zippers Proteins 47, 209-218
43. Bocharov, E. V., 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
44. Defour, J. P., Itaya, M., Gryshkova, V., Brett, I. C., Pecquet, C., Sato, T., Smith, S. O., and Constantinescu, S. N. (2013) Tryptophan at the transmembrane-cytosolic junction modulates thrombopoietin receptor dimerization and activation Proc. Natl. Acad. Sci. U. S. A. 110, 2540-2545
45. Li, E., You, M., and Hristova, K. (2005) Sodium dodecyl sulfate - Polyacrylamide gel electrophoresis and Forster resonance energy transfer suggest weak interactions between fibroblast growth factor receptor 3 (FGFR3) transmembrane domains in the absence of extracellular domains and ligands Biochemistry 44, 352-360