Phosphorylation-Dependent Changes in Structure and Dynamics in ERK2 Detected by SDSL and EPR

Biophysical Journal

Volumn 86, Issue 1 I, 2004, Pages 395-403

  Hoofnagle, Andrew N ^a,b   Stoner, James W ^c   Lee, Thomas ^b   Eaton, Sandra S ^c   Ahn, Natalie G ^b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF DENVER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1;

ANISOTROPY; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DIFFUSION; ELECTRON SPIN RESONANCE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME REGULATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTON TRANSPORT; REPRODUCIBILITY; SITE DIRECTED SPIN LABELING; STRUCTURE ANALYSIS;

EID: 0346688715     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(04)74115-6     Document Type: Article

References (46)

1. Alonso, A., W. P. dos Santos, S. J. Leonor, J. G. dos Santos, and M. Tabak. 2001. Stratum comeum protein dynamics as evaluated by a spin-label maleimide derivative: Effect of urea. Biophys. J. 81:3566-3576.
2. Amin, S. S., K. Cryer, B. Y. Zhang, S. K. Dutta, S. S. Eaton, O. P. Anderson, S. M. Miller, B. A. Reul, S. M. Brichard, and D. C. Crans. 2000. Chemistry and insulin-mimetic properties of bis(acetylacetonate)oxovanadium(IV) and derivatives. Inorg. Chem. 39:406-416.
3. Anand, G. S., C. A. Hughes, J. M. Jones, S. S. Taylor, and E. A. Komives. 2002. Amide H/H-2 exchange reveals communication between the cAMP and catalytic subunit-binding sites in the R-I alpha subunit of protein kinase A. J. Mol. Biol. 323:377-386.
4. Barnakov, A., C. Altenbach, L. Barnakova, W. L. Hubbell, and G. L. Hazelbauer. 2002. Site-directed spin labeling of a bacterial chemoreceptor reveals a dynamic, loosely packed transmembrane domain. Protein Sci. 11:1472-1481.
5. Bames, J. P., Z. C. Liang, H. S. McHaourab, J. H. Freed, and W. L. Hubbell. 1999. A multifrequency electron spin resonance study of T4 lysozyme dynamics. Biophys. J. 76:3298-3306.
6. Budil, D. E., S. Lee, S. Saxena, and J. H. Freed. 1996. Nonlinear-least-squares analysis of slow-motion EPR spectra in one and two dimensions using a modified Levenberg-Marquardt algorithm. J. Magn. Reson. 120:155-189.
7. Canagarajah, B. J., A. Khokhlatchev, M. H. Cobb, and E. J. Goldsmith. 1997. Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell. 90:859-869.
8. Columbus, L., and W. L. Hubbell. 2002. A new spin on protein dynamics. Trends Biochem. Sci. 27:288-295.
9. Columbus, L., T. Kalai, J. Jeko, K. Hideg, and W. L. Hubbell. 2001. Molecular motion of spin labeled side chains in alpha-helices: analysis by variation of side chain structure. Biochemistry. 40:3828-3846.
10. Cox, S., E. Radzio-Andzelm, and S. S. Taylor. 1994. Domain movements in protein kinases. Curr. Opin. Struct. Biol. 4:893-901.
11. Earle, K. A., D. E. Budil, and J. H. Freed. 1993. 250-GHz EPR of nitroxides in the slow-motional regime: models of rotational diffusion. J. Phys. Chem. 97:13289-13297.
12. Emrick, M. A., A. N. Hoofnagle, A. S. Miller, L. F. Ten Eyck, and N. G. Ahn. 2001. Constitutive activation of extracellular signal-regulated kinase 2 by synergistic point mutations. J. Biol. Chem. 276:46469-46479.
13. Fox, T., J. T. Coll. X. L. Xie, P. J. Ford, U. A. Germann, M. D. Porter, S. Pazhanisamy, M. A. Fleming, V. Galullo, M. S. S. Su, and K. P. Wilson. 1998. A single amino acid substitution makes ERK2 susceptible to pyridinyl imidazole inhibitors of p38 MAP kinase. Protein Sci. 7:2249-2255.
14. Glasgow, B. J., O. K. Gasymov, A. R. Abduragimov, T. N. Yusifov, C. Altenbach, and W. L. Hubbell. 1999. Side chain mobility and ligand interactions of the G strand of tear lipocalins by site-directed spin labeling. Biochemistry. 38:13707-13716.
15. Hoofnagle, A. N., K. A. Resing, and N. G. Ahn. 2003. Protein analysis by hydrogen exchange mass spectrometry. Annu. Rev. Biophys. Biomol. Struct. 32:1-25.
16. Hoofnagle, A. N., K. A. Resing, E. J. Goldsmith, and N. G. Ahn. 2001. Changes in protein conformational mobility upon activation of extracellular regulated protein kinase-2 as detected by hydrogen exchange. Proc. Natl. Acad. Sci. USA. 98:956-961.
17. Hu, S. H., M. W. Parker, J. Y. Lei, M. C. J. Wilce, G. M. Benian, and B. E. Kemp. 1994. Insights into autoregulation from the crystal-structure of twitchin kinase. Nature. 369:581-584.
18. Hubbell, W. L., D. S. Cafiso, and C. Altenbach. 2000. Identifying conformational changes with site-directed spin labeling. Nat. Struct. Biol. 7:735-739.
19. Hubbell, W. L., H. S. McHaourab, C. Altenbach, and M. A. Lietzow. 1996. Watching proteins move using site-directed spin labeling. Structure. 4:779-783.
20. Johnson, L. N., M. E. M. Noble, and D. J. Owen. 1996. Active and inactive protein kinases: structural basis for regulation. Cell. 85:149-158.
21. Khokhlatchev, A. V., B. Canagarajah, J. Wilsbacher, M. Robinson, M. Atkinson, E. Goldsmith, and M. H. Cobb. 1998. Phosphorylation of the MAP kinase ERK2 promotes its homodimerization and nuclear translocation. Cell. 93:605-615.
22. Knighton, D. R., J. H. Zheng, L. F. Teneyck, N. H. Xuong, S. S. Taylor, and J. M. Sowadski. 1991. Structure of a peptide inhibitor bound to the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science. 253:414-420.
23. Langen, R., K. J. Oh, D. Cascio, and W. L. Hubbell. 2000. Crystal structures of spin labeled T4 lysozyme mutants: implications for the interpretation of EPR spectra in terms of structure. Biochemistry. 39:8396-8405.
24. Li, F., M. Gangal, C. Juliano, E. Gorfain, S. S. Taylor, and D. A. Johnson. 2002. Evidence for an internal entropy contribution to phosphoryl transfer: a study of domain closure, backbone flexibility, and the catalytic cycle of cAMP-dependent protein kinase. J. Mol. Biol. 315:459-469.
25. Liu, Y. S., P. Sompompisut, and E. Perozo. 2001. Structure of the KcsA channel intracellular gate in the open state. Nat. Struct. Biol. 8:883-887.
26. Madhusudan, P. Akamine, N. H. Xuong, and S. S. Taylor. 2002. Crystal structure of a transition state mimic of the catalytic subunit of cAMP-dependent protein kinase. Nat. Struct. Biol. 9:273-277.
27. Mansour, S. J., J. M. Candia, J. E. Matsuura, M. C. Manning, and N. G. Ahn. 1996. Interdependent domains controlling the enzymatic activity of mitogen-activated protein kinase kinase 1. Biochemistry. 35:15529-15536.
28. Mchaourab, H. S., and E. Perozo. 2000. Determination of protein folds and conformational dynamics using spin-labeling EPR spectroscopy. Biol. Magn. Reson. 19:185-247.
29. Narayana, N., S. Cox, N. H. Xuong, L. F. TenEyck, and S. S. Taylor. 1997a. A binary complex of the catalytic subunit of cAMP-dependent protein kinase and adenosine further defines conformational flexibility. Structure. 5:921-935.
30. Narayana, N., S. Cox, S. Shaltiel, S. S. Taylor, and N. H. Xuong. 1997b. Crystal structure of a polyhistidine-tagged recombinant catalytic subunit of cAMP-dependent protein kinase complexed with the peptide inhibitor PKI(5-24) and adenosine. Biochemistry. 36:4438-4448.
31. Olah, G. A., R. D. Mitchell, T. R. Sosnick, D. A. Walsh, and J. Trewhella. 1993. Solution structure of the cAMP-dependent protein kinase catalytic subunit and its contraction upon binding the protein kinase inhibitor peptide. Biochemistry. 32:3649-3657.
32. Pearson, G., F. Robinson, T. B. Gibson, B. E. Xu, M. Karandikar, K. Berman, and M. H. Cobb. 2001. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22:153-183.
33. Prowse, C. N., and J. Lew. 2001. Mechanism of activation of ERK2 by dual phosphorylation. J. Biol. Chem. 276:99-103.
34. Quine, R. W., G. R. Eaton, and S. S. Eaton. 1986. Versatile computer interface for a Varian E9 EPR spectrometer. J. Magn. Reson. 66:164-167.
35. Resing, K. A., and N. G. Ahn. 1997. Protein phosphorylation analysis by electrospray ionization mass spectrometry. Methods Enzymol. 283:29-44.
36. Resing, K. A., and N. G. Ahn. 1998. Deuterium exchange mass spectrometry as a probe of protein kinase activation. Analysis of wild-type and constitutively active mutants of MAP kinase kinase-1. Biochemistry. 37:463-475.
37. Resing, K. A., A. N. Hoofnagle, and N. G. Ahn. 1999. Modeling deuterium exchange behavior of ERK2 using pepsin mapping to probe secondary structure. J. Am. Soc. Mass Spectrom. 10:685-702.
38. Robbins, D. J., E. Z. Zhen, H. Owaki, C. A. Vanderbilt, D. Ebert, T. D. Geppert, and M. H. Cobb. 1993. Regulation and properties of extracellular signal-regulated protein kinases 1 and 2 in vitro. J. Biol. Chem. 268:5097-5106.
39. Schneider, D. J., and J. H. Freed. 1989. Calculating slow motional magnetic resonance spectra. Biol. Magn. Reson. 8:1-76.
40. Toy, A. D., S. H. H. Chaston, J. R. Pilbrow, and T. D. Smith. 1971. Electron spin resonance study of copper(II) chelates of certain monothio-beta-diketones and diethyldithiocarbamate. Inorg. Chem. 10:2219-2225.
41. Tsigelny, I., J. P. Greenberg, S. Cox, W. L. Nichols, S. S. Taylor, and L. F. Ten Eyck. 1999. 600 ps molecular dynamics reveals stable substructures and flexible hinge points in cAMP dependent protein kinase. Biopolymers. 50:513-524.
42. Victor, K. G., and D. S. Cafiso. 2001. Location and dynamics of basic peptides at the membrane interface: electron paramagnetic resonance spectroscopy of tetramethyl-piperidine-N-oxyl-4-amino-4-carboxylic acid-labeled peptides. Biophys. J. 81:2241-2250.
43. Wand, A. J., M. R. Ehrhardt, and P. F. Flynn. 1998. High-resolution NMR of encapsulated proteins dissolved in low-viscosity fluids. Proc. Natl. Acad. Sci. USA. 95:15299-15302.
44. Wilson, K. P., M. J. Fitzgibbon, P. N. Caron, J. P. Griffith, W. Y. Chen, P. G. McCaffrey, S. P. Chambers, and M. S. S. Su. 1996. Crystal structure of p38 mitogen-activated protein kinase. J. Biol. Chem. 271:27696-27700.
45. Young, M. A., S. Gonfloni, G. Superti-Furga, B. Roux, and J. Kuriyan. 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.
46. Zhang, F. M., A. Strand, D. Robbins, M. H. Cobb, and E. J. Goldsmith. 1994. Atomic structure of the MAP kinase ERK2 at 2.3 A resolution. Nature. 367:704-711.