New insights into FAK signaling and localization based on detection of a FAT domain folding intermediate

Structure

Volumn 12, Issue 12, 2004, Pages 2161-2171

  Dixon, Richard D S ^a   Chen, Yiwen ^b   Ding, Feng ^a   Khare, Sagar D ^a   Prutzman, Kirk C ^a   Schaller, Michael D ^c   Campbell, Sharon L ^a,c   Dokholyan, Nikolay V ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b The University of North Carolina at Chapel Hill   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOCAL ADHESION KINASE; MITOGEN ACTIVATED PROTEIN KINASE; PAXILLIN;

ARTICLE; FOCAL ADHESION; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEIN TARGETING; SEPARATION TECHNIQUE;

FOCAL ADHESION PROTEIN-TYROSINE KINASES; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; TEMPERATURE;

EID: 9944258521     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2004.09.011     Document Type: Article

References (54)

1. Abe H., Gō N. Noninteracting local structure model of folding and unfolding transition in globular proteins. II. Formulation. Biopolymers. 20:1981;1013-1031
2. Arold S.T., Hoellerer M.K., Noble M.E.M. The structural basis of localization and signaling by the focal adhesion targeting domain. Structure. 10:2002;319-327
3. Bai Y., Milne J.S., Mayne L., Englander S.W. Primary structure effects on peptide group hydrogen exchange. Proteins. 17:1993;75-86
4. Bai Y., Milne J.S., Mayne L., Englander S.W. Protein stability parameters measured by hydrogen exchange. Proteins. 20:1994;4-14
5. Bai Y., Sosnick T.R., Mayne L., Englander S.W. Protein folding intermediates. native-state hydrogen exchange Science. 269:1995;192-197
6. Borreguero J.M., Dokholyan N.V., Buldyrev S.V., Stanley H.E., Shakhnovich E.I. Thermodynamics and folding kinetics analysis of the SH3 domain from discrete molecular dynamics. J. Mol. Biol. 318:2002;863-876
7. Brown N.R., Noble M.E.M., Endicott J.A., Johnson L.N. The structural basis for specificity of substrate and recruitment peptides for cyclin-dependent kinases. Nat. Cell Biol. 1:1999;438-443
8. Chamberlain A.K., Handel T.M., Marqusee S. Detection of rare partially folded molecules in equilibrium with the native conformation of RNaseH. Nat. Struct. Biol. 3:1996;782-787
9. Chen H.-C., Appeddu P.A., Parsons J.T., Hildebrand J.D., Schaller M.D., Guan J.-L. Interaction of focal adhesion kinase with cytoskeletal protein talin. J. Biol. Chem. 270:1995;16995
10. Clementi C., Garcia A., Onuchic J.N. Interplay among tertiary contacts, secondary structure information and side-chain packing in the protein folding mechanism. an all-atom representation study J. Mol. Biol. 326:2003;933-954
11. Cooley M.A., Broome J.M., Ohngemach C., Romer L.H., Schaller M.D. Paxillin binding is not the sole determinant of focal adhesion localization or dominant-negative activity of focal adhesion kinase/focal adhesion kinase-related nonkinase. Mol. Biol. Cell. 11:2000;3247-3263
12. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., Bax A. NMRPipe. a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR. 6:1995;277-293
13. Ding F., Borreguero J.M., Buldyrev S.V., Stanley H.E., Dokholyan N.V. A mechanism for the alpha-helix to beta-hairpin transition. Proteins. 53:2003;220-228
14. Ding F., Dokholyan N.V., Buldyrev S.V., Stanley H.E., Shakhnovich E.I. Direct molecular dynamics observation of protein folding transition state ensemble. Biophys. J. 83:2002;3525-3532. a
15. Ding F., Dokholyan N.V., Buldyrev S.V., Stanley H.E., Shakhnovich E.I. Molecular dynamics simulation of C-Src SH3 aggregation suggests a generic amyloidogenesis mechanism. J. Mol. Biol. 324:2002;851-857. b
16. Dokholyan N.V., Buldyrev S.V., Stanley H.E., Shakhnovich E.I. Molecular dynamics studies of folding of a protein-like model. Fold. Des. 3:1998;577-587
17. Fuentes E.J., Wand A.J. Local dynamics and stability of apocytochrome b562 examined by hydrogen exchange. Biochemistry. 37:1998;3687-3698
18. Gabarra-Niecko V., Schaller M.D., Dunty J.M. FAK regulates biological processes important for the pathogenesis of cancer. Cancer Metastasis Rev. 22:2003;359-374
19. Gao G., Prutzman K.C., King M.L., Scheswohl D.M., DeRose E.F., London R.E., Schaller M.D., Campbell S.L. NMR solution structure of the focal adhesion targeting domain of focal adhesion kinase in complex with a Paxillin LD peptide. evidence for a two site binding model J. Biol. Chem. 279:2004;8441-8451
20. Gō N., Abe H. Noninteracting local structure model of folding and unfolding transition in globular proteins. I. Formulation. Biopolymers. 20:1981;991-1011
21. Hayashi I., Vuori K., Liddington R.C. The focal adhesion targeting (FAT) region of focal adhesion kinase is a four-helix bundle that binds paxillin. Nat. Struct. Biol. 9:2002;101-106
22. Hildebrand J., Schaller M., Parsons J. Paxillin, a tyrosine phosphorylated focal adhesion-associated protein binds to the carboxyl terminal domain of focal adhesion kinase. Mol. Biol. Cell. 6:1995;637-647
23. Hildebrand J.D., Schaller M.D., Parsons J.T. Identification of sequences required for the efficient localization of the focal adhesion kinase, pp125FAK, to cellular focal adhesions. J. Cell Biol. 123:1993;993
24. Hoellerer M.K., Noble M.E.M., Labesse G., Campbell I.D., Werner J.M., Arold S.T. Molecular recognition of paxillin LD motifs by the focal adhesion targeting domain. Structure. 11:2003;1207-1217
25. Hubbard S.R. Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analog. EMBO J. 16:1997;5572-5581
26. Hwang T.-L., Mori S., van Zijl P.C.M. Application of Phase-Modulated CLEAN chemical EXchange spectroscopy (CLEANEX-PM) to detect water-protein proton exchange and intermolecular NOEs. J. Am. Chem. Soc. 119:1997;6203-6204
27. Hwang T.-L., van Zijl P.C.M., Mori S. Accurate quantitation of water-amide proton exchange rates using the Phase-Modulated CLEAN chemical EXchange (CLEANEX-PM) approach with a Fast-HSQC (FHSQC) detection scheme. J. Biomol. NMR. 11:1998;221-226
28. Johnson B., Blevins R.A. NMRView. a computer program for the visualization and analysis of NMR data J. Biomol. NMR. 4:1994;603-614
29. Karanicolas J., Brooks C.L. III. The origins of asymmetry in the folding transition states of protein L and protein G. Protein Sci. 11:2002;2351-2361
30. Karplus, M., and Shakhnovich, E.I. (1994). Protein folding: theoretical studies of thermodynamics and dynamics. In Protein Folding, T. Creighton, ed. (New York, W.H. Freeman & Company), pp. 127-196.
31. Katz B.-Z., Romer L., Miyamoto S., Volberg T., Matsumoto K., Cukierman E., Gieger B., Yamada K.M. Targeting membrane-localized FAK to focal adhesions. roles of tyrosine phosphorylation and Src family kinases J. Biol. Chem. 278:2003;29115-29120
32. Khare S.D., Ding F., Dokholyan N.V. Folding of Cu, Zn superoxide dismutase and familial amyotrophic lateral sclerosis. J. Mol. Biol. 334:2003;515-525
33. Kuriyan J., Cowburn D. Modular peptide recognition domains in eukaryotic signaling. Annu. Rev. Biophys. Biomol. Struct. 26:1997;259-288
34. Liu G., Guibao C.D., Zheng J. Structural insight into the mechanisms of targeting and signaling of focal adhesion kinase. Mol. Cell. Biol. 22:2002;2751-2760
35. Maity H., Lim W.K., Rumbley J.N., Englander S.W. Protein hydrogen exchange mechanism. local fluctuations Protein Sci. 12:2003;153-160
36. Mayne L., Englander S.W. Two-state vs. multistate protein unfolding studied by optical melting and hydrogen exchange. Protein Sci. 9:2000;1873-1877
37. Milne J.S., Mayne L., Roder H., Wand A.J., Englander S.W. Determinants of protein hydrogen exchange studied in equine cytochrome c. Protein Sci. 7:1998;739-745
38. Parsons J.T. Focal adhesion kinase. the first ten years J. Cell Sci. 116:2003;1409-1416
39. Perrett S., Clarke J., Hounslow A.M., Fersht A.R. Relationship between equilibrium amide proton exchange behavior and the folding pathway of barnase. Biochemistry. 34:1995;9288-9298
40. Prutzman K.C., Gao G., King M.L., Iyer V.V., Mueller G.A., Schaller M.D., Campbell S.L. The focal adhesion targeting domain of focal adhesion kinase contains a hinge region that modulates tyrosine 926 phosphorylation. Structure. 12:2004;881-891
41. Rahuel J., Gay B., Erdmann D., Strauss A., Garcia-Echeverria C., Furet P., Caravatti G., Fretz H., Schoepfer J., Grutter M. Structural basis for specificity of Grb2-SH2 revealed by a novel ligand binding mode. Nat. Struct. Biol. 3:1996;586-589
42. Santoro M.M., Bolen D.W. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl a-chymotrypsin using different denaturants. Biochemistry. 27:1988;8063-8068
43. Schaller M.D. Biochemical signals and biological responses elicited by the focal adhesion kinase. Biochim. Biophys. Acta. 1540:2001;1-21
44. Schlaepfer D.D., Hunter T. Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases. Mol. Cell. Biol. 16:1996;5623-5633
45. Schlaepfer D.D., Hunter T. Focal adhesion kinase overexpression enhances ras-dependent integrin signaling to ERK2/ mitogen-activated protein kinase through interactions with and activation of c-Src. J. Biol. Chem. 272:1997;13189-13195
46. Shen Y., Schaller M.D. Focal adhesion targeting. the critical determinant of FAK regulation and substrate phosphorylation Mol. Biol. Cell. 10:1999;2507-2518
47. Smith A.V., Hall C.K. Protein refolding versus protein aggregation. computer simulations on an intermediate-resolution protein model J. Mol. Biol. 312:2001;187-202
48. Smith S.W., Hall C.K., Freeman B.D. Molecular dynamics for polymeric fluids using discontinuous potentials. J. Comput. Phys. 134:1997;917-951
49. Tachibana K., Sato T., D'Avirro N., Morimoto C. Direct association of pp125FAK with paxillin, the focal adhesion-targeting mechanism of pp125FAK. J. Exp. Med. 182:1995;1089-1099
50. Thomas J.W., Cooley M.A., Broome J.M., Salgia R., Griffin J.D., Lombardo C.R., Schaller M.D. The role of focal adhesion kinase binding in the regulation of tyrosine phosphorylation of paxillin. J. Biol. Chem. 274:1999;36684-36692
51. Vendruscolo M., Paci E., Dobson C.M., Karplus M. Rare fluctuations of native proteins sampled by equilibrium hydrogen exchange. J. Am. Chem. Soc. 125:2003;15686-15687
52. Zhou Y., Karplus M. Folding of a model three-helix bundle protein. a thermodynamic and kinetic analysis J. Mol. Biol. 293:1999;917-951. a
53. Zhou Y., Karplus M. Interpreting the folding kinetics of helical proteins. Nature. 401:1999;400-403. b
54. Zhou Y., Karplus M., Wichert J.M., Hall C.K. Equilibrium thermodynamics of homopolymers and clusters. molecular dynamics and Monte Carlo simulations of system with square-well interactions J. Chem. Phys. 107:1997;10691-10708