Phosphorylation releases constraints to domain motion in ERK2

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 7, 2014, Pages 2506-2511

  Xiao, Yao ^a   Lee, Thomas ^a   Latham, Michael Parker ^a,b   Warner, Lisa Rose ^a,c   Tanimoto, Akiko ^a,d   Pardi, Arthur ^a   Ahn, Natalie G ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ENZYME ACTIVATION; ESCHERICHIA COLI; MAGNETIC RESONANCE SPECTROSCOPY; MITOGEN-ACTIVATED PROTEIN KINASE 1; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; RATS;

EID: 84894379546     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1318899111     Document Type: Article

References (39)

1. Roskoski R, Jr. (2012) ERK1/2 MAP kinases: Structure, function, and regulation. Pharmacol Res 66(2):105-143.
2. Pearson G, et al. (2001) Mitogen-activated protein (MAP) kinase pathways: Regulation and physiological functions. Endocr Rev 22(2):153-183.
3. Prowse CN, Lew J (2001) Mechanism of activation of ERK2 by dual phosphorylation. J Biol Chem 276(1):99-103.
4. Canagarajah BJ, Khokhlatchev A, Cobb MH, Goldsmith EJ (1997) Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell 90(5):859-869.
5. Zhang F, Strand A, Robbins D, Cobb MH, Goldsmith EJ (1994) Atomic structure of the MAP kinase ERK2 at 2.3 Å resolution. Nature 367(6465):704-711.
6. Lee T, et al. (2004) Docking motif interactions in MAP kinases revealed by hydrogen exchange mass spectrometry. Mol Cell 14(1):43-55.
7. Lee T, Hoofnagle AN, Resing KA, Ahn NG (2005) Hydrogen exchange solvent protection by an ATP analogue reveals conformational changes in ERK2 upon activation. J Mol Biol 353(3):600-612.
8. Hoofnagle AN, Stoner JW, Lee T, Eaton SS, Ahn NG (2004) Phosphorylation-dependent changes in structure and dynamics in ERK2 detected by SDSL and EPR. Biophys J 86(1 Pt 1):395-403.
9. Hoofnagle AN, Resing KA, Goldsmith EJ, Ahn NG (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(3):956-961.
10. Smock RG, Gierasch LM (2009) Sending signals dynamically. Science 324(5924):198-203.
11. Nagar B, et al. (2003) Structural basis for the autoinhibition of c-Abl tyrosine kinase. Cell 112(6):859-871.
12. Baldwin AJ, Kay LE (2009) NMR spectroscopy brings invisible protein states into focus. Nat Chem Biol 5(11):808-814.
13. Mittermaier AK, Kay LE (2009) Observing biological dynamics at atomic resolution using NMR. Trends Biochem Sci 34(12):601-611.
14. Bhabha G, et al. (2011) A dynamic knockout reveals that conformational fluctuations influence the chemical step of enzyme catalysis. Science 332(6026):234-238.
15. Eisenmesser EZ, et al. (2005) Intrinsic dynamics of an enzyme underlies catalysis. Nature 438(7064):117-121.
16. Fraser JS, et al. (2009) Hidden alternative structures of proline isomerase essential for catalysis. Nature 462(7273):669-673.
17. Korzhnev DM, Kloiber K, Kanelis V, Tugarinov V, Kay LE (2004) Probing slow dynamics in high molecular weight proteins by methyl-TROSY NMR spectroscopy: Application to a 723-residue enzyme. J Am Chem Soc 126(12):3964-3973.
18. Korzhnev DM, Kloiber K, Kay LE (2004) Multiple-quantum relaxation dispersion NMR spectroscopy probing millisecond time-scale dynamics in proteins: Theory and application. J Am Chem Soc 126(23):7320-7329.
19. Gardner KH, Kay LE (1997) Production and incorporation of N-15, C-13, H-2 (H-1-delta 1 methyl) isoleucine into proteins for multidimensional NMR studies. J Am Chem Soc 119(32):7599-7600.
20. Goto NK, Gardner KH, Mueller GA, Willis RC, Kay LE (1999) A robust and cost-effective method for the production of Val, Leu, Ile (delta 1) methyl-protonated 15N-, 13C-, 2Hlabeled proteins. J Biomol NMR 13(4):369-374.
21. Shapiro PS, et al. (1998) Activation of the MKK/ERK pathway during somatic cell mitosis: Direct interactions of active ERK with kinetochores and regulation of the mitotic 3F3/2 phosphoantigen. J Cell Biol 142(6):1533-1545.
22. Tugarinov V, Kay LE (2003) Ile, Leu, and Val methyl assignments of the 723-residue malate synthase G using a new labeling strategy and novel NMR methods. J Am Chem Soc 125(45):13868-13878.
23. Sinha N, Kumar S, Nussinov R (2001) Interdomain interactions in hinge-bending transitions. Structure 9(12):1165-1181.
24. Johnson DA, Akamine P, Radzio-Andzelm E, Madhusudan M, Taylor SS (2001) Dynamics of cAMP-dependent protein kinase. Chem Rev 101(8):2243-2270.
25. Robbins DJ, et al. (1993) Regulation and properties of extracellular signal-regulated protein kinases 1 and 2 in vitro. J Biol Chem 268(7):5097-5106.
26. Akamine P, et al. (2003) Dynamic features of cAMP-dependent protein kinase revealed by apoenzyme crystal structure. J Mol Biol 327(1):159-171.
27. Masterson LR, et al. (2011) Dynamically committed, uncommitted, and quenched states encoded in protein kinase A revealed by NMR spectroscopy. Proc Natl Acad Sci USA 108(17):6969-6974.
28. Masterson LR, et al. (2010) Dynamics connect substrate recognition to catalysis in protein kinase A. Nat Chem Biol 6(11):821-828.
29. Chen H, et al. (2007) A molecular brake in the kinase hinge region regulates the activity of receptor tyrosine kinases. Mol Cell 27(5):717-730.
30. Deindl S, et al. (2007) Structural basis for the inhibition of tyrosine kinase activity of ZAP-70. Cell 129(4):735-746.
31. Shan Y, et al. (2012) Oncogenic mutations counteract intrinsic disorder in the EGFR kinase and promote receptor dimerization. Cell 149(4):860-870.
32. Shan Y, Arkhipov A, Kim ET, Pan AC, Shaw DE (2013) Transitions to catalytically inactive conformations in EGFR kinase. Proc Natl Acad Sci USA 110(18):7270-7275.
33. Kornev AP, Haste NM, Taylor SS, Eyck LF (2006) Surface comparison of active and inactive protein kinases identifies a conserved activation mechanism. Proc Natl Acad Sci USA 103(47):17783-17788.
34. Taylor SS, Kornev AP (2011) Protein kinases: Evolution of dynamic regulatory proteins. Trends Biochem Sci 36(2):65-77.
35. Francis DM, et al. (2011) Resting and active states of the ERK2:HePTP complex. J Am Chem Soc 133(43):17138-17141.
36. Emrick MA, et al. (2006) The gatekeeper residue controls autoactivation of ERK2 via a pathway of intramolecular connectivity. Proc Natl Acad Sci USA 103(48):18101-18106.
37. Palmer AG III (2004) NMR characterization of the dynamics of biomacromolecules. Chem Rev 104(8):3623-3640.
38. Vranken WF, et al. (2005) The CCPN data model for NMR spectroscopy: Development of a software pipeline. Proteins 59(4):687-696.
39. Skrynnikov NR, Mulder FA, Hon B, Dahlquist FW, Kay LE (2001) Probing slow time scale dynamics at methyl-containing side chains in proteins by relaxation dispersion NMR measurements: Application to methionine residues in a cavity mutant of T4 lysozyme. J Am Chem Soc 123(19):4556-4566.