Remote changes in the dynamics of the phosphotyrosine-binding domain of insulin receptor substrate-1 induced by phosphopeptide binding

Biochemistry

Volumn 47, Issue 50, 2008, Pages 13371-13382

  Jarymowycz, Virginia A ^a   Stone, Martin J ^b  

^a INDIANA UNIVERSITY   (United States)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE NETWORKS; AMIDES; AMINES; AMINO ACIDS; BINDING ENERGY; DYNAMICS; FLOW INTERACTIONS; HORMONES; HYDROCARBONS; INSULIN; NUCLEAR MAGNETIC RESONANCE;

AMIDE GROUPS; BINDING DOMAINS; COOPERATIVE NETWORKS; INSULIN RECEPTORS; INTERACTION NETWORKS; METHYL GROUPS; NMR RELAXATIONS; PEPTIDE BINDINGS; PHOSPHOPEPTIDE; PROTEIN STRUCTURES; SIDE CHAINS; SUBSTANTIAL DISTANCES; TRYPTOPHAN SIDE CHAINS;

BINDING SITES;

AMIDE; INSULIN RECEPTOR SUBSTRATE 1; PHOSPHOPEPTIDE; PHOSPHOTYROSINE; TRYPTOPHAN;

ARTICLE; BINDING SITE; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

BINDING SITES; CELLS, CULTURED; CRYSTALLOGRAPHY, X-RAY; HUMANS; INSULIN RECEPTOR SUBSTRATE PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHOPEPTIDES; PHOSPHOTYROSINE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS;

EID: 57649129011     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801096b     Document Type: Article

References (49)

1. Rajagopalan, P. T., Lutz, S., and Benkovic, S. J. (2002) Coupling interactions of distal residues enhance dihydrofolate reductase catalysis: Mutational effects on hydride transfer rates. Biochemistry 41, 12618-12628.
2. Liebeton, K., Zonta, A., Schimossek, K., Nardini, M., Lang, D., Dijkstra, B. W., Reetz, M. T., and Jaeger, K. E. (2000) Directed evolution of an enantioselective lipase. Chem. Biol. 7, 709-718.
3. Gregoret, L. M., and Sauer, R. T. (1993) Additivity of mutant effects assessed by binomial mutagenesis. Proc. Natl. Acad. Sci. U.S.A. 90, 4246-4250.
4. Green, S. M., and Shortle, D. (1993) Patterns of nonadditivity between pairs of stability mutations in staphylococcal nuclease. Biochemistry 32, 10131-10139.
5. Istomin, A. Y., Gromiha, M. M., Vorov, O. K., Jacobs, D. J., and Livesay, D. R. (2008) New insight into long-range nonadditivity within protein double-mutant cycles. Proteins 70, 915-924.
6. Rod, T. H., Radkiewicz, J. L., and Brooks, C. L., III (2003) Correlated motion and the effect of distal mutations in dihydrofolate reductase. Proc. Natl. Acad. Sci. U.S.A. 100, 6980-6985.
7. Lockless, S. W., and Ranganathan, R. (1999) Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286, 295-299.
8. Socolich, M., Lockless, S. W., Russ, W. P., Lee, H., Gardner, K. H., and Ranganathan, R. (2005) Evolutionary information for specifying a protein fold. Nature 437, 512-518.
9. Russ, W. P., Lowery, D. M., Mishra, P., Yaffe, M. B., and Ranganathan, R. (2005) Natural-like function in artificial WW domains. Nature 437, 579-583.
10. Fuentes, E. J., Der, C. J., and Lee, A. L. (2004) Ligand-dependent dynamics and intramolecular signaling in a PDZ domain. J. Mol. Biol. 335, 1105-1115.
11. Clarkson, M. W., and Lee, A. L. (2004) Long-range dynamic effects of point mutations propagate through side chains in the serine protease inhibitor eglin c. Biochemistry 43, 12448-12458.
12. Clarkson, M. W., Gilmore, S. A., Edged, M. H., and Lee, A. L. (2006) Dynamic coupling and allosteric behavior in a nonallosteric protein. Biochemistry 45, 7693-7699.
13. White, M. F. (1994) The IRS-1 signaling system. Curr. Opin. Genet. Dev. 4, 47-54.
14. White, M. F. (2003) IRS-Protein Scaffolds and Insulin/IGF Action. In Handbook of Cell Signaling, pp 409-419, Academic Press, New York.
15. Uhlik, M. T., Temple, B., Bencharit, S., Kimple, A. J., Siderovski, D. P., and Johnson, G. L. (2005) Structural and evolutionary division of phosphotyrosine binding (PTB) domains. J. Mol. Biol. 345, 1-20.
16. Takeuchi, H., Matsuda, M., Yamamoto, T., Kanematsu, T., Kikkawa, U., Yagisawa, H., Watanabe, Y., and Hirata, M. (1998) PTB domain of insulin receptor substrate-1 binds inositol compounds. Biochem. J. 334 (Part 1), 211-218.
17. Dhe-Paganon, S., Ottinger, E. A., Nolte, R. T., Eck, M. J., and Shoelson, S. E. (1999) Crystal structure of the pleckstrin homology-phosphotyrosine binding (PH-PTB) targeting region of insulin receptor substrate 1. Proc. Natl. Acad. Sci. U.S.A. 96, 8378-8383.
18. Eck, M. J., DhePaganon, S., Trub, T., Nolte, R. T., and Shoelson, S. E. (1996) Structure of the IRS-1 PTB domain bound to the juxtamembrane region of the insulin receptor. Cell 85, 695-705.
19. Olejniczak, E. T., Zhou, M. M., and Fesik, S. W. (1997) Changes in the NMR-derived motional parameters of the insulin receptor substrate 1 phosphotyrosine binding domain upon binding to an interleukin 4 receptor phosphopeptide. Biochemistry 36, 4118-4124.
20. Zhou, M. M., Huang, B. H., Olejniczak, E. T., Meadows, R. P., Shuker, S. B., Miyazaki, M., Trub, T., Shoelson, S. E., and Fesik, S. W. (1996) Structural basis for IL-4 receptor phosphopeptide recognition by the IRS-1 PTB domain. Nat. Struct. Biol. 3, 388-393.
21. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M. R., Appel, R. D., and Bairoch, A. (2005) Protein Identification and Analysis Tools on the ExPasy Server. In The Proteomics Protocols Handbook (Walker, J. M., Ed.) pp 571-607, Humana Press, Totowa, NJ.
22. 13C labeling. Biochemistry 28, 7510-7516.
23. Grzesiek, S., and Bax, A. (1992) Correlating Backbone Amide and Side-Chain Resonances in Larger Proteins by Multiple Relayed Triple Resonance Nmr. J. Am. Chem. Soc. 114, 6291-6293.
24. Wittekind, M., and Mueller, L. (1993) Hncacb, A High-Sensitivity 3D Nmr Experiment to Correlate Amide-Proton and Nitrogen Resonances with the α-Carbon and β-Carbon Resonances in Proteins. J. Magn. Reson., Ser. B 101, 201-205.
25. Muhandiram, D. R., and Kay, L. E. (1994) Gradient-Enhanced Triple-Resonance 3-Dimensional Nmr Experiments with Improved Sensitivity. J. Magn. Reson., Ser.B 103, 203-216.
26. 15N resonance assignments of the N-terminal Sh3 domain of Drk in folded and unfolded states using enhanced-sensitivity pulsed-field gradient NMR techniques. J. Biomol. NMR 4, 845-858.
27. 13C isotropic mixing for determining sequence-specific resonance assignments of isotopically-enriched proteins. J. Am. Chem. Soc. 114, 10974-10975.
28. 13C magnetization. J. Magn. Reson., Ser. B 101, 114-119.
29. Bax, A., Clore, G. M., and Gronenborn, A. M. (1990) H-1-H-1 Correlation Via Isotropic Mixing of C-13 Magnetization, A New 3-Dimensional Approach for Assigning H-1 and C-13 Spectra of C-13-Enriched Proteins. J. Magn. Reson. 88, 425-431.
30. Bax, A., Delaglio, F., Grzesiek, S., and Vuister, G. W. (1994) Resonance assignment of methionine methyl groups and chi 3 angular information from long-range proton-carbon and carbon-carbon J correlation in a calmodulin-peptide complex. J. Biomol. NMR 4, 787-797.
31. 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease. Biochemistry 28, 8972-8979.
32. 15N NMR relaxation. Biochemistry 33, 5984-6003.
33. 15N chemical shift anisotropy relaxation interference: Unambiguous determination of rotational diffusion tensors and chemical exchange effects in biological macromolecules. J. Am. Chem. Soc. 120, 7905-7915.
34. 2H-labeled proteins in solution. J. Am. Chem. Soc. 117, 11536-11544.
35. Seewald, M. J., Pichumani, K., Stowell, C., Tibbals, B. V., Regan, L., and Stone, M. J. (2000) The role of backbone conformational heat capacity in protein stability: Temperature dependent dynamics of the B1 domain of Streptococcal protein G. Protein Sci. 9, 1177-1193.
36. 15N chemical shift anisotropy from NMR relaxation data. Ubiquitin as a test example. J. Am. Chem. Soc. 120, 7109-7110.
37. Bruschweiler, R., Liao, X. B., and Wright, P. E. (1995) Long-range motional restrictions in a multidomain zinc-finger protein from anisotropic tumbling. Science 268, 886-889.
38. Lipari, G., and Szabo, A. (1982) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104, 4546-4559.
39. Lipari, G., and Szabo, A. (1982) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104, 4559-4570.
40. 1H NMR spectroscopy. Biochemistry 29, 7387-7401.
41. 15N nuclear magnetic-relaxation of proteins. J. Am. Chem. Soc. 112, 4989-4991.
42. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: The central helix is flexible. Biochemistry 31, 5269-5278.
43. Mandel, A. M., Akke, M., and Palmer, A. G., III (1995) Backbone dynamics of Escherichia coli ribonuclease HI: Correlations with structure and function in an active enzyme. J. Mol. Biol. 246, 144-163.
44. Stone, M. J., Chandrasekhar, K., Holmgren, A., Wright, P. E., and Dyson, H. J. (1993) Comparison of Backbone and Tryptophan Side-Chain Dynamics of Reduced and Oxidized Escherichia coli Thioredoxin Using N-15 Nmr Relaxation Measurements. Biochemistry 32, 426-435.
45. 2H-enriched proteins in solution. J. Am. Chem. Soc. 124, 6439-6448.
46. 2H quadrupolar couplings in oriented proteins. How uniform is the quadrupolar coupling constant? J. Am. Chem. Soc. 121, 10608-10613.
47. Moore, D. S., and McCabe, G. P. (2004) Introduction to the Practice of Statistics, W. H. Freeman and Company, New York.
48. Mayer, K. L., Earley, M. R., Gupta, S., Pichumani, K., Regan, L., and Stone, M. J. (2003) Covariation of backbone motion throughout a small protein domain. Nat. Struct. Biol. 10, 962-965.
49. Goehlert, V. A., Krupinska, E., Regan, L., and Stone, M. J. (2004) Analysis of side chain mobility among protein G B1 domain mutants with widely varying stabilities. Protein Sci. 13, 3322-3330.