Sodium dodecyl sulfate-polyacrylamide gel electrophoresis and förster resonance energy transfer suggest weak interactions between fibroblast growth factor receptor 3 (FGFR3) transmembrane domains in the absence of extracellular domains and ligands

Biochemistry

Volumn 44, Issue 1, 2005, Pages 352-360

  Li, Edwin ^a   You, Min ^a   Hristova, Kalina ^a  

^a Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; CELLS; DIMERIZATION; ELECTROPHORESIS; ENERGY TRANSFER; GELS; LIPIDS;

BILAYERS; FÖRSTER RESONANCE ENERGY TRANSFER (FRET); RECEPTOR TYROSINE KINASES (RTK); TRANSMEMBRANE (TM) DOMAINS;

PROTEINS;

DIMER; FIBROBLAST GROWTH FACTOR RECEPTOR 3; FLUORESCEIN; GLYCOPHORIN A; LIGAND; MEMBRANE PROTEIN; PROTEIN TYROSINE KINASE; RHODAMINE;

ARTICLE; CELL MEMBRANE; DIMERIZATION; ENERGY TRANSFER; LIPID BILAYER; LIPID VESICLE; MUTATION; PEPTIDE SYNTHESIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; BINDING SITES; CELL MEMBRANE; CIRCULAR DICHROISM; DIMERIZATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENCE RESONANCE ENERGY TRANSFER; LIGANDS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN-TYROSINE KINASES; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 3; RECEPTORS, FIBROBLAST GROWTH FACTOR; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 11844249905     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048480k     Document Type: Article

References (51)

1. Hynes, N. E., and Stern, D. F. (1994) The biology of erbB-2/neu/ HER-2 and its role in cancer, Biochim. Biophys. Acta 1198, 165-184.
2. Cappellen, D., de Oliveira, C., Ricol, D., Diez de Medina, S. G., Bourdin, J., Sastre-Garau, X., Chopin, D., Thiery, J. P., and Radvanyi, F. (1999) Frequent activating mutations of FGFR3 in human bladder and cervix carcinomas, Nat. Genet. 23, 18-20.
3. Wilkie, A. O. M., Morriss-Kay, G. M., Jones, E. Y., and Heath, J. K. (1995) Functions of fibroblast growth factors and their receptors, Curr. Biol. 5, 500-507.
4. Schlessinger, J. (2002) Ligand-induced, receptor-mediated dimerization and activation of EGF receptor, Cell 110, 669-672.
5. Lemmon, M. A., Bu, Z. M., Ladbury, J. E., Zhou, M., Pinchasi, D., Lax, I., Engelman, D. M., and Schlessinger, J. (1997) Two EGF molecules contribute additively to stabilization of the EGFR dimer, EMBO J. 16, 281-294.
6. Spivakkroizman, T., Lemmon, M. A., Dikic, I., Ladbury, J. E., Pinchasi, D., Huang, J., Jaye, M., Crumley, G., Schlessinger, J., and Lax, I. (1994) Heparin-Induced Oligomerization of Fgf Molecules Is Responsible for Fgf Receptor Dimerization, Activation, and Cell-Proliferation, Cell 79, 1015-1024.
7. Lemmon, M. A., and Schlessinger, J. (1994) Regulation of Signal-Transduction and Signal Diversity by Receptor Oligomerization, Trends Biochem. Sci. 19, 459-463.
8. Lemmon, M. A., and Engelman, D. M. (1994) Specificity and promiscuity in membrane helix interactions, Q. Rev. Biophys. 27, 157-218.
9. Tanner, K. G., and Kyte, J. (1999) Dimerization of the extracellular domain of the receptor for epidermal growth factor containing the membrane-spanning segment in response to treatment with epidermal growth factor, J. Biol. Chem. 274, 35985-35990.
10. Miloso, M., Mazzotti, M., Vass, W. C., and Beguinot, L. (1995) SHC and GRB-2 are constitutively activated by an epidermal growth factor receptor with a point mutation in the transmembrane domain, J. Biol. Chem. 270, 19557-19562.
11. Bange, J., Prechtl, D., Cheburkin, Y., Specht, K., Harbeck, N., Schmitt, M., Knyazeva, T., Muller, S., Gartner, S., Sures, I., Wang, H. Y., Imyanitov, E., Haring, H. U., Knayzev, P., Iacobelli, S., Hofler, H., and Ullrich, A. (2002) Cancer progression and tumor cell motility are associated with the FGFR4 Arg(388) allele, Cancer Res. 62, 840-847.
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 Rhijin, B., van Tilborg, A., Lurkin, I., Bonaventure, J., de Vries, A., Thiery, J. P., van der Kwast, T. H., Zwarthoff, E., and Radvanyi, F. (2002) Novel fibroblast growth factor receptor 3 (FGFR3) mutations in bladder cancer previously identified in nonlethal skeletal disorders, Eur. J. Hum. Genet. 10, 819-824.
14. 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.
15. Segatto, O., King, C. R., Pierce, J. H., di Fiore, P. P., and Aaronson, S. A. (1988) Different structural alterations upregulate in vitro tyrosine kinase activity and transforming potency of the erbB-2 gene, Mol. Cell. Biol. 8, 5570-5574.
16. 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.
17. Vajo, Z., Francomano, C. A., and Wilkin, D. J. (2000) The molecular and genetic basis of fibroblast growth factor receptor 3 disorders: The achondroplasia family of skeletal dysplasias, Muenke craniosynostosis, and Crouzon syndrome with acanthosis nigricans, Endocr. Rev. 21, 23-39.
18. Webster, M. K., and Donoghue, D. J. (1996) Constitutive activation of fibroblast growth factor receptor 3 by the transmembrane domain point mutation found in achondroplasia, EMBO J. 15, 520-527.
19. Olah, G. A., and Huang, H. W. (1988) Circular dichroism of oriented α helices. I. Proof of the exciton theory, J. Chem. Phys. 89, 2531-2538.
20. Olah, G. A., and Huang, H. W. (1988) Circular dichroism of oriented α helices. II. Electric field oriented polypeptides, J. Chem. Phys. 89, 6956-6962.
21. Hristova, K., Wimley, W. C., Mishra, V. K., Anantharamaiah, G. M., Segrest, J. P., and White, S. H. (1999) An amphipathic α-helix at a membrane interface: A structural study using a novel X-ray diffraction method, J. Mol. Biol. 290, 99-117.
22. Hristova, K., Dempsey, C. E., and White, S. H. (2001) Structure, location, and lipid perturbations of melittin at the membrane interface, Biophys. J. 80, 801-811.
23. Adair, B. D., and Engelman, D. M. (1994) Glycophorin a helical transmembrane domains dimerize in phospholipid bilayers - a resonance energy transfer study, Biochemistry 33, 5539-5544.
24. Li, M., Reddy, L. G., Bennett, R., Silva, N. D., Jones, L. R., and Thomas, D. D. (1999) A fluorescence energy transfer method for analyzing protein oligomeric structure: Application to phospholamban, Biophys. J. 76, 2587-2599.
25. Lemmon, M. A., Flanagan, J. M., Hunt, J. F., Adair, B. D., Bormann, B. J., Dempsey, C. E., and Engelman, D. M. (1992) Glycophorin-A dimerization is driven by specific interactions between transmembrane α-helices, J. Biol. Chem. 267, 7683-7689.
26. Lemmon, M. A., Flanagan, J. M., Hunt, J. F., Adair, B. D., Bormann, B. J., Dempsey, C. E., and Engelman, D. M. (1992) Glycophorin-A Dimerization Is Driven by Specific Interactions Between Transmembrane Alpha-Helices, J. Biol. Chem. 267, 7683-7689.
27. Russ, W. P., and Engelman, D. M. (1999) TOXCAT: A measure of transmembrane helix association in a biological membrane, Proc. Natl. Acad. Sci. U.S.A. 96, 863-868.
28. Fleming, K. G., and Engelman, D. M. (2001) Specificity in transmembrane helix-helix interactions can define a hierarchy of stability for sequence variants, Proc. Natl. Acad. Sci. U.S.A. 98, 14340-14344.
29. Sulistijo, E. S., Jaszewski, T. M., and MacKenzie, K. R. (2003) Sequence-specific dimerization of the transmembrane domain of the "BH3-only" protein BNIP3 in membranes and detergent, J. Biol. Chem. 278, 51950-51956.
30. Cornea, R. L., Jones, L. R., Autry, J. M., and Thomas, D. D. (1997) Mutation and phosphorylation change the oligomeric structure of phospholamban in lipid bilayers, Biochemistry 36, 2960-2967.
31. Watanabe, Y. (2002) Effect of various mild surfactants on the reassembly of an oligomeric integral membrane protein OmpF porin, J. Protein Chem. 21, 169-175.
32. Blakey, D., Leech, A., Thomas, G. H., Coutts, G., Findlay, K., and Merrick, M. (2002) Purification of the Escherichia coli ammonium transporter AmtB reveals a trimeric stoichiometry, Biochem. J. 364, 527-535.
33. Partridge, A. W., Melnyk, R. A., and Deber, C. M. (2002) Polar residues in membrane domains of proteins: Molecular basis for helix-helix association in a mutant CFTR transmembrane segment, Biochemistry 41, 3647-3653.
34. Melnyk, R. A., Partridge, A. W., and Deber, C. M. (2002) Transmembrane domain mediated self-assembly of major coat protein subunits from Ff bacteriophage, J. Mol. Biol. 315, 63-72.
35. Melnyk, R. A., Partridge, A. W., and Deber, C. M. (2001) Retention of native-like oligomerization states in transmembrane segment peptides: Application to the Escherichi coli aspartate receptor, Biochemistry 40, 11106-11113.
36. Fisher, L. E., Engelman, D. M., and Sturgis, J. N. (1999) Detergents modulate dimerization, but not helicity, of the glycophorin A transmembrane domain, J. Mol. Biol. 293, 639-651.
37. Wu, P., and Brand, L. (1994) Resonance energy transfer: Methods and applications, Anal. Biochem. 218, 1-13.
38. Kenworthy, A. K., Petranova, N., and Edidin, M. (2000) High-resolution FRET microscopy of cholera toxin B-subunit and GPI-anchored proteins in cell plasma membranes, Mol. Biol. Cell 11, 1645-1655.
39. Kenworthy, A. K., and Edidin, M. (1998) Distribution of a glycosylphosphatidylinositol-anchored protein at the apical surface of MDCK cells examined at a resolution of < 100 Å using imaging fluorescence resonance energy tranfer, J. Cell Biol. 142, 69-84.
40. Clegg, R. M. (1995) Fluorescence resonance energy transfer, Curr. Opin. Biotechnol. 6, 103-110.
41. Clegg, R. M. (1996) in Fluorescence Imaging Spectroscopy and Microscopy (Wang, X. F. and Herman, B., Eds.) pp 179-252, John Wiley, New York.
42. Wu, Y., Huang, H. W., and Olah, G. A. (1990) Method of oriented circular dichroism, Biophys. J. 57, 797-806.
43. Gambhir, A., Hangyas-Mihalyne, G., Zaitseva, I., Cafiso, D. S., Wang, J. Y., Murray, D., Pentyala, S. N., Smith, S. O., and McLaughlin, S. (2004) Electrostatic sequestration of PIP2 on phospholipid membranes by basic/aromatic regions of proteins, Biophys. J. 86, 2188-2207.
44. Wolber, P. K., and Hudson, B. S. (1979) An analytic solution to the Förster energy transfer problem in two dimensions, Biophys. J. 28, 197-210.
45. Wimley, W. C., and White, S. H. (2000) Determining the membrane topology of peptides by fluorescence quenching, Biochemistry 39, 161-170.
46. Bell, C. A., Tynan, J. A., Hart, K. C., Meyer, A. N., Robertson, S. C., and Donoghue, D. J. (2000) Rotational coupling of the transmembrane and kinase domains of the Neu receptor tyrosine kinase, Mol. Biol. Cell 11, 3589-3599.
47. Fleming, K. G., Ackerman, A. L., and Engelman, D. M. (1997) The effect of point mutations on the free energy of transmembrane α-helix dimerization, J. Mol. Biol. 272, 266-275.
48. Deng, C., Wynshaw-Boris, A., Zhou, F., Kuo, A., and Leder, P. (1996) Fibroblast growth factor receptor 3 is a negative regulator of bone growth, Cell 84, 911-921.
49. Nguyen, H. B., Estacion, M., and Gargus, J. J. (1997) Mutations causing achondroplasia and thanatophoric dysplasia alter bFGF-induced calcium signals in human diploid fibroblasts, Hum. Mol. Genet. 6, 681-688.
50. Colvin, J. S., Bohne, B. A., Harding, G. W., Mcewen, D. G., and Ornitz, D. M. (1996) Skeletal overgrowth and deafness in mice lacking fibroblast growth factor receptor 3, Nat. Genet. 12, 390-397.
51. Passos-Bueno, M. R., Wilcox, W. R., Jabs, E. W., Sertié, A. L., Alonso, L. G., and Kitoh, H. (1999) Clinical spectrum of fibroblast growth factor receptor mutations, Hum. Mutat. 14, 115-125.