Hydrogen-Exchange Mass Spectrometry Reveals Activation-Induced Changes in the Conformational Mobility of p38α MAP Kinase

Journal of Molecular Biology

Volumn 379, Issue 5, 2008, Pages 1075-1093

  Sours, Kevin M ^a   Kwok, Stan C ^b   Rachidi, Thami ^a   Lee, Thomas ^a   Ring, Adam ^a   Hoofnagle, Andrew N ^a   Resing, Katheryn A ^a   Ahn, Natalie G ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

conformational mobility; hydrogen exchange; MAP kinase; mass spectrometry; p38

Indexed keywords

AMIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 14;

ARTICLE; DIMERIZATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HYDROGEN EXCHANGE MASS SPECTROMETRY; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; ULTRACENTRIFUGATION;

EID: 44349104122     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.04.044     Document Type: Article

References (45)

1. Lee J.C., Kumar S., Griswold D.E., Underwood D.C., Votta B.J., and Adams J.L. Inhibition of p38 MAP kinase as a therapeutic strategy. Immunopharmacology 47 (2000) 185-201
2. Johnson D.A., Akamine P., Radzio-Andzelm E., Madhusudan M., and Taylor S.S. Dynamics of cAMP-dependent protein kinase. Chem. Rev. 101 (2001) 2243-2270
3. Zhang F., Strand A., Robbins D., Cobb M.H., and Goldsmith E.J. Atomic structure of the MAP kinase ERK2 at 2.3 A resolution. Nature 367 (1994) 704-711
4. Canagarajah B.J., Khokhlatchev A., Cobb M.H., and Goldsmith E.J. Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell 90 (1997) 859-869
5. Lee T., Hoofnagle A.H., Kabuyama Y., Stroud J., Min X., Goldsmith E.J., et al. Docking motif interactions in MAP kinases revealed by hydrogen exchange mass spectrometry. Mol. Cell 14 (2004) 43-55
6. Resing K., and Ahn N.G. 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 (1998) 463-475
7. Hoofnagle A.N., Resing K.A., and Ahn N.G. Changes in protein conformational mobility upon activation of extracelluar regulated protein kinase-2 as detected by hydrogen exchange. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 956-961
8. Hoofnagle A.H., Resing K.A., and Ahn N.G. Protein analysis by hydrogen exchange mass spectrometry. Annu. Rev. Biophys. Biomol. Struct. 32 (2003) 1-25
9. Busenlehner L.S., and Armstrong R.N. Insights into enzyme structure and dynamics elucidated by amide H/D exchange mass spectrometry. Arch. Biochem. Biophys. 433 (2005) 34-46
10. Hamuro Y., Zawadzki K.M., Kim J.S., Stranz D.D., Taylor S.S., and Woods V.L. Dynamics of cAPK type IIbeta activation revealed by enhanced amide H/2H exchange mass spectrometry (DXMS). J. Mol. Biol. 327 (2003) 1065-1076
11. Wong L., Lieser S., Chie-Leon B., Miyashita O., Aubol B., Shaffer J., et al. Dynamic coupling between the SH2 domain and active site of the COOH terminal Src kinase, Csk. J. Mol. Biol. 341 (2004) 93-106
12. Alverdi V., Mazon H., Versluis C., Hemrika W., Esposito G., van den Heuvel R., et al. cGMP binding prepares PKG for substrate binding by disclosing the C-terminal domain. J. Mol. Biol. 375 (2007) 1380-1393
13. Hoofnagle A.H., Stoner J.W., Lee T., Eaton S.S., and Ahn N.G. Phosphorylation-dependent changes in structure and dynamics in ERK2 detected by SDSL and EPR. Biophys. J. 86 (2004) 395-403
14. Lee T., Hoofnagle A.N., Resing K.A., and Ahn N.G. Hydrogen exchange solvent protection by an ATP analogue reveals conformation change in ERK2 upon activation. J. Mol. Biol. 353 (2005) 600-612
15. Wang Z., Harkins P.C., Ulevitch R.J., Han J., Cobb M.H., and Goldsmith E.J. The structure of mitogen-activated protein kinase p38 at 2.1Å resolution. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 2327-2332
16. Wilson K.P., Fitzgibbon M.J., Caron P.R., Griffith J.P., Chen W., McCaffrey P.G., et al. Crystal structure of p38 mitogen-activated protein kinase. J. Biol. Chem. 271 (1996) 27696-27700
17. Xie X., Gu Y., Fox T., Coll J.T., Fleming M.A., Markland W., et al. Crystal structure of JNK3: a kinase implicated in neuronal apoptosis. Structure 6 (1998) 983-991
18. ter Haar E., Prabhakar P., Liu X., and Lepre C. Crystal structure of the p38 alpha-MAPKAP kinase 2 heterodimer. J. Biol. Chem. 282 (2007) 9733-9739
19. White A., Pargellis C.A., Studts J.M., Werneburg B.G., and Farmer B.T. Molecular basis of MAPK-activated protein kinase 2: p38 assembly. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 6353-6358
20. Bellon S., Fitzgibbon M.J., Fox T., Hsiao H.M., and Wilson K.P. The structure of phosphorylated p38 gamma is monomeric and reveals a conserved activation-loop conformation. Structure 7 (1999) 1057-1065
21. Nolen B., Taylor S., and Ghosh G. Regulation of protein kinases; controlling activity through activation segment conformation. Mol. Cell 15 (2004) 661-675
22. Perkins D.N., Pappin J.C., Creasy D.M., and Cottrell J.S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20 (1999) 3551-3567
23. Zhang Z. Prediction of low-energy collision-induced dissociation spectra of peptides. Anal. Chem. 76 (2004) 3908-3922
24. Zhang Z. Prediction of low-energy collision-induced dissociation spectra of peptides with three or more charges. Anal. Chem. 77 (2005) 6364-6373
25. Sun S., Meyer-Arendt K., Eichelberger B., Brown B., Yen C.Y., Old W., et al. Improved validation of peptides MS/MS assignments using spectral intensity prediction. Mol. Cell. Proteomics 6 (2006) 1-17
26. Diskin R., Lebendiker M., Engelberg D., and Livnah O. Structures of p38alpha active mutants reveal conformational changes in the L16 loop that induce autophosphorylation and activation. J. Mol. Biol. 365 (2007) 66-76
27. Diskin R., Askari N., Capone R., Engelberg D., and Livnah O. Active mutants of the human p38a mitogen-activated protein kinase. J. Biol. Chem. 279 (2004) 47040-47049
28. Avitzour M., Diskin R., Raboy B., Askari N., Engelberg D., and Livnah O. Intrinsically active variants of all human p38 isoforms. FEBS J. 274 (2007) 963-975
29. Doza Y.N., Cuenda A., Thomas G.M., Cohen P., and Nebreda A.R. Activation of the MAP kinase homologue RK requires the phosphorylation of Thr-180 and Tyr-182 and both residues are phosphorylated in chemically stresses KB cells. FEBS Lett. 364 (1995) 223-228
30. Tanoue T., Adachi M., Moriguchi T., and Nishida R. A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nat. Cell Biol. 2 (2000) 110-116
31. Chang C.I., Xu B.E., Akella R., Cobb M.H., and Goldsmith E.J. Crystal structure of MAP kinase p38 complexed to the docking sites on its nuclear substrate MEF2A and activator MKK3B. Mol. Cell 9 (2002) 1241-1249
32. Engel K., Kotlyarov A., and Gaestel M. Leptomycin B-sensitive nuclear export of MAPKAP kinase 2 is regulated by phosphorylation. EMBO J. 17 (1998) 3363-3371
33. Ge B., Gram H., DiPadova F., Huang B., New L., Ulevitch R.J., et al. MAPKK-independent activation of p38alpha mediated by TAB1-dependent autophosphorylation pf p38alpha. Science 295 (2002) 1291-1294
34. Zhou H., Zheng M., Chen J., Changchuan X., Kolatkar A.R., Zarubin T., et al. Determinants that control the specific interactions between TAB1 and p38α. Mol. Cell. Biol. 26 (2006) 3824-3834
35. Raingeaud J., Gupta S., Rogers J.S., Dickens M., Han J., Ulevitch R.J., and Davis R.J. Pro-inflammatory cytokines and environmental stress cause p38 mitogen activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem. 270 (1995) 7420-7426
36. Haystead T.A., Dent P., Wu J., Haystead C.M., and Sturgill T.W. Ordered phosphorylation of p42mapk by MAP kinase kinase. FEBS Lett. 306 (1992) 17-22
37. Zhang J., Zhang F., Ebert D., Cobb M.H., and Goldsmith E.J. Activity of the MAP kinase ERK2 is controlled by a flexible surface loop. Structure 3 (1995) 299-307
38. Wang Z., Canagarajah B.J., Boehm J.C., Kassisà S., Cobb M.H., Young P.R., et al. Structural basis of inhibitor selectivity in MAP kinases. Structure 6 (1998) 1117-1128
39. Frantz B., Klatt T., Pang M., Parsons J., Rolando A., Williams H., et al. The activation state of p38 mitogen-activated protein kinase determines the efficiency of ATP competition for pyridinylimidazole inhibitor binding. Biochemistry 37 (1998) 13846-13853
40. Fox T., Fitzgibbon M.J., Fleming M.A., Hsiao H.M., Brummel C.L., and Su M.S.S. Kinetic mechanism and ATP binding site reactivity of p38γ MAP kinase. FEBS Lett. 461 (1999) 323-328
41. Wilsbacher J.L., and Cobb M.H. Bacterial expression of activated mitogen-activated protein kinases. Methods Enzymol. 332 (2001) 387-400
42. Resing K.A., Hoofnagle A.N., and Ahn N.G. Modeling deuterium exchange behavior of ERK2 using pepsin mapping to probe secondary structure. J. Am. Soc. Mass Spectrom. 10 (1999) 685-702
43. Hoofnagle A.N., Resing K.A., and Ahn N.G. Practical methods for deuterium exchange/mass spectrometry. Methods Mol. Biol. 250 (2003) 283-298
44. Lee T., Hoofnagle A.N., Resing K.A., and Ahn N.G. Protein hydrogen exchange measured by electrospray ionization mass spectrometry. In: Celis J.E. (Ed). Cell Biology: A Laboratory Handbook. 3rd edit. vol. 4 (2006), Elsevier Academic Press, Burlington, MA. 443-449
45. Johnson M.L., Correia J.J., Yphantis D.A., and Halvorson H.R. Analysis of data from the analytical ultracentrifuge by nonlinear least-squares techniques. Biophys. J. 36 (1981) 575-588