NMR studies of a heterotypic Sam-Sam domain association: The interaction between the lipid phosphatase Ship2 and the EphA2 receptor

Biochemistry

Volumn 47, Issue 48, 2008, Pages 12721-12728

  Leone, Marilisa ^a   Cellitti, Jason ^a   Pellecchia, Maurizio ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; BINDING ENERGY; FLOW INTERACTIONS; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; THREE DIMENSIONAL; VOLUMETRIC ANALYSIS;

ANTICANCER ACTIVITIES; BINDING AFFINITIES; BIOLOGICAL PROCESSES; DIMENSIONAL STRUCTURES; DO-MAINS; HETERODIMERIZATION; ISOTHERMAL TITRATION CALORIMETRIES; LIPID PHOSPHATASES; NMR STUDIES; PROTEIN INTERACTIONS; RECEPTOR ENDOCYTOSISES; SMALL MOLECULES; STRUCTURAL ELEMENTS;

ASSOCIATION REACTIONS;

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

AMINO ACID SEQUENCE; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; ENDOCYTOSIS; ISOTHERMAL TITRATION CALORIMETRY; NUCLEAR OVERHAUSER EFFECT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE;

AMINO ACID SEQUENCE; ANTINEOPLASTIC AGENTS; CALORIMETRY; DRUG DESIGN; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECEPTOR, EPHA2;

EID: 57049090580     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801713f     Document Type: Article

References (45)

1. Pesesse, X., Moreau, C., Drayer, A. L., Woscholski, R., Parker, P., and Erneux, C. (1998) The SH2 domain containing inositol 5-phosphatase SHIP2 displays phosphatidylinositol 3,4,5-trisphosphate and inositol 1,3,4,5-tetrakisphosphate 5-phosphatase activity. FEBS Lett 437 (3), 301-303.
2. Pesesse, X., Deleu, S., De Smedt, F., Drayer, L., and Erneux, C. (1997) Identification of a second SH2-domain-containing protein closely related to the phosphatidylinositol polyphosphate 5-phosphatase SHIP. Biochem. Biophys. Res. Commun. 239, (3), 697-700.
3. Clement, S., Krause, U., Desmedt, F., Tanti, J. F., Behrends, J., Pesesse, X., Sasaki, T., Penninger, J., Doherty, M., Malaisse, W., Dumont, J. E., Le Marchand-Brustel, Y., Erneux, C., Hue, L., and Schurmans, S. (2001) The lipid phosphatase SHIP2 controls insulin sensitivity. Nature 409 (6816), 92-97.
4. Sleeman, M. W., Wortley, K. E., Lai, K. M., Gowen, L. C., Kintner, J., Kline, W. O., Garcia, K., Stitt, T. N., Yancopoulos, G. D., Wiegand, S. J., and Glass, D. J. (2005) Absence of the lipid phosphatase SHIP2 confers resistance to dietary obesity. Nat. Med. 11 (2), 199-205.
5. Lazar, D. F., and Saltiel, A. R. (2006) Lipid phosphatases as drug discovery targets for type 2 diabetes. Nat. Rev. Drug Discovery 5 (4), 333-342.
6. 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 (4), 2683-2694.
7. Walker-Daniels, J., Hess, A. R., Hendrix, M. J., and Kinch, M. S. (2003) Differential regulation of EphA2 in normal and malignant cells. Am. J. Pathol. 162 (4), 1037-1042.
8. Ireton, R. C., and Chen, J. (2005) EphA2 receptor tyrosine kinase as a promising target for cancer therapeutics. Curr. Cancer Drug Targets 5 (3), 149-157.
9. Carles-Kinch, K., Kilpatrick, K. E., Stewart, J. C., and Kinch, M. S. (2002) Antibody targeting of the EphA2 tyrosine kinase inhibits malignant cell behavior. Cancer Res. 62 (10), 2840-2847.
10. 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 (5), 1353-1358.
11. 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 (8), 2836-2841.
12. Harada, B. T., Knight, M. J., Imai, S., Qiao, F., Ramachander, R., Sawaya, M. R., Gingery, M., Sakane, F., and Bowie, J. U. (2008) Regulation of enzyme localization by polymerization: polymer formation by the SAM domain of diacylglycerol kinase delta1. Structure 16 (3), 380-387.
13. Neri, D., Szyperski, T., Otting, G., Senn, H., and Wuthrich, K. (1989) Stereospecific nuclear magnetic resonance assignments of the methyl groups of valine and leucine in the DNA-binding domain of the 434 repressor by biosynthetically directed fractional 13C labeling. Biochemistry 28 (19), 7510-7516.
14. Grzesiek, S., and Bax, A. (1993) Amino acid type determination in the sequential assignment procedure of uniformly 13C/15N-enriched proteins. J. Biomol. NMR 3 (2), 185-204.
15. Bartels, C., Xia, T. H., Billeter, M., Güntert, P., and Wüthrich, K. (1995) The program XEASY for computer-supported NMR spectral analysis of biological macromolecules. J. Biomol. NMR 5, 1-10.
16. Farrow, N. A., Muhandiram, R., Singer, A. U., Pascal, S. M., Kay, C. M., Gish, G., Shoelson, S. E., Pawson, T., Forman-Kay, J. D., and Kay, L. E. (1994) Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33 (19), 5984-6003.
17. Viles, J. H., Duggan, B. M., Zaborowski, E., Schwarzinger, S., Huntley, J. J., Kroon, G. J., Dyson, H. J., and Wright, P. E. (2001) Potential bias in NMR relaxation data introduced by peak intensity analysis and curve fitting methods. J. Biomol. NMR 21 (1), 1-9.
18. Kay, L. E., Torchia, D. A., and Bax, A. (1989) Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 28 (23), 8972-8979.
19. Talluri, S., and Wagner, G. (1996) An optimized 3D NOESY-HSQC. J. Magn. Reson. B 112 (2), 200-205.
20. Kumar, A., Ernst, R. R., and Wuthrich, K. (1980) A 2D nuclear Overhauser enhancement (2D NOE) experiment for elucidation of complete proton-proton cross relaxation networks in biological macromolecules. Biochm. Biophys. Res. Commun. 95, 1-6.
21. 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 (1), 209-227.
22. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics 14 (1), 51-529-32.
23. 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 (4), 477-486.
24. Teschner, M., Henn, C., Vollhardt, H., Reiling, S., and Brickmann, J. (1994) Texture mapping: a new tool for molecular graphics. J. Mol. Graphics 12 (2), 98-105.
25. 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 (7), 1731-1737.
26. Pellecchia, M. (2005) Solution nuclear magnetic resonance spectroscopy techniques for probing intermolecular interactions. Chem. Biol. 12 (9), 961-971.
27. Pellecchia, M., Sem, D. S., and Wuthrich, K. (2002) NMR in drug discovery. Nat. Rev. Drug Discovery 1 (3), 211-219.
28. Farmer, B. T., Constantine, K. L., Goldfarb, V., Friedrichs, M. S., Wittekind, M., Yanchunas, J., Robertson, J. G., and Mueller, L. (1996) Localizing the NADP+ binding site on the MurB enzyme by NMR. Nat. Struct. Biol. 3 (12), 995-997.
29. Kwan, J. J., and Donaldson, L. W. (2007) The NMR structure of the murine DLC2 SAM domain reveals a variant fold that is similar to a four-helix bundle. BMC Struct. Biol. 7 (1), 34.
30. Cicero, D. O., Falconi, M., Candi, E., Mele, S., Cadot, B., Di Venere, A., Rufini, S., Melino, G., and Desideri, A. (2006) NMR structure of the p63 SAM domain and dynamical properties of G534V and T537P pathological mutants, identified in the AEC syndrome. Cell Biochem. Biophys. 44 (3), 475-489.
31. Edwards, T. A., Butterwick, J. A., Zeng, L., Gupta, Y. K., Wang, X., Wharton, R. P., Palmer, A. G., 3rd, Aggarwal, A. K., and Solution structure of the Vts1 SAM domain in the presence of, R. N. A. (2006) J. Mol. Biol. 356 (5), 1065-1072.
32. Li, H., Fung, K. L., Jin, D. Y., Chung, S. S., Ching, Y. P., Ng, I. O., Sze, K. H., Ko, B. C., and Sun, H. (2007) Solution structures, dynamics, and lipid-binding of the sterile alpha-motif domain of the deleted in liver cancer 2. Proteins 67 (4), 1154-1166.
33. Oberstrass, F. C., Lee, A., Stefl, R., Janis, M., Chanfreau, G., and Allain, F. H. (2006) Shape-specific recognition in the structure of the Vts1p SAM domain with RNA. Nat. Struct. Mol. Biol. 13 (2), 160-167.
34. 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 (17), 3389-3402.
35. Stapleton, D., Balan, I., Pawson, T., and Sicheri, F. (1999) The crystal structure of an Eph receptor SAM domain reveals a mechanism for modular dimerization. Nat. Struct. Biol. 6 (1), 44-49.
36. Thanos, C. D., Faham, S., Goodwill, K. E., Cascio, D., Phillips, M., and Bowie, J. U. (1999) Monomeric structure of the human EphB2 sterile alpha motif domain. J. Biol. Chem. 274 (52), 37301-37306.
37. Raaijmakers, J. H., Deneubourg, L., Rehmann, H., de Koning, J., Zhang, Z., Krugmann, S., Erneux, C., and Bos, J. L. (2007) The PI3K effector Arap3 interacts with the PI(3,4,5)P(3) phosphatase SHIP2 in a SAM domain-dependent manner. Cell. Signalling 19 (6), 1249-1257.
38. Slupsky, C. M., Gentile, L. N., Donaldson, L. W., Mackereth, C. D., Seidel, J. J., Graves, B. J., and McIntosh, L. P. (1998) Structure of the Ets-1 pointed domain and mitogen-activated protein kinase phosphorylation site. Proc. Natl. Acad. Sci. U.S.A. 95 (21), 12129-12134.
39. Smalla, M., Schmieder, P., Kelly, M., Ter Laak, A., Krause, G., Ball, L., Wahl, M., Bork, P., and Oschkinat, H. (1999) Solution structure of the receptor tyrosine kinase EphB2 SAM domain and identification of two distinct homotypic interaction sites. Protein Sci. 8 (10), 1954-1961.
40. Bhattacharjya, S., Xu, P., Gingras, R., Shaykhutdinov, R., Wu, C., Whiteway, M., and Ni, F. (2004) Solution structure of the dimeric SAM domain of MAPKKK Ste11 and its interactions with the adaptor protein Ste50 from the budding yeast: implications for Ste11 activation and signal transmission through the Ste50-Ste11 complex. J. Mol. Biol. 344 (4), 1071-1087.
41. Thanos, C. D., Goodwill, K. E., and Bowie, J. U. (1999) Oligomeric structure of the human EphB2 receptor SAM domain. Science 283 (5403), 833-836.
42. Kim, C. A., Phillips, M. L., Kim, W., Gingery, M., Tran, H. H., Robinson, M. A., Faham, S., and Bowie, J. U. (2001) Polymerization of the SAM domain of TEL in leukemogenesis and transcriptional repression. EMBO J. 20 (15), 4173-4182.
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 (6), 453-457.
44. Qiao, F., Song, H., Kim, C. A., Sawaya, M. R., Hunter, J. B., Gingery, M., Rebay, I., Courey, A. J., and Bowie, J. U. (2004) Derepression by depolymerization; structural insights into the regulation of Yan by Mae. Cell 118 (2), 163-173.
45. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and ClustalX version 2.0. Bioinformatics 23 (21), 2947-2948.