The structure of the Tiam1 PDZ Domain/ phospho-syndecan1 complex reveals a ligand conformation that modulates protein dynamics

Structure

Volumn 21, Issue 3, 2013, Pages 342-354

  Liu, Xu ^a   Shepherd, Tyson R ^a,c   Murray, Ann M ^a   Xu, Zhen ^a   Fuentes, Ernesto J ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; SYNDECAN 1; T CELL LYMPHOMA INVASION AND METASTASIS 1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CRYSTAL STRUCTURE; HUMAN; MOLECULAR DYNAMICS; PDZ DOMAIN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; BINDING SITES; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PDZ DOMAINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; STRUCTURE-ACTIVITY RELATIONSHIP; SYNDECAN-1; SYNDECAN-2; SYNDECAN-3; SYNDECAN-4;

EID: 84874931864     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.01.004     Document Type: Article

References (71)

1. N.B. Adey, L. Huang, P.A. Ormonde, M.L. Baumgard, R. Pero, D.V. Byreddy, S.V. Tavtigian, and P.L. Bartel Threonine phosphorylation of the MMAC1/PTEN PDZ binding domain both inhibits and stimulates PDZ binding Cancer Res. 60 2000 35 37
2. P.V. Afonine, R.W. Grosse-Kunstleve, P.D. Adams, V.Y. Lunin, and A. Urzhumtsev On macromolecular refinement at subatomic resolution with interatomic scatterers Acta Crystallogr. D Biol. Crystallogr. 63 2007 1194 1197
3. E. Akiva, G. Friedlander, Z. Itzhaki, and H. Margalit A dynamic view of domain-motif interactions PLoS Comput. Biol. 8 2012 e1002341
4. V.K. Asundi, and D.J. Carey Phosphorylation of recombinant N-syndecan (syndecan 3) core protein Biochem. Biophys. Res. Commun. 240 1997 502 506
5. G. Birrane, J. Chung, and J.A. Ladias Novel mode of ligand recognition by the Erbin PDZ domain J. Biol. Chem. 278 2003 1399 1402
6. P. Boisguerin, B. Ay, G. Radziwill, R.D. Fritz, K. Moelling, and R. Volkmer Characterization of a putative phosphorylation switch: adaptation of SPOT synthesis to analyze PDZ domain regulation mechanisms ChemBioChem 8 2007 2302 2307
7. J. Chen, C.L. Brooks 3rd, and P.E. Wright Model-free analysis of protein dynamics: assessment of accuracy and model selection protocols based on molecular dynamics simulation J. Biomol. NMR 29 2004 243 257
8. A.R. Cohen, D.F. Woods, S.M. Marfatia, Z. Walther, A.H. Chishti, and J.M. Anderson Human CASK/LIN-2 binds syndecan-2 and protein 4.1 and localizes to the basolateral membrane of epithelial cells J. Cell Biol. 142 1998 129 138
9. R. Cole, and J.P. Loria FAST-Modelfree: a program for rapid automated analysis of solution NMR spin-relaxation data J. Biomol. NMR 26 2003 203 213
10. J.R. Couchman Transmembrane signaling proteoglycans Annu. Rev. Cell Dev. Biol. 26 2010 89 114
11. P. De Los Rios, F. Cecconi, A. Pretre, G. Dietler, O. Michielin, F. Piazza, and B. Juanico Functional dynamics of PDZ binding domains: a normal-mode analysis Biophys. J. 89 2005 14 21
12. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
13. A. Dhulesia, J. Gsponer, and M. Vendruscolo Mapping of two networks of residues that exhibit structural and dynamical changes upon binding in a PDZ domain protein J. Am. Chem. Soc. 130 2008 8931 8939
14. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
15. I.M. Ethell, K. Hagihara, Y. Miura, F. Irie, and Y. Yamaguchi Synbindin, A novel syndecan-2-binding protein in neuronal dendritic spines J. Cell Biol. 151 2000 53 68
16. W. Feng, H. Wu, L.N. Chan, and M. Zhang Par-3-mediated junctional localization of the lipid phosphatase PTEN is required for cell polarity establishment J. Biol. Chem. 283 2008 23440 23449
17. K.K. Frederick, M.S. Marlow, K.G. Valentine, and A.J. Wand Conformational entropy in molecular recognition by proteins Nature 448 2007 325 329
18. E.J. Fuentes, C.J. Der, and A.L. Lee Ligand-dependent dynamics and intramolecular signaling in a PDZ domain J. Mol. Biol. 335 2004 1105 1115
19. E.J. Fuentes, S.A. Gilmore, R.V. Mauldin, and A.L. Lee Evaluation of energetic and dynamic coupling networks in a PDZ domain protein J. Mol. Biol. 364 2006 337 351
20. Y. Gao, M. Li, W. Chen, and M. Simons Synectin, syndecan-4 cytoplasmic domain binding PDZ protein, inhibits cell migration J. Cell. Physiol. 184 2000 373 379
21. N. Halabi, O. Rivoire, S. Leibler, and R. Ranganathan Protein sectors: evolutionary units of three-dimensional structure Cell 138 2009 774 786
22. B.Z. Harris, B.J. Hillier, and W.A. Lim Energetic determinants of internal motif recognition by PDZ domains Biochemistry 40 2001 5921 5930
23. A. Hienola, S. Tumova, E. Kulesskiy, and H. Rauvala N-syndecan deficiency impairs neural migration in brain J. Cell Biol. 174 2006 569 580
24. B.A. Johnson, and R.A. Blevins NMR View: A computer program for the visualization and analysis of NMR data J. Biomol. NMR 4 1994 603 614
25. B.S. Kang, D.R. Cooper, F. Jelen, Y. Devedjiev, U. Derewenda, Z. Dauter, J. Otlewski, and Z.S. Derewenda PDZ tandem of human syntenin: crystal structure and functional properties Structure 11 2003 459 468
26. L.E. Kay, D.R. Muhandiram, N.A. Farrow, Y. Aubin, and J.D. Forman-Kay Correlation between dynamics and high affinity binding in an SH2 domain interaction Biochemistry 35 1996 361 368
27. Y. Kong, and M. Karplus Signaling pathways of PDZ2 domain: a molecular dynamics interaction correlation analysis Proteins 74 2009 145 154
28. D.M. Korzhnev, I. Bezsonova, S. Lee, T.V. Chalikian, and L.E. Kay Alternate binding modes for a ubiquitin-SH3 domain interaction studied by NMR spectroscopy J. Mol. Biol. 386 2009 391 405
29. G. Kozlov, D. Banville, K. Gehring, and I. Ekiel Solution structure of the PDZ2 domain from cytosolic human phosphatase hPTP1E complexed with a peptide reveals contribution of the beta2-beta3 loop to PDZ domain-ligand interactions J. Mol. Biol. 320 2002 813 820
30. K. Lambaerts, S.A. Wilcox-Adelman, and P. Zimmermann The signaling mechanisms of syndecan heparan sulfate proteoglycans Curr. Opin. Cell Biol. 21 2009 662 669
31. A.B. Law, E.J. Fuentes, and A.L. Lee Conservation of side-chain dynamics within a protein family J. Am. Chem. Soc. 131 2009 6322 6323
32. A.L. Lee, and A.J. Wand Assessing potential bias in the determination of rotational correlation times of proteins by NMR relaxation J. Biomol. NMR 13 1999 101 112
33. H.J. Lee, and J.J. Zheng PDZ domains and their binding partners: structure, specificity, and modification Cell Commun. Signal. 8 2010 1 18
34. α nuclear spin relaxation J. Biomol. NMR 9 1997 287 298
35. 13C NMR relaxation techniques for the study of protein methyl group dynamics in solution J. Am. Chem. Soc. 121 1999 2891 2902
36. A.L. Lee, S.A. Kinnear, and A.J. Wand Redistribution and loss of side chain entropy upon formation of a calmodulin-peptide complex Nat. Struct. Biol. 7 2000 72 77
37. G. Lipari, and A. Szabo Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules: 1. Theory and range of validity J. Am. Chem. Soc. 104 1982 4546 4559
38. S.W. Lockless, and R. Ranganathan Evolutionarily conserved pathways of energetic connectivity in protein families Science 286 1999 295 299
39. G.I. Makhatadze, V.V. Loladze, D.N. Ermolenko, X. Chen, and S.T. Thomas Contribution of surface salt bridges to protein stability: guidelines for protein engineering J. Mol. Biol. 327 2003 1135 1148
40. A. Malliri, S. van Es, S. Huveneers, and J.G. Collard The Rac exchange factor Tiam1 is required for the establishment and maintenance of cadherin-based adhesions J. Biol. Chem. 279 2004 30092 30098
41. A.M. Mandel, M. Akke, and A.G. Palmer 3rd Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme J. Mol. Biol. 246 1995 144 163
42. M.S. Marlow, J. Dogan, K.K. Frederick, K.G. Valentine, and A.J. Wand The role of conformational entropy in molecular recognition by calmodulin Nat. Chem. Biol. 6 2010 352 358
43. M. Masuda, T. Maruyama, T. Ohta, A. Ito, T. Hayashi, K. Tsukasaki, S. Kamihira, S. Yamaoka, H. Hoshino, and T. Yoshida CADM1 interacts with Tiam1 and promotes invasive phenotype of human T-cell leukemia virus type I-transformed cells and adult T-cell leukemia cells J. Biol. Chem. 285 2010 15511 15522
44. A.E. Mertens, T.P. Rygiel, C. Olivo, R. van der Kammen, and J.G. Collard The Rac activator Tiam1 controls tight junction biogenesis in keratinocytes through binding to and activation of the Par polarity complex J. Cell Biol. 170 2005 1029 1037
45. (2)H-enriched proteins in solution J. Am. Chem. Soc. 124 2002 6439 6448
46. Y. Miyamoto, J. Yamauchi, A. Tanoue, C. Wu, and W.C. Mobley TrkB binds and tyrosine-phosphorylates Tiam1, leading to activation of Rac1 and induction of changes in cellular morphology Proc. Natl. Acad. Sci. USA 103 2006 10444 10449
47. A.T. Namanja, T. Peng, J.S. Zintsmaster, A.C. Elson, M.G. Shakour, and J.W. Peng Substrate recognition reduces side-chain flexibility for conserved hydrophobic residues in human Pin1 Structure 15 2007 313 327
48. A.T. Namanja, X.J. Wang, B. Xu, A.Y. Mercedes-Camacho, K.A. Wilson, F.A. Etzkorn, and J.W. Peng Stereospecific gating of functional motions in Pin1 Proc. Natl. Acad. Sci. USA 108 2011 12289 12294
49. T. Nishimura, T. Yamaguchi, K. Kato, M. Yoshizawa, Y. Nabeshima, S. Ohno, M. Hoshino, and K. Kaibuchi PAR-6-PAR-3 mediates Cdc42-induced Rac activation through the Rac GEFs STEF/Tiam1 Nat. Cell Biol. 7 2005 270 277
50. N. Ota, and D.A. Agard Intramolecular signaling pathways revealed by modeling anisotropic thermal diffusion J. Mol. Biol. 351 2005 345 354
51. V.L. Ott, and A.C. Rapraeger Tyrosine phosphorylation of syndecan-1 and -4 cytoplasmic domains in adherent B82 fibroblasts J. Biol. Chem. 273 1998 35291 35298
52. L. Pangon, C. Van Kralingen, M. Abas, R.J. Daly, E.A. Musgrove, and M.R. Kohonen-Corish The PDZ-binding motif of MCC is phosphorylated at position -1 and controls lamellipodia formation in colon epithelial cells Biochim. Biophys. Acta 1823 2012 1058 1067
53. C.M. Petit, J. Zhang, P.J. Sapienza, E.J. Fuentes, and A.L. Lee Hidden dynamic allostery in a PDZ domain Proc. Natl. Acad. Sci. USA 106 2009 18249 18254
54. J.W. Pflugrath The finer things in X-ray diffraction data collection Acta Crystallogr. D Biol. Crystallogr. 55 1999 1718 1725
55. J. Reiland, V.L. Ott, C.S. Lebakken, C. Yeaman, J. McCarthy, and A.C. Rapraeger Pervanadate activation of intracellular kinases leads to tyrosine phosphorylation and shedding of syndecan-1 Biochem. J. 319 1996 39 47
56. J.A. Roper, R.C. Williamson, and M.D. Bass Syndecan and integrin interactomes: large complexes in small spaces Curr. Opin. Struct. Biol. 22 2012 583 590
57. T.R. Shepherd, and E.J. Fuentes Structural and thermodynamic analysis of PDZ-ligand interactions Methods Enzymol. 488 2011 81 100
58. T.R. Shepherd, S.M. Klaus, X. Liu, S. Ramaswamy, K.A. DeMali, and E.J. Fuentes The Tiam1 PDZ domain couples to Syndecan1 and promotes cell-matrix adhesion J. Mol. Biol. 398 2010 730 746
59. T.R. Shepherd, R.L. Hard, A.M. Murray, D. Pei, and E.J. Fuentes Distinct ligand specificity of the Tiam1 and Tiam2 PDZ domains Biochemistry 50 2011 1296 1308
60. B. Sulka, H. Lortat-Jacob, R. Terreux, F. Letourneur, and P. Rousselle Tyrosine dephosphorylation of the syndecan-1 PDZ binding domain regulates syntenin-1 recruitment J. Biol. Chem. 284 2009 10659 10671
61. M. Tanaka, R. Ohashi, R. Nakamura, K. Shinmura, T. Kamo, R. Sakai, and H. Sugimura Tiam1 mediates neurite outgrowth induced by ephrin-B1 and EphA2 EMBO J. 23 2004 1075 1088
62. 15N NMR relaxation J. Am. Chem. Soc. 117 1995 12562 12566
63. R.C. Tyler, F.C. Peterson, and B.F. Volkman Distal interactions within the par3-VE-cadherin complex Biochemistry 49 2010 951 957
64. S.R. Tzeng, and C.G. Kalodimos Protein dynamics and allostery: an NMR view Curr. Opin. Struct. Biol. 21 2011 62 67
65. S.R. Tzeng, and C.G. Kalodimos Protein activity regulation by conformational entropy Nature 488 2012 236 240
66. A. Vagin, and A. Teplyakov MOLREP: an automated program for molecular replacement J. Appl. Cryst. 30 1997 1022 1025
67. A.A. Vagin, R.A. Steiner, A.A. Lebedev, L. Potterton, S. McNicholas, F. Long, and G.N. Murshudov REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use Acta Crystallogr. D Biol. Crystallogr. 60 2004 2184 2195
68. P. von Nandelstadh, M. Ismail, C. Gardin, H. Suila, I. Zara, A. Belgrano, G. Valle, O. Carpen, and G. Faulkner A class III PDZ binding motif in the myotilin and FATZ families binds enigma family proteins: a common link for Z-disc myopathies Mol. Cell. Biol. 29 2009 822 834
69. D.S. Whitney, F.C. Peterson, and B.F. Volkman A conformational switch in the CRIB-PDZ module of Par-6 Structure 19 2011 1711 1722
70. H. Zhang, and I.G. Macara The polarity protein PAR-3 and TIAM1 cooperate in dendritic spine morphogenesis Nat. Cell Biol. 8 2006 227 237
71. P. Zimmermann, D. Tomatis, M. Rosas, J. Grootjans, I. Leenaerts, G. Degeest, G. Reekmans, C. Coomans, and G. David Characterization of syntenin, a syndecan-binding PDZ protein, as a component of cell adhesion sites and microfilaments Mol. Biol. Cell 12 2001 339 350