Energetics of ErbB1 transmembrane domain dimerization in lipid bilayers

Biophysical Journal

Volumn 96, Issue 11, 2009, Pages 4622-4630

  Chen, Lirong ^a   Merzlyakov, Mikhail ^a   Cohen, Tomer ^b   Shai, Yechiel ^b   Hristova, Kalina ^a  

^a Johns Hopkins University   (United States)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; EPIDERMAL GROWTH FACTOR RECEPTOR; MEMBRANE PROTEIN; PROTEIN TYROSINE KINASE; 1,2 DILAUROYLPHOSPHATIDYLCHOLINE; 1,2-DILAUROYLPHOSPHATIDYLCHOLINE; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLCHOLINE; 2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; DETERGENT; FLUORESCEIN; PHOSPHATIDYLCHOLINE; RHODAMINE;

ANALYTIC METHOD; ARTICLE; CALCULATION; CIRCULAR DICHROISM; DIMERIZATION; ENERGY TRANSFER; LIPID BILAYER; PROTEIN EXPRESSION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; ALGORITHM; CHEMISTRY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; SPECTROFLUOROMETRY;

ALGORITHMS; CIRCULAR DICHROISM; DETERGENTS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCEIN; LIPID BILAYERS; PHOSPHATIDYLCHOLINES; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; RECEPTOR, EPIDERMAL GROWTH FACTOR; RHODAMINES; SIGNAL TRANSDUCTION; SPECTROMETRY, FLUORESCENCE;

EID: 68949110276     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.03.004     Document Type: Article

References (42)

1. Fantl, W. J., D. E. Johnson, and L. T. Williams. 1993. Signaling by receptor tyrosine kinases. Annu. Rev. Biochem. 62:453-481.
2. Schlessinger, J. 2000. Cell signaling by receptor tyrosine kinases. Cell. 103:211-225.
3. Weiss, A., and J. Schlessinger. 1998. Switching signals on or off by receptor dimerization. Cell. 94:277-280.
4. Linggi, B., and G. Carpenter. 2006. ErbB receptors: new insights on mechanisms and biology. Trends Cell Biol. 16:649-656.
5. Sakai, K., H. Yokote, K. Murakami-Murofushi, T. Tamura, N. Saijo, et al. 2007. Pertuzumab, a novel HER dimerization inhibitor, inhibits the growth of human lung cancer cells mediated by the HER3 signaling pathway. Cancer Sci. 98:1498-1503.
6. Burgess, A. W., H. S. Cho, C. Eigenbrot, K. M. Ferguson, T. P. J. Garrett, et al. 2003. An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors. Mol. Cell. 12:541-552.
7. Cho, H. S., and D. J. Leahy. 2002. Structure of the extracellular region of HER3 reveals an interdomain tether. Science. 297:1330-1333.
8. Cho, H. S., K. Mason, K. X. Ramyar, A. M. Stanley, S. B. Gabelli, et al. 2003. Structure of the extracellular region of HER2 alone and in complex with the Herceptin Fab. Nature. 421:756-760.
9. Bouyain, S., P. A. Longo, S. Q. Li, K. M. Ferguson, and D. J. Leahy. 2005. The extracellular region of ErbB4 adopts a tethered conformation in the absence of ligand. Proc. Natl. Acad. Sci. USA. 102:15024-15029.
10. Plotnikov, A. N., S. R. Hubbard, J. Schlessinger, and M. Mohammadi. 2000. Crystal structures of two FGF-FGFR complexes reveal the determinants of ligand-receptor specificity. Cell. 101:413-424.
11. Plotnikov, A. N., J. Schlessinger, S. R. Hubbard, and M. Mohammadi. 1999. Structural basis for FGF receptor dimerization and activation. Cell. 98:641-650.
12. Bell, C. A., J. A. Tynan, K. C. Hart, A. N. Meyer, S. C. Robertson, et al. 2000. Rotational coupling of the transmembrane and kinase domains of the Neu receptor tyrosine kinase. Mol. Biol. Cell. 11:3589-3599.
13. Mendrola, J. M., M. B. Berger, M. C. King, and M. A. Lemmon. 2002. The single transmembrane domains of ErbB receptors self-associate in cell membranes. J. Biol. Chem. 277:4704-4712.
14. Gerber, D., N. Sal-Man, and Y. Shai. 2004. Two motifs within a transmembrane domain, one for homodimerization and the other for heterodimerization. J. Biol. Chem. 279:21177-21182.
15. Fleishman, S. J., J. Schlessinger, and N. Ben-Tal. 2002. A putative molecular-activation switch in the transmembrane domain of erbB2. Proc. Natl. Acad. Sci. USA. 99:15937-15940.
16. Li, E., and K. Hristova. 2006. Role of receptor tyrosine kinase transmembrane domains in cell signaling and human pathologies. Biochemistry. 45:6241-6251.
17. Tanner, K. G., and J. Kyte. 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.
18. Duneau, J. P., A. P. Vegh, and J. N. Sturgis. 2007. A dimerization hierarchy in the transmembrane domains of the HER receptor family. Biochemistry. 46:2010-2019.
19. Stanley, A. M., and K. G. Fleming. 2005. The transmembrane domains of ErbB receptors do not dimerize strongly in micelles. J. Mol. Biol. 347:759-772.
20. Matthews, E. E., M. Zoonens, and D. M. Engelman. 2006. Dynamic helix interactions in transmembrane signaling. Cell. 127:447-450.
21. Li, E., M. You, and K. Hristova. 2005. SDS-PAGE and FRET suggest weak interactions between FGFR3 TM domains in the absence of extracellular domains and ligands. Biochemistry. 44:352-360.
22. Iwamoto, T., M. You, E. Li, J. Spangler, J. M. Tomich, et al. 2005. Synthesis and initial characterization of FGFR3 transmembrane domain: Consequences of sequence modifications. Biochim. Biophys. Acta. 1668:240-247.
23. You, M., E. Li, W. C. Wimley, and K. Hristova. 2005. FRET in liposomes: measurements of TM helix dimerization in the native bilayer environment. Anal. Biochem. 340:154-164.
24. Vogel, H. 1987. Comparison of the conformation and orientation of alamethicin and melittin in lipid membranes. Biochemistry. 26:4562-4572.
25. Hristova, K., W. C. Wimley, V. K. Mishra, G. M. Anantharamaiah, J. P. Segrest, et al. 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.
26. Hristova, K., C. E. Dempsey, and S. H. White. 2001. Structure, location, and lipid perturbations of melittin at the membrane interface. Biophys. J. 80:801-811.
27. Han, X., M. Mihailescu, and K. Hristova. 2006. Neutron diffraction studies of fluid bilayers with transmembrane proteins: structural consequences of the achondroplasia mutation. Biophys. J. 91:3736-3747.
28. Han, X., K. Hristova, and W. C. Wimley. 2008. Protein folding in membranes: insights from neutron diffraction studies of a membrane beta-sheet oligomer. Biophys. J. 94:492-505.
29. Li, E., M. You, and K. Hristova. 2006. FGFR3 dimer stabilization due to a single amino acid pathogenic mutation. J. Mol. Biol. 356:600-612.
30. Merzlyakov, M., L. Chen, and K. Hristova. 2007. Studies of receptor tyrosine kinase transmembrane domain interactions: the EmEx-FRET method. J. Membr. Biol. 215:93-103.
31. Posokhov, Y. O., M. Merzlyakov, K. Hristova, and A. S. Ladokhin. 2008. A simple "proximity" correction for Förster resonance energy transfer efficiency determination in membranes using lifetime measurements. Anal. Biochem. 380:134-136.
32. Fisher, L. E., D. M. Engelman, and J. N. Sturgis. 1999. Detergents modulate dimerization, but not helicity, of the glycophorin A transmembrane domain. J. Mol. Biol. 293:639-651.
33. Artemenko, E. O., N. S. Egorova, A. S. Arseniev, and A. V. Feofanov. 2008. Transmembrane domain of EphA1 receptor forms dimers in membrane-like environment. Biochim. Biophys. Acta. 1778:2361-2367.
34. Therien, A. G., F. E. M. Grant, and C. M. Deber. 2001. Interhelical hydrogen bonds in the CFTR membrane domain. Nat. Struct. Biol. 8:597-601.
35. You, M., J. Spangler, E. Li, X. Han, P. Ghosh, et al. 2007. Effect of pathogenic cysteine mutations on FGFR3 transmembrane domain dimerization in detergents and lipid bilayers. Biochemistry. 46:11039-11046.
36. Li, E., and K. Hristova. 2004. Imaging FRET measurements of transmembrane helix interactions in lipid bilayers on a solid support. Langmuir. 20:9053-9060.
37. Adair, B. D., and D. M. Engelman. 1994. Glycophorin a helical transmembrane domains dimerize in phospholipid bilayers - a resonance energy transfer study. Biochemistry. 33:5539-5544.
38. Li, M., L. G. Reddy, R. Bennett, N. D. Silva, Jr., L. R. Jones, et al. 1999. A fluorescence energy transfer method for analyzing protein oligomeric structure: Application to phospholamban. Biophys. J. 76:2587-2599.
39. Wolber, P. K., and B. S. Hudson. 1979. An analytic solution to the Förster energy transfer problem in two dimensions. Biophys. J. 28:197-210.
40. You, M., E. Li, and K. Hristova. 2006. The achondroplasia mutation does not alter the dimerization energetics of FGFR3 transmembrane domain. Biochemistry. 45:5551-5556.
41. Lemmon, M. A., Z. M. Bu, J. E. Ladbury, M. Zhou, D. Pinchasi, et al. 1997. Two EGF molecules contribute additively to stabilization of the EGFR dimer. EMBO J. 16:281-294.
42. He, L., and K. Hristova. 2008. Pathogenic activation of receptor tyrosine kinases in mammalian membranes. J. Mol. Biol. 384:1130-1142.