Structural and functional characterization of alternative transmembrane domain conformations in VEGF receptor 2 activation

Structure

Volumn 22, Issue 8, 2014, Pages 1077-1089

  Manni, Sandro ^a   Mineev, Konstantin S ^b   Usmanova, Dinara ^b,c   Lyukmanova, Ekaterina N ^b   Shulepko, Mikhail A ^b,d   Kirpichnikov, Mikhail P ^b,d   Winter, Jonas ^a   Matkovic, Milos ^a   Deupi, Xavier ^a   Arseniev, Alexander S ^b,c   Ballmer Hofer, Kurt ^a  

^a PAUL SCHERRER INSTITUTE   (Switzerland)

^b SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^c MOSCOW INSTITUTE OF PHYSICS AND TECHNOLOGY   (Russian Federation)

^d MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ENHANCED GREEN FLUORESCENT PROTEIN; GLUTAMIC ACID; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOLIPASE D; VASCULOTROPIN RECEPTOR 2; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2, HUMAN;

ARTICLE; CELL MEMBRANE; CELL MIGRATION; CONFOCAL MICROSCOPY; DIMERIZATION; ENZYME ACTIVITY; HOMEOSTASIS; HUMAN; IMMUNOFLUORESCENCE MICROSCOPY; MOLECULAR DYNAMICS; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVATION; GENETICS; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; DIMERIZATION; ENZYME ACTIVATION; HUMANS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84905725412     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2014.05.010     Document Type: Article

References (61)

1. J.H. Bae, T.J. Boggon, F. Tomé, V. Mandiyan, I. Lax, and J. Schlessinger Asymmetric receptor contact is required for tyrosine autophosphorylation of fibroblast growth factor receptor in living cells Proc. Natl. Acad. Sci. USA 107 2010 2866 2871
2. C.I. Bargmann, and R.A. Weinberg Oncogenic activation of the neu-encoded receptor protein by point mutation and deletion EMBO J. 7 1988 2043 2052
3. W.A. Barton, D. Tzvetkova-Robev, E.P. Miranda, M.V. Kolev, K.R. Rajashankar, J.P. Himanen, and D.B. Nikolov Crystal structures of the Tie2 receptor ectodomain and the angiopoietin-2-Tie2 complex Nat. Struct. Mol. Biol. 13 2006 524 532
4. C.A. Bell, J.A. Tynan, K.C. Hart, A.N. Meyer, S.C. Robertson, and D.J. Donoghue Rotational coupling of the transmembrane and kinase domains of the Neu receptor tyrosine kinase Mol. Biol. Cell 11 2000 3589 3599
5. E.V. Bocharov, Y.E. Pustovalova, K.V. Pavlov, P.E. Volynsky, M.V. Goncharuk, Y.S. Ermolyuk, D.V. Karpunin, A.A. Schulga, M.P. Kirpichnikov, and R.G. Efremov et al. Unique dimeric structure of BNip3 transmembrane domain suggests membrane permeabilization as a cell death trigger J. Biol. Chem. 282 2007 16256 16266
6. E.V. Bocharov, K.S. Mineev, P.E. Volynsky, Y.S. Ermolyuk, E.N. Tkach, A.G. Sobol, V.V. Chupin, M.P. Kirpichnikov, R.G. Efremov, and A.S. Arseniev Spatial structure of the dimeric transmembrane domain of the growth factor receptor ErbB2 presumably corresponding to the receptor active state J. Biol. Chem. 283 2008 6950 6956
7. E.V. Bocharov, M.L. Mayzel, P.E. Volynsky, K.S. Mineev, E.N. Tkach, Y.S. Ermolyuk, A.A. Schulga, R.G. Efremov, and A.S. Arseniev Left-handed dimer of EphA2 transmembrane domain: Helix packing diversity among receptor tyrosine kinases Biophys. J. 98 2010 881 889
8. E.V. Bocharov, K.S. Mineev, M.V. Goncharuk, and A.S. Arseniev Structural and thermodynamic insight into the process of "weak" dimerization of the ErbB4 transmembrane domain by solution NMR Biochim. Biophys. Acta 1818 2012 2158 2170
9. E.V. Bocharov, D.M. Lesovoy, S.A. Goncharuk, M.V. Goncharuk, K. Hristova, and A.S. Arseniev Structure of FGFR3 transmembrane domain dimer: implications for signaling and human pathologies Structure 21 2013 2087 2093
10. M.S. Brozzo, S. Bjelić, K. Kisko, T. Schleier, V.M. Leppänen, K. Alitalo, F.K. Winkler, and K. Ballmer-Hofer Thermodynamic and structural description of allosterically regulated VEGFR-2 dimerization Blood 119 2012 1781 1788
11. J. Cavanagh Protein NMR spectroscopy: Principles and practice 2007 Academic Press Amsterdam
12. L. Chen, L. Novicky, M. Merzlyakov, T. Hristov, and K. Hristova Measuring the energetics of membrane protein dimerization in mammalian membranes J. Am. Chem. Soc. 132 2010 3628 3635
13. L. Chen, J. Placone, L. Novicky, and K. Hristova The extracellular domain of fibroblast growth factor receptor 3 inhibits ligand-independent dimerization Sci. Signal. 3 2010 ra86
14. T.J. Dolinsky, J.E. Nielsen, J.A. McCammon, and N.A. Baker PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations Nucleic Acids Res. 32 2004 W665 W667
15. D.D. Dosch, and K. Ballmer-Hofer Transmembrane domain-mediated orientation of receptor monomers in active VEGFR-2 dimers FASEB J. 24 2010 32 38
16. N.F. Endres, R. Das, A.W. Smith, A. Arkhipov, E. Kovacs, Y. Huang, J.G. Pelton, Y. Shan, D.E. Shaw, and D.E. Wemmer et al. Conformational coupling across the plasma membrane in activation of the EGF receptor Cell 152 2013 543 556
17. K.M. Ferguson, M.B. Berger, J.M. Mendrola, H.S. Cho, D.J. Leahy, and M.A. Lemmon EGF activates its receptor by removing interactions that autoinhibit ectodomain dimerization Mol. Cell 11 2003 507 517
18. N. Ferrara, K. Carver-Moore, H. Chen, M. Dowd, L. Lu, K.S. O'Shea, L. Powell-Braxton, K.J. Hillan, and M.W. Moore Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene Nature 380 1996 439 442
19. C. Finger, C. Escher, and D. Schneider The single transmembrane domains of human receptor tyrosine kinases encode self-interactions Sci. Signal. 2 2009 ra56
20. P. Guentert Automated NMR protein structure calculation Prog. Nucl. Magn. Reson. Spectrosc. 43 2003 105 125
21. W.J. Gullick, A.C. Bottomley, F.J. Lofts, D.G. Doak, D. Mulvey, R. Newman, M.J. Crumpton, M.J. Sternberg, and I.D. Campbell Three dimensional structure of the transmembrane region of the proto-oncogenic and oncogenic forms of the neu protein EMBO J. 11 1992 43 48
22. K. Henzler-Wildman, and D. Kern Dynamic personalities of proteins Nature 450 2007 964 972
23. C.A. Hyde, A. Giese, E. Stuttfeld, S.J. Abram, D. Villemagne, T. Schleier, H.K. Binz, and K. Ballmer-Hofer Targeting the extracellular domains D4 and D7 of VEGFR-2 reveals allosteric receptor regulatory sites Mol. Cell. Biol. 32 2012 3802 3813
24. M. Jinnin, D. Medici, L. Park, N. Limaye, Y. Liu, E. Boscolo, J. Bischoff, M. Vikkula, E. Boye, and B.R. Olsen Suppressed NFAT-dependent VEGFR1 expression and constitutive VEGFR2 signaling in infantile hemangioma Nat. Med. 14 2008 1236 1246
25. N. Jura, N.F. Endres, K. Engel, S. Deindl, R. Das, M.H. Lamers, D.E. Wemmer, X. Zhang, and J. Kuriyan Mechanism for activation of the EGF receptor catalytic domain by the juxtamembrane segment Cell 137 2009 1293 1307
26. N. Jura, X. Zhang, N.F. Endres, M.A. Seeliger, T. Schindler, and J. Kuriyan Catalytic control in the EGF receptor and its connection to general kinase regulatory mechanisms Mol. Cell 42 2011 9 22
27. F.C. Kelleher, H. O'Sullivan, E. Smyth, R. McDermott, and A. Viterbo Fibroblast growth factor receptors, developmental corruption and malignant disease Carcinogenesis 34 2013 2198 2205
28. R.L.J. Keller The Computer Aided Resonance Assignment Tutorial 2004 Cantina Verlag Goldau
29. K. Kisko, M.S. Brozzo, J. Missimer, T. Schleier, A. Menzel, V.M. Leppänen, K. Alitalo, T. Walzthoeni, R. Aebersold, and K. Ballmer-Hofer Structural analysis of vascular endothelial growth factor receptor-2/ligand complexes by small-angle X-ray solution scattering FASEB J. 25 2011 2980 2986
30. S. Koch, S. Tugues, X. Li, L. Gualandi, and L. Claesson-Welsh Signal transduction by vascular endothelial growth factor receptors Biochem. J. 437 2011 169 183
31. M.A. Lemmon, and K.M. Ferguson A new twist in the transmembrane signaling tool-kit Cell 130 2007 213 215
32. V.M. Leppänen, A.E. Prota, M. Jeltsch, A. Anisimov, N. Kalkkinen, T. Strandin, H. Lankinen, A. Goldman, K. Ballmer-Hofer, and K. Alitalo Structural determinants of growth factor binding and specificity by VEGF receptor 2 Proc. Natl. Acad. Sci. USA 107 2010 2425 2430
33. V.M. Leppänen, D. Tvorogov, K. Kisko, A.E. Prota, M. Jeltsch, A. Anisimov, S. Markovic-Mueller, E. Stuttfeld, K.N. Goldie, K. Ballmer-Hofer, and K. Alitalo Structural and mechanistic insights into VEGF receptor 3 ligand binding and activation Proc. Natl. Acad. Sci. USA 110 2013 12960 12965
34. Y. Li, K. Mangasarian, A. Mansukhani, and C. Basilico Activation of FGF receptors by mutations in the transmembrane domain Oncogene 14 1997 1397 1406
35. E. Li, M. You, and K. Hristova FGFR3 dimer stabilization due to a single amino acid pathogenic mutation J. Mol. Biol. 356 2006 600 612
36. H. Liu, X. Chen, P.J. Focia, and X. He Structural basis for stem cell factor-KIT signaling and activation of class III receptor tyrosine kinases EMBO J. 26 2007 891 901
37. A.D. MacKerell, D. Bashford, M. Bellott, R.L. Dunbrack, J.D. Evanseck, M.J. Field, S. Fischer, J. Gao, H. Guo, and S. Ha et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102 1998 3586 3616
38. L.Z. Mi, C. Lu, Z. Li, N. Nishida, T. Walz, and T.A. Springer Simultaneous visualization of the extracellular and cytoplasmic domains of the epidermal growth factor receptor Nat. Struct. Mol. Biol. 18 2011 984 989
39. K.S. Mineev, E.V. Bocharov, Y.E. Pustovalova, O.V. Bocharova, V.V. Chupin, and A.S. Arseniev Spatial structure of the transmembrane domain heterodimer of ErbB1 and ErbB2 receptor tyrosine kinases J. Mol. Biol. 400 2010 231 243
40. K.S. Mineev, N.F. Khabibullina, E.N. Lyukmanova, D.A. Dolgikh, M.P. Kirpichnikov, and A.S. Arseniev Spatial structure and dimer - monomer equilibrium of the ErbB3 transmembrane domain in DPC micelles Biochim. Biophys. Acta 1808 2011 2081 2088
41. K.S. Mineev, D.M. Lesovoy, D.R. Usmanova, S.A. Goncharuk, M.A. Shulepko, E.N. Lyukmanova, M.P. Kirpichnikov, E.V. Bocharov, and A.S. Arseniev NMR-based approach to measure the free energy of transmembrane helix-helix interactions Biochim. Biophys. Acta 1838 1 Pt B 2014 164 172
42. H. Ogiso, R. Ishitani, O. Nureki, S. Fukai, M. Yamanaka, J.H. Kim, K. Saito, A. Sakamoto, M. Inoue, M. Shirouzu, and S. Yokoyama Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains Cell 110 2002 775 787
43. Y. Opatowsky, I. Lax, F. Tomé, F. Bleichert, V.M. Unger, and J. Schlessinger Structure, domain organization, and different conformational states of stem cell factor-induced intact KIT dimers Proc. Natl. Acad. Sci. USA 111 2014 1772 1777
44. V.Y. Orekhov, and V.A. Jaravine Analysis of non-uniformly sampled spectra with multi-dimensional decomposition Prog. Nucl. Magn. Reson. Spectrosc. 59 2011 271 292
45. L. Pellegrini, D.F. Burke, F. von Delft, B. Mulloy, and T.L. Blundell Crystal structure of fibroblast growth factor receptor ectodomain bound to ligand and heparin Nature 407 2000 1029 1034
46. J.C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R.D. Skeel, L. Kalé, and K. Schulten Scalable molecular dynamics with NAMD J. Comput. Chem. 26 2005 1781 1802
47. A.N. Plotnikov, J. Schlessinger, S.R. Hubbard, and M. Mohammadi Structural basis for FGF receptor dimerization and activation Cell 98 1999 641 650
48. C. Ruch, G. Skiniotis, M.O. Steinmetz, T. Walz, and K. Ballmer-Hofer Structure of a VEGF-VEGF receptor complex determined by electron microscopy Nat. Struct. Mol. Biol. 14 2007 249 250
49. J. Schlessinger Signal transduction. Autoinhibition control Science 300 2003 750 752
50. C. Schubert, C. Schalk-Hihi, G.T. Struble, H.C. Ma, I.P. Petrounia, B. Brandt, I.C. Deckman, R.J. Patch, M.R. Player, J.C. Spurlino, and B.A. Springer Crystal structure of the tyrosine kinase domain of colony-stimulating factor-1 receptor (cFMS) in complex with two inhibitors J. Biol. Chem. 282 2007 4094 4101
51. F. Shalaby, J. Rossant, T.P. Yamaguchi, M. Gertsenstein, X.F. Wu, M.L. Breitman, and A.C. Schuh Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice Nature 376 1995 62 66
52. F. Shalaby, J. Ho, W.L. Stanford, K.D. Fischer, A.C. Schuh, L. Schwartz, A. Bernstein, and J. Rossant A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis Cell 89 1997 981 990
53. Y. Shen, F. Delaglio, G. Cornilescu, and A. Bax TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts J. Biomol. NMR 44 2009 213 223
54. S.O. Smith, C.S. Smith, and B.J. Bormann Strong hydrogen bonding interactions involving a buried glutamic acid in the transmembrane sequence of the neu/erbB-2 receptor Nat. Struct. Biol. 3 1996 252 258
55. M.H.M. Olsson, C.R. Soedergaard, M. Rostkowski, and J. Jensen PROPKA3: Consistent Treatment of Internal and Surface Residues in Empirical pKa Predictions J. Chem. Theory Comput. 7 2000 525 537
56. D.J. Stauber, A.D. DiGabriele, and W.A. Hendrickson Structural interactions of fibroblast growth factor receptor with its ligands Proc. Natl. Acad. Sci. USA 97 2000 49 54
57. R.H. Tao, and I.N. Maruyama All EGF(ErbB) receptors have preformed homo- and heterodimeric structures in living cells J. Cell Sci. 121 2008 3207 3217
58. M. Walter, I.S. Lucet, O. Patel, S.E. Broughton, R. Bamert, N.K. Williams, E. Fantino, A.F. Wilks, and J. Rossjohn The 2.7 A crystal structure of the autoinhibited human c-Fms kinase domain J. Mol. Biol. 367 2007 839 847
59. M.K. Webster, and D.J. Donoghue Constitutive activation of fibroblast growth factor receptor 3 by the transmembrane domain point mutation found in achondroplasia EMBO J. 15 1996 520 527
60. S. Yuzawa, Y. Opatowsky, Z. Zhang, V. Mandiyan, I. Lax, and J. Schlessinger Structural basis for activation of the receptor tyrosine kinase KIT by stem cell factor Cell 130 2007 323 334
61. X. Zhang, J. Gureasko, K. Shen, P.A. Cole, and J. Kuriyan An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor Cell 125 2006 1137 1149