Structure of Full-Length Human PDGFRβ Bound to Its Activating Ligand PDGF-B as Determined by Negative-Stain Electron Microscopy

Journal of Molecular Biology

Volumn 427, Issue 24, 2015, Pages 3921-3934

  Chen, Po Han ^a   Unger, Vinzenz ^b   He, Xiaolin ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

cancer; electron microscopy; membrane protein structure; receptor tyrosine kinase; signal transduction

Indexed keywords

DIMER; PLATELET DERIVED GROWTH FACTOR B; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN BINDING;

ARTICLE; CONFORMATION; CRYSTAL STRUCTURE; DIMERIZATION; ELECTRON MICROSCOPY; ENZYME ACTIVATION; FLUORESCENCE COUPLED SIZE EXCLUSION CHROMATOGRAPHY; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SIZE EXCLUSION CHROMATOGRAPHY; CHEMISTRY; ENZYME ACTIVE SITE; HEK293 CELL LINE; HUMAN; MOLECULAR MODEL; PROTEIN QUATERNARY STRUCTURE; STAINING; ULTRASTRUCTURE;

CATALYTIC DOMAIN; HEK293 CELLS; HUMANS; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTO-ONCOGENE PROTEINS C-SIS; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; STAINING AND LABELING;

EID: 84948695261     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.10.003     Document Type: Article

References (40)

1. N. Kohler, and A. Lipton Platelets as a source of fibroblast growth-promoting activity Exp. Cell Res. 87 1974 297 301
2. R. Ross, J. Glomset, B. Kariya, and L. Harker A platelet-dependent serum factor that stimulates the proliferation of arterial smooth muscle cells in vitro Proc. Natl. Acad. Sci. U. S. A. 71 1974 1207 1210
3. J. Andrae, R. Gallini, and C. Betsholtz Role of platelet-derived growth factors in physiology and medicine Genes Dev. 22 2008 1276 1312
4. A. Ostman PDGF receptors-mediators of autocrine tumor growth and regulators of tumor vasculature and stroma Cytokine Growth Factor Rev. 15 2004 275 286
5. M.A. Lemmon, and J. Schlessinger Cell signaling by receptor tyrosine kinases Cell 141 2010 1117 1134
6. L. Coussens, C. Van Beveren, D. Smith, E. Chen, R.L. Mitchell, C.M. Isacke, I.M. Verma, and A. Ullrich Structural alteration of viral homologue of receptor proto-oncogene fms at carboxyl terminus Nature 320 1986 277 280
7. O. Rosnet, S. Marchetto, O. deLapeyriere, and D. Birnbaum Murine Flt3, a gene encoding a novel tyrosine kinase receptor of the PDGFR/CSF1R family Oncogene 6 1991 1641 1650
8. X. Chen, H. Liu, P.J. Focia, A.H. Shim, and X. He Structure of macrophage colony stimulating factor bound to FMS: Diverse signaling assemblies of class III receptor tyrosine kinases Proc. Natl. Acad. Sci. U. S. A. 105 2008 18267 18272
9. 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
10. 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
11. K. Verstraete, G. Vandriessche, M. Januar, J. Elegheert, A.V. Shkumatov, A. Desfosses, K. Van Craenenbroeck, D.I. Svergun, I. Gutsche, B. Vergauwen, and S.N. Savvides Structural insights into the extracellular assembly of the hematopoietic Flt3 signaling complex Blood 118 2011 60 68
12. X. Ma, W.Y. Lin, Y. Chen, S. Stawicki, K. Mukhyala, Y. Wu, F. Martin, J.F. Bazan, and M.A. Starovasnik Structural basis for the dual recognition of helical cytokines IL-34 and CSF-1 by CSF-1R Structure 20 2012 676 687
13. H. Liu, C. Leo, X. Chen, B.R. Wong, L.T. Williams, H. Lin, and X. He The mechanism of shared but distinct CSF-1R signaling by the non-homologous cytokines IL-34 and CSF-1 Biochim. Biophys. Acta 1824 2012 938 945
14. Y. Opatowsky, I. Lax, F. Tome, 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. U. S. A. 111 2014 1772 1777
15. A. Goehring, C.H. Lee, K.H. Wang, J.C. Michel, D.P. Claxton, I. Baconguis, T. Althoff, S. Fischer, K.C. Garcia, and E. Gouaux Screening and large-scale expression of membrane proteins in mammalian cells for structural studies Nat. Protoc. 9 2014 2574 2585
16. J.D. Pedelacq, S. Cabantous, T. Tran, T.C. Terwilliger, and G.S. Waldo Engineering and characterization of a superfolder green fluorescent protein Nat. Biotechnol. 24 2006 79 88
17. H. Stark GraFix: Stabilization of fragile macromolecular complexes for single particle cryo-EM Methods Enzymol. 481 2010 109 126
18. S.H. Scheres RELION: Implementation of a Bayesian approach to cryo-EM structure determination J. Struct. Biol. 180 2012 519 530
19. A.H. Shim, H. Liu, P.J. Focia, X. Chen, P.C. Lin, and X. He Structures of a platelet-derived growth factor/propeptide complex and a platelet-derived growth factor/receptor complex Proc. Natl. Acad. Sci. U. S. A. 107 2010 11307 11312
20. Y. Yang, S. Yuzawa, and J. Schlessinger Contacts between membrane proximal regions of the PDGF receptor ectodomain are required for receptor activation but not for receptor dimerization Proc. Natl. Acad. Sci. U. S. A. 105 2008 7681 7686
21. M.A. Lemmon, D. Pinchasi, M. Zhou, I. Lax, and J. Schlessinger Kit receptor dimerization is driven by bivalent binding of stem cell factor J. Biol. Chem. 272 1997 6311 6317
22. J. Felix, J. Elegheert, I. Gutsche, A.V. Shkumatov, Y. Wen, N. Bracke, E. Pannecoucke, I. Vandenberghe, B. Devreese, D.I. Svergun, E. Pauwels, B. Vergauwen, and S.N. Savvides Human IL-34 and CSF-1 establish structurally similar extracellular assemblies with their common hematopoietic receptor Structure 21 2013 528 539
23. J. Elegheert, A. Desfosses, A.V. Shkumatov, X. Wu, N. Bracke, K. Verstraete, K. Van Craenenbroeck, B.R. Brooks, D.I. Svergun, B. Vergauwen, I. Gutsche, and S.N. Savvides Extracellular complexes of the hematopoietic human and mouse CSF-1 receptor are driven by common assembly principles Structure 19 2011 1762 1772
24. K. Verstraete, and S.N. Savvides Extracellular assembly and activation principles of oncogenic class III receptor tyrosine kinases Nat. Rev. Cancer 12 2012 753 766
25. C. Muhle-Goll, S. Hoffmann, S. Afonin, S.L. Grage, A.A. Polyansky, D. Windisch, M. Zeitler, J. Burck, and A.S. Ulrich Hydrophobic matching controls the tilt and stability of the dimeric platelet-derived growth factor receptor (PDGFR) beta transmembrane segment J. Biol. Chem. 287 2012 26178 26186
26. A. Arkhipov, Y. Shan, R. Das, N.F. Endres, M.P. Eastwood, D.E. Wemmer, J. Kuriyan, and D.E. Shaw Architecture and membrane interactions of the EGF receptor Cell 152 2013 557 569
27. N.F. Endres, R. Das, A.W. Smith, A. Arkhipov, E. Kovacs, Y. Huang, J.G. Pelton, Y. Shan, D.E. Shaw, D.E. Wemmer, J.T. Groves, and J. Kuriyan Conformational coupling across the plasma membrane in activation of the EGF receptor Cell 152 2013 543 556
28. M. Chavent, A.P. Chetwynd, P.J. Stansfeld, and M.S. Sansom Dimerization of the EphA1 receptor tyrosine kinase transmembrane domain: Insights into the mechanism of receptor activation Biochemistry 53 2014 6641 6652
29. A.J. Brooks, W. Dai, M.L. O'Mara, D. Abankwa, Y. Chhabra, R.A. Pelekanos, O. Gardon, K.A. Tunny, K.M. Blucher, C.J. Morton, M.W. Parker, E. Sierecki, Y. Gambin, G.A. Gomez, K. Alexandrov, I.A. Wilson, M. Doxastakis, A.E. Mark, and M.J. Waters Mechanism of activation of protein kinase JAK2 by the growth hormone receptor Science 344 2014 1249783
30. D. DiMaio, and L.M. Petti The E5 proteins Virology 445 2013 99 114
31. J.H. Bae, T.J. Boggon, F. Tome, 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. U. S. A. 107 2010 2866 2871
32. J.H. Bae, and J. Schlessinger Asymmetric tyrosine kinase arrangements in activation or autophosphorylation of receptor tyrosine kinases Mol. Cell 29 2010 443 448
33. 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
34. H. Chen, C.F. Xu, J. Ma, A.V. Eliseenkova, W. Li, P.M. Pollock, N. Pitteloud, W.T. Miller, T.A. Neubert, and M. Mohammadi A crystallographic snapshot of tyrosine trans-phosphorylation in action Proc. Natl. Acad. Sci. U. S. A. 105 2008 19660 19665
35. M. Ohi, Y. Li, Y. Cheng, and T. Walz Negative staining and image classification - Powerful tools in modern electron microscopy Biol. Proced. Online 6 2004 23 34
36. S.H. Scheres, R. Nunez-Ramirez, C.O. Sorzano, J.M. Carazo, and R. Marabini Image processing for electron microscopy single-particle analysis using XMIPP Nat. Protoc. 3 2008 977 990
37. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - A visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
38. W. Humphrey, A. Dalke, and K. Schulten VMD: Visual molecular dynamics J. Mol. Graph. 14 1996 27 28
39. W. Wriggers Using Situs for the integration of multi-resolution structures Biophys. Rev. 2 2010 21 27
40. J.C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R.D. Skeel, L. Kale, and K. Schulten Scalable molecular dynamics with NAMD J. Comput. Chem. 26 2005 1781 1802