Solution structure of the first Sam domain of Odin and binding studies with the EphA2 receptor

Biochemistry

Volumn 51, Issue 10, 2012, Pages 2136-2145

  Mercurio, Flavia Anna ^a   Marasco, Daniela ^a,b,c   Pirone, Luciano ^c   Pedone, Emilia Maria ^b,c   Pellecchia, Maurizio ^d   Leone, Marilisa ^b,c  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b Centro Interuniversitario di Ricerca sui Peptidi Bioattivi (CIRPEB)   (Italy)

^c CNR   (Italy)

^d BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; BINDING MODES; BINDING STUDIES; CANCER CELLS; ISOTHERMAL TITRATION CALORIMETRY; MICROMOLAR RANGE; MOLECULAR MODELING STUDIES; NMR CHEMICAL SHIFT PERTURBATIONS; RECEPTOR ENDOCYTOSIS; SOLUTION STRUCTURES; STRUCTURAL ELEMENTS; THERAPEUTIC COMPOUNDS; TOPOLOGY CHARACTERISTICS;

BINDING ENERGY;

MOLECULAR BIOLOGY;

ANKYRIN; EPHRIN RECEPTOR A2; PHOSPHATASE; PROTEIN ODIN; PROTEIN SHIP2; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING KINETICS; CARBON NUCLEAR MAGNETIC RESONANCE; ENDOCYTOSIS; HETERONUCLEAR SINGLE QUANTUM COHERENCE; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR DOCKING; MOLECULAR INTERACTION; MOLECULAR MODEL; NITROGEN NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; RECEPTOR BINDING; STERILE ALPHA MOTIF DOMAIN; SURFACE PLASMON RESONANCE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ENDOCYTOSIS; HUMANS; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTOR, EPHA2; RECOMBINANT PROTEINS; SOLUTIONS; SURFACE PLASMON RESONANCE; THERMODYNAMICS;

EID: 84858225733     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300141h     Document Type: Article

References (46)

1. Pasquale, E. B. (2010) Eph receptors and ephrins in cancer: Bidirectional signalling and beyond Nat. Rev. Cancer 10, 165-180
2. Surawska, H., Ma, P. C., and Salgia, R. (2004) The role of ephrins and Eph receptors in cancer Cytokine Growth Factor Rev. 15, 419-433 (Pubitemid 39550453)
3. Koolpe, M., Dail, M., and Pasquale, E. B. (2002) An ephrin mimetic peptide that selectively targets the EphA2 receptor J. Biol. Chem. 277, 46974-46979 (Pubitemid 36159202)
4. Cooper, M. A., Son, A. I., Komlos, D., Sun, Y., Kleiman, N. J., and Zhou, R. (2008) Loss of ephrin-A5 function disrupts lens fiber cell packing and leads to cataract Proc. Natl. Acad. Sci. U.S.A. 105, 16620-16625
5. Jun, G., Guo, H., Klein, B. E., Klein, R., Wang, J. J., Mitchell, P., Miao, H., Lee, K. E., Joshi, T., Buck, M., Chugha, P., Bardenstein, D., Klein, A. P., Bailey-Wilson, J. E., Gong, X., Spector, T. D., Andrew, T., Hammond, C. J., Elston, R. C., Iyengar, S. K., and Wang, B. (2009) EPHA2 is associated with age-related cortical cataract in mice and humans PLoS Genet. 5, e1000584
6. Zhang, T., Hua, R., Xiao, W., Burdon, K. P., Bhattacharya, S. S., Craig, J. E., Shang, D., Zhao, X., Mackey, D. A., Moore, A. T., Luo, Y., Zhang, J., and Zhang, X. (2009) Mutations of the EPHA2 receptor tyrosine kinase gene cause autosomal dominant congenital cataract Hum. Mutat. 30, E603-E611
7. Lupberger, J., Zeisel, M. B., Xiao, F., Thumann, C., Fofana, I., Zona, L., Davis, C., Mee, C. J., Turek, M., Gorke, S., Royer, C., Fischer, B., Zahid, M. N., Lavillette, D., Fresquet, J., Cosset, F. L., Rothenberg, S. M., Pietschmann, T., Patel, A. H., Pessaux, P., Doffoel, M., Raffelsberger, W., Poch, O., McKeating, J. A., Brino, L., and Baumert, T. F. (2011) EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy Nat. Med. 17, 589-595
8. Zhuang, G., Hunter, S., Hwang, Y., and Chen, J. (2007) Regulation of EphA2 receptor endocytosis by SHIP2 lipid phosphatase via phosphatidylinositol 3-kinase-dependent Rac1 activation J. Biol. Chem. 282, 2683-2694 (Pubitemid 47076792)
9. Kim, J., Lee, H., Kim, Y., Yoo, S., Park, E., and Park, S. (2010) The SAM domains of Anks family proteins are critically involved in modulating the degradation of EphA receptors Mol. Cell. Biol. 30, 1582-1592
10. Kim, C. A. and Bowie, J. U. (2003) SAM domains: Uniform structure, diversity of function Trends Biochem. Sci. 28, 625-628 (Pubitemid 37500895)
11. Meruelo, A. D. and Bowie, J. U. (2009) Identifying polymer-forming SAM domains Proteins 74, 1-5
12. Leone, M., Cellitti, J., and Pellecchia, M. (2008) NMR studies of a heterotypic Sam-Sam domain association: The interaction between the lipid phosphatase Ship2 and the EphA2 receptor Biochemistry 47, 12721-12728
13. Rajakulendran, T., Sahmi, M., Kurinov, I., Tyers, M., Therrien, M., and Sicheri, F. (2008) CNK and HYP form a discrete dimer by their SAM domains to mediate RAF kinase signaling Proc. Natl. Acad. Sci. U.S.A. 105, 2836-2841 (Pubitemid 351723630)
14. Ramachander, R. and Bowie, J. U. (2004) SAM domains can utilize similar surfaces for the formation of polymers and closed oligomers J. Mol. Biol. 342, 1353-1358 (Pubitemid 39208663)
15. Wei, Z., Zheng, S., Spangler, S. A., Yu, C., Hoogenraad, C. C., and Zhang, M. (2011) Liprin-mediated large signaling complex organization revealed by the liprin-α/CASK and liprin-α/liprin-β complex structures Mol. Cell 43, 586-598
16. Emaduddin, M., Edelmann, M. J., Kessler, B. M., and Feller, S. M. (2008) Odin (ANKS1A) is a Src family kinase target in colorectal cancer cells Cell Commun. Signaling 6, 7
17. Ghersi, E., Vito, P., Lopez, P., Abdallah, M., and D'Adamio, L. (2004) The intracellular localization of amyloid β protein precursor (AβPP) intracellular domain associated protein-1 (AIDA-1) is regulated by AβPP and alternative splicing J. Alzheimer's Dis. 6, 67-78 (Pubitemid 38418559)
18. Leone, M., Cellitti, J., and Pellecchia, M. (2009) The Sam domain of the lipid phosphatase Ship2 adopts a common model to interact with Arap3-Sam and EphA2-Sam BMC Struct. Biol. 9, 59
19. 13C labeling Biochemistry 28, 7510-7516 (Pubitemid 19238098)
20. 15N- enriched proteins J. Biomol. NMR 3, 185-204
21. Bartels, C., Xia, T., Billeter, M., Güntert, P., and Wüthrich, K. (1995) The program XEASY for computer-supported NMR spectral analysis of biological macromolecules J. Biomol. NMR 6, 1-10
22. 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease Biochemistry 28, 8972-8979 (Pubitemid 19283459)
23. Morris, K. and Johnson, C. S. (1992) Diffusion-ordered two-dimensional nuclear magnetic resonance spectroscopy J. Am. Chem. Soc. 114, 3139-3141
24. Price, W. S. (1997) Pulsed-field gradient nuclear magnetic resonance as a tool for studying translational diffusion: Part 1. Basic theory Concepts Magn. Reson. 9, 299-336 (Pubitemid 127116750)
25. Talluri, S. and Wagner, G. (1996) An optimized 3D NOESY-HSQC J. Magn. Reson., Ser. B 112, 200-205 (Pubitemid 126758725)
26. Kumar, A., Ernst, R. R., and Wuthrich, K. (1980) A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules Biochem. Biophys. Res. Commun. 95, 1-6
27. Herrmann, T., Guntert, P., and Wuthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA J. Mol. Biol. 319, 209-227 (Pubitemid 34729497)
28. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures J. Mol. Graphics 14, 29-32, 51-55
29. Sanner, M. F., Olson, A. J., and Spehner, J. C. (1996) Reduced surface: An efficient way to compute molecular surfaces Biopolymers 38, 305-320
30. Johnsson, B., Lofas, S., and Lindquist, G. (1991) Immobilization of proteins to a carboxymethyldextran-modified gold surface for biospecific interaction analysis in surface plasmon resonance sensors Anal. Biochem. 198, 268-277
31. Rich, R. L. and Myszka, D. G. (2001) BIACORE J: A new platform for routine biomolecular interaction analysis J. Mol. Recognit. 14, 223-228 (Pubitemid 32824543)
32. de Vries, S. J., van Dijk, M., and Bonvin, A. M. (2010) The HADDOCK web server for data-driven biomolecular docking Nat. Protoc. 5, 883-897
33. van Dijk, A. D. and Bonvin, A. M. (2006) Solvated docking: Introducing water into the modelling of biomolecular complexes Bioinformatics 22, 2340-2347 (Pubitemid 44566962)
34. Kurabi, A., Brener, S., Mobli, M., Kwan, J. J., and Donaldson, L. W. (2009) A nuclear localization signal at the SAM-SAM domain interface of AIDA-1 suggests a requirement for domain uncoupling prior to nuclear import J. Mol. Biol. 392, 1168-1177
35. Pellecchia, M. (2005) Solution nuclear magnetic resonance spectroscopy techniques for probing intermolecular interactions Chem. Biol. 12, 961-971 (Pubitemid 41338806)
36. + binding site on the MurB enzyme by NMR Nat. Struct. Biol. 3, 995-997 (Pubitemid 27014626)
37. Stafford, R. L., Hinde, E., Knight, M. J., Pennella, M. A., Ear, J., Digman, M. A., Gratton, E., and Bowie, J. U. (2011) Tandem SAM Domain Structure of Human Caskin1: A Presynaptic, Self-Assembling Scaffold for CASK Structure 19, 1826-1836
38. Dominguez, C., Boelens, R., and Bonvin, A. M. (2003) HADDOCK: A protein-protein docking approach based on biochemical or biophysical information J. Am. Chem. Soc. 125, 1731-1737 (Pubitemid 36232568)
39. Zhuang, G., Brantley-Sieders, D. M., Vaught, D., Yu, J., Xie, L., Wells, S., Jackson, D., Muraoka-Cook, R., Arteaga, C., and Chen, J. (2010) Elevation of receptor tyrosine kinase EphA2 mediates resistance to trastuzumab therapy Cancer Res. 70, 299-308
40. Thanos, C. D., Faham, S., Goodwill, K. E., Cascio, D., Phillips, M., and Bowie, J. U. (1999) Monomeric structure of the human EphB2 sterile α motif domain J. Biol. Chem. 274, 37301-37306
41. Wilkins, D. K., Grimshaw, S. B., Receveur, V., Dobson, C. M., Jones, J. A., and Smith, L. J. (1999) Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques Biochemistry 38, 16424-16431
42. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs Nucleic Acids Res. 25, 3389-3402 (Pubitemid 27359211)
43. Kim, C. A., Gingery, M., Pilpa, R. M., and Bowie, J. U. (2002) The SAM domain of polyhomeotic forms a helical polymer Nat. Struct. Biol. 9, 453-457 (Pubitemid 34568791)
44. Lee, H. J., Hota, P. K., Chugha, P., Guo, H., Miao, H., Zhang, L., Kim, S. J., Stetzik, L., Wang, B. C., and Buck, M. (2012) NMR Structure of a Heterodimeric SAM:SAM Complex: Characterization and Manipulation of EphA2 Binding Reveal New Cellular Functions of SHIP2 Structure 20, 41-55
45. Shiels, A., Bennett, T. M., Knopf, H. L., Maraini, G., Li, A., Jiao, X., and Hejtmancik, J. F. (2008) The EPHA2 gene is associated with cataracts linked to chromosome 1p Mol. Vision 14, 2042-2055
46. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR J. Biomol. NMR 8, 477-486 (Pubitemid 126706801)