An examination of dynamics crosstalk between SH2 and SH3 domains by hydrogen/deuterium exchange and mass spectrometry

Protein Science

Volumn 15, Issue 1, 2006, Pages 65-73

  Hochrein, James M ^a   Lerner, Edwina C ^b   Schiavone, Anthony P ^b   Smithgall, Thomas E ^b   Engen, John R ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Domains; Hck; Ligand binding; Protein dynamics; Src homology 2; Src homology 3

Indexed keywords

HEMATOPOIETIC CELL KINASE; PROTEIN TYROSINE KINASE;

ARTICLE; COVALENT BOND; DEUTERIUM HYDROGEN EXCHANGE; LIGAND BINDING; MASS SPECTROMETRY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; SRC HOMOLOGY DOMAIN; STRUCTURE ANALYSIS;

ALLOSTERIC SITE; DEUTERIUM EXCHANGE MEASUREMENT; HUMANS; LIGANDS; MASS SPECTROMETRY; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-HCK; SRC HOMOLOGY DOMAINS; THERMODYNAMICS;

EID: 29344471038     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.051782206     Document Type: Article

References (38)

1. Bai, Y., Milne, J.S., Mayne, L., and Englander, S.W. 1993. Primary structure effects on peptide group hydrogen exchange. Proteins 17: 75-86.
2. Barila, D. and Superti-Furga, G. 1998. An intramolecular SH3-domain interaction regulates c-Abl activity. Nat. Genet. 18: 280-282.
3. Brown, M.T. and Cooper, J.A. 1996. Regulation, substrates and functions of src. Biochim. Biophys. Acta 1287: 121-149.
4. Bru, C., Courcelle, E., Carrere, S., Beausse, Y., Dalmar, S., and Kahn, D. 2005. The ProDom database of protein domain families: More emphasis on 3D. Nucleic Acids Res. 33: D212-D215.
5. Busenlehner, L.S. and Armstrong, R.N. 2005. Insights into enzyme structure and dynamics elucidated by amide H/D exchange mass spectrometry. Arch. Biochem. Biophys. 433: 34-46.
6. Cobos, E.S., Pisabarro, M.T., Vega, M.C., Lacroix, E., Serrano, L., Ruiz-Sanz, J., and Martinez, J.C. 2004. A miniprotein scaffold used to assemble the polyproline II binding epitope recognized by SH3 domains. J. Mol. Biol. 342: 355-365.
7. Engen, J.R., Smithgall, T.E., Gmeiner, W.H., and Smith, D.L. 1997. Identification and localization of slow, natural, cooperative unfolding in the hematopoietic cell kinase SH3 domain by amide hydrogen exchange and mass spectrometry. Biochemistry 36: 14384-14391.
8. Engen, J.R., Gmeiner, W.H., Smithgall, T.E., and Smith, D.L. 1999a. Hydrogen exchange shows peptide binding stabilizes motions in Hck SH2. Biochemistry 38: 8926-8935.
9. Engen, J.R., Smithgall, T.E., Gmeiner, W.H., and Smith, D.L. 1999b. Comparison of SH3 and SH2 domain dynamics when expressed alone or in an SH(3+2) construct: The role of protein dynamics in functional regulation. J. Mol. Biol. 287: 645-656.
10. Erpel, T., Superti-Furga, G., and Courtneidge, S.A. 1995. Mutational analysis of the Src SH3 domain: The same residues of the ligand binding surface are important for intra- and intermolecular interactions. EMBO J. 14: 963-975.
11. Gavin, A.C. and Superti-Furga, G. 2003. Protein complexes and proteome organization from yeast to man. Curr. Opin. Chem. Biol. 7: 21-27.
12. Gmeiner, W.H., Xu, I., Horita, D.A., Smithgall, T.E., Engen, J.R., Smith, D.L., and Byrd, R.A. 2001. Intramolecular binding of a proximal PPII helix to an SH3 domain in the fusion protein SH3Hck : PPIIhGAP. Cell Biochem. Biophys. 35: 115-126.
13. Gonfloni, S., Williams, J.C., Hattula, K., Weijland, A., Wierenga, R.K., and Superti-Furga, G. 1997. The role of the linker between the SH2 domain and catalytic domain in the regulation and function of Src. EMBO J. 16: 7261-7271.
14. Gonfloni, S., Frischknecht, F., Way, M., and Superti-Furga, G. 1999. Leucine 255 of Src couples intramolecular interactions to inhibitions of catalysis. Nat. Struct. Biol. 6: 760-764.
15. Hoofnagle, A.N., Resing, K.A., and Ahn, N.G. 2003. Protein analysis by hydrogen exchange mass spectrometry. Annu. Rev. Biophys. Biomol. Struct. 32: 1-25.
16. Kuriyan, J. and Cowburn, D. 1997. Modular peptide recognition domains in eukaryotic signaling. Annu. Rev. Biophys. Biomol. Struct. 26: 259-288.
17. Ladbury, J.E., Lemmon, M.A., Zhou, M., Green, J., Botfield, M.C., and Schlessinger, J. 1995. Measurement of the binding of tyrosyl phosphopeptides to SH2 domains: A reappraisal. Proc. Natl. Acad. Sci. 92: 3199-3203.
18. Lee, C.-H., Leung, B., Lemmon, M.A., Zheng, J., Cowburn, D., Kuriyan, J., and Saksela, K. 1995. A single amino acid in the SH3 domain of Hck determines its high affinity and specificity in binding to HIV-1 Nef protein. EMBO J. 14: 5006-5015.
19. Lerner, E.C. and Smithgall, T.E. 2002. SH3-dependent stimulation of Src-family kinase autophosphorylation without tail release from the SH2 domain in vivo. Nat. Struct. Biol. 9: 365-369.
20. Lerner, E.C., Trible, R.P., Schiavone, A.P., Hochrein, J.M., Engen, J.R., and Smithgall, T.E. 2005. Activation of the SRC-family kinase HCK without SH3-linker release. J. Biol. Chem. (in press).
21. Mandell, J.G., Baerga-Ortiz, A., Akashi, S., Takio, K., and Komives, E.A. 2001. Solvent accessibility of the thrombin-thrombomodulin interface. J. Mol. Biol. 306: 575-589.
22. Musacchio, A., Wilmanns, M., and Saraste, M. 1994. Structure and function of the SH3 domain. Prog. Biophys. Mol. Biol. 61: 283-297.
23. Pawson, T. 1992. SH2 and SH3 domains. Curr. Opin. Struct. Biol. 2: 432-437.
24. Pawson, T., Raina, M., and Nash, P. 2002. Interaction domains: From simple binding events to complex cellular behavior. FEBS Lett. 513: 2-10.
25. Pisabarro, M.T., Serrano, L., and Wilmanns,M. 1998. Crystal structure of the abl-SH3 domain complexed with a designed high-affinity peptide ligand: Implications for SH3-ligand interactions. J. Mol. Biol. 281: 513-521.
26. Redfield, C. 2004. Using nuclear magnetic resonance spectroscopy to study molten globule states of proteins. Methods 34: 121-132.
27. Schaffhausen, B. 1995. SH2 domain structure and function. Biochim. Biophys. Acta 1242: 61-75.
28. Schindler, T., Sicheri, F., Pico, A., Gazit, A., Levitzki, A., and Kuriyan, J. 1999. Crystal structure of Hck in complex with a Src family-selective tyrosine kinase inhibitor. Mol. Cell 3: 639-648.
29. Sicheri, F., Moarefi, I., and Kuriyan, J. 1997. Crystal structure of the Src family tyrosine kinase Hck. Nature 385: 602-609.
30. Songyang, Z., Shoelson, S.E., Chaudhuri, M., Gish, G., Pawson, T., Haser, W.G., King, F., Roberts, T., Ratnofsky, S., and Lechleider, R.J. 1993. SH2 domains recognize specific phosphopeptide sequences. Cell 72: 767-778.
31. Superti-Furga, G., Fumagalli, S., Koegl, M., Courtneidge, S.A., and Draetta, G. 1993. Csk inhibition of c-Src activity requires both the SH2 and SH3 domains of Src. EMBO J. 12: 2625-2634.
32. Tessari, M., Gentile, L.N., Taylor, S.J., Shalloway, D.I., Nicholson, L.K., and Vuister, G.W. 1997. Heteronuclear NMR studies of the combined Src homology domains 2 and 3 of pp60 c-Src: Effects of phosphopeptide binding. Biochemistry 37: 14561-14571.
33. Wong, L., Lieser, S.A., Miyashita, O., Miller, M., Tasken, K., Onuchic, J.N., Adams, J.A., Woods Jr., V.L., and Jennings, P.A. 2005. Coupled motions in the SH2 and kinase domains of Csk control Src phosphorylation. J. Mol. Biol. 351: 131-143.
34. Xu, W., Harrison, S.C., and Eck, M.J. 1997. Three-dimensional structure of the tyrosine kinase c-Src. Nature 385: 595-602.
35. Xu, W., Doshi, A., Lei, M., Eck, M.J., and Harrison, S.C. 1999. Crystal structures of c-Src reveal features of its autoinhibitory mechanism. Mol. Cell 3: 629-638.
36. Yan, X., Watson, J., Ho, P.S., and Deinzer, M.L. 2004. Mass spectrometric approaches using electrospray ionization charge states and hydrogen-deuterium exchange for determining protein structures and their conformational changes. Mol. Cell. Proteomics 3: 10-23.
37. Young, M.A., Gonfloni, S., Superti-Furga, G., Roux, B., and Kuriyan, J. 2001. Dynamic coupling between the SH2 and SH3 domains of c-Src and Hck underlies their inactivation by C-terminal tyrosine phosphorylation. Cell 105: 115-126.
38. Zhang, Z. and Smith, D.L. 1993. Determination of amide hydrogen exchange by mass spectrometry: A new tool for protein structure elucidation. Protein Sci. 2: 522-531.