Mechanism and consequence of the autoactivation of p38α mitogen-activated protein kinase promoted by TAB1

Nature Structural and Molecular Biology

Volumn 20, Issue 10, 2013, Pages 1182-1192

  De Nicola, Gian Felice ^a,b   Martin, Eva Denise ^a   Chaikuad, Apirat ^c   Bassi, Rekha ^a   Clark, James ^a   Martino, Luigi ^b   Verma, Sharwari ^a   Sicard, Pierre ^a   Tata, Renée ^b   Atkinson, R Andrew ^b   Knapp, Stefan ^c,d   Conte, Maria R ^b   Marber, Michael S ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 14; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1 BINDING PROTEIN 1; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CARDIOTOXICITY; CATALYSIS; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVATION; ENZYME STABILITY; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; MOLECULAR DOCKING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; RAT; THERMODYNAMICS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ANIMALS; ENZYME ACTIVATION; HUMANS; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 14; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MYOCARDIAL ISCHEMIA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHORYLATION; RATS; SEQUENCE HOMOLOGY, AMINO ACID;

BACTERIA (MICROORGANISMS); MAMMALIA; RATTUS;

EID: 84885433426     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2668     Document Type: Article

References (49)

1. Cuenda, A. & Rousseau, S. p38 MAP-kinases pathway regulation, function and role in human diseases. Biochim. Biophys. Acta 1773, 1358-1375 (2007). (Pubitemid 47125981)
2. Mudgett, J.S. et al. Essential role for p38α mitogen-activated protein kinase in placental angiogenesis. Proc. Natl. Acad. Sci. USA 97, 10454-10459 (2000).
3. Beardmore, V.A. et al. Generation and characterization of p38β (MAPK11) gene-targeted mice. Mol. Cell Biol. 25, 10454-10464 (2005). (Pubitemid 41681967)
4. Lee, J.C. et al. A protein kinase involved in the regulation of infammatory cytokine biosynthesis. Nature 372, 739-746 (1994).
5. Gum, R.J. et al. Acquisition of sensitivity of stress-activated protein kinases to the p38 inhibitor, SB 203580, by alteration of one or more amino acids within the ATP binding pocket. J. Biol. Chem. 273, 15605-15610 (1998). (Pubitemid 28298174)
6. Dominguez, C., Powers, D.A. & Tamayo, N. p38 MAP kinase inhibitors: many are made, but few are chosen. Curr. Opin. Drug Discov. Devel. 8, 421-430 (2005). (Pubitemid 40921741)
7. Genovese, M.C. Inhibition of p38: has the fat lady sung? Arthritis Rheum. 60, 317-320 (2009).
8. Hammaker, D. & Firestein, G.S. "Go upstream, young man": lessons learned from the p38 saga. Ann. Rheum. Dis. 69 (suppl. 1), i77-i82 (2010).
9. Martin, D.E., Felice De Nicola, G. & Marber, M.S. New therapeutic targets in cardiology: p38α mitogen-activated protein kinase for ischemic heart disease. Circulation 126, 357-368 (2012).
10. Tanno, M. et al. Diverse mechanisms of myocardial p38 mitogen-activated protein kinase activation: evidence for MKK-independent activation by a TAB1-associated mechanism contributing to injury during myocardial ischemia. Circ. Res. 93, 254-261 (2003). (Pubitemid 36993237)
11. Li, J., Miller, E.J., Ninomiya-Tsuji, J., Russell, R.R. III & Young, L.H. AMP-activated protein kinase activates p38 mitogen-activated protein kinase by increasing its recruitment to tab1 in the ischemic heart. Circ. Res. 97, 872-879 (2005). (Pubitemid 41552672)
12. Ota, A., Zhang, J., Ping, P., Han, J. & Wang, Y. Specifc regulation of noncanonical p38α activation by Hsp90-Cdc37 chaperone complex in cardiomyocyte. Circ. Res. 106, 1404-1412 (2010).
13. Fiedler, B. et al. cGMP-dependent protein kinase type I inhibits TAB1-p38 mitogen-activated protein kinase apoptosis signaling in cardiac myocytes. J. Biol. Chem. 281, 32831-32840 (2006). (Pubitemid 46036838)
14. Shi, J. et al. Amyloidogenic light chains induce cardiomyocyte contractile dysfunction and apoptosis via a non-canonical p38α MAPK pathway. Proc. Natl. Acad. Sci. USA 107, 4188-4193 (2010).
15. Ge, B. et al. MAPKK-independent activation of p38α mediated by TAB1-dependent autophosphorylation of p38α. Science 295, 1291-1294 (2002). (Pubitemid 34157620)
16. Cheung, P.C., Campbell, D.G., Nebreda, A.R. & Cohen, P. Feedback control of the protein kinase TAK1 by SAPK2a/p38α. EMBO J. 22, 5793-5805 (2003). (Pubitemid 37408818)
17. Diskin, R., Lebendiker, M., Engelberg, D. & Livnah, O. Structures of p38α active mutants reveal conformational changes in L16 loop that induce autophosphorylation and activation. J. Mol. Biol. 365, 66-76 (2007). (Pubitemid 44821197)
18. Salvador, J.M. et al. Alternative p38 activation pathway mediated by T cell receptor-proximal tyrosine kinases. Nat. Immunol. 6, 390-395 (2005). (Pubitemid 41716779)
19. Lochhead, P.A. Protein kinase activation loop autophosphorylation in cis: overcoming a Catch-22 situation. Sci. Signal. 2, e4 (2009).
20. Wilson, K.P. et al. Crystal structure of p38 mitogen-activated protein kinase. J. Biol. Chem. 271, 27696-27700 (1996). (Pubitemid 26367339)
21. Zhang, W.X. et al. Time-resolved Forster resonance energy transfer assays for the binding of nucleotide and protein substrates to p38α protein kinase. Anal. Biochem. 343, 76-83 (2005).
22. Shrestha, A., Hamilton, G., O'Neill, E., Knapp, S. & Elkins, J.M. Analysis of conditions affecting auto-phosphorylation of human kinases during expression in bacteria. Protein Expr. Purif. 81, 136-143 (2012).
23. Jacquet, S. et al. The role of RIP2 in p38 MAPK activation in the stressed heart. J. Biol. Chem. 283, 11964-11971 (2008).
24. Kumphune, S. et al. A chemical genetic approach reveals that p38α MAPK activation by diphosphorylation aggravates myocardial infarction and is prevented by the direct binding of SB203580. J. Biol. Chem. 285, 2968-2975 (2010).
25. Sicard, P. et al. The activation of p38α, and not p38β, mitogen-activated protein kinase is required for ischemic preconditioning. J. Mol. Cell Cardiol. 48, 1324-1328 (2010).
26. Ge, B. et al. TAB1β (transforming growth factor-β-activated protein kinase 1-binding protein 1β), a novel splicing variant of TAB1 that interacts with p38α but not TAK1. J. Biol. Chem. 278, 2286-2293 (2003). (Pubitemid 36801298)
27. Zhou, H. et al. Determinants that control the specifc interactions between TAB1 and p38α. Mol. Cell. Biol. 26, 3824-3834 (2006). (Pubitemid 43726399)
28. Rothweiler, U. et al. p38α MAP kinase dimers with swapped activation segments and a novel catalytic loop conformation. J. Mol. Biol. 411, 474-485 (2011).
29. Cameron, A.J., Escribano, C., Saurin, A.T., Kostelecky, B. & Parker, P.J. PKC maturation is promoted by nucleotide pocket occupation independently of intrinsic kinase activity. Nat. Struct. Mol. Biol. 16, 624-630 (2009).
30. Blethrow, J., Zhang, C., Shokat, K.M. & Weiss, E.L. Design and use of analog-sensitive protein kinases. Curr. Protoc. Mol. Biol. 66, 18.11 (2004).
31. Wang, Z. et al. The structure of mitogen-activated protein kinase p38 at 2.1-A resolution. Proc. Natl. Acad. Sci. USA 94, 2327-2332 (1997).
32. Kornev, A.P., Taylor, S.S. & Ten Eyck, L.F. A helix scaffold for the assembly of active protein kinases. Proc. Natl. Acad. Sci. USA 105, 14377-14382 (2008).
33. Bhattacharyya, R.P. et al. The Ste5 scaffold allosterically modulates signaling output of the yeast mating pathway. Science 311, 822-826 (2006). (Pubitemid 43228840)
34. Wang, Y. et al. Cardiac muscle cell hypertrophy and apoptosis induced by distinct members of the p38 mitogen activated protein kinase family. J. Biol. Chem. 273, 2161-2168 (1998). (Pubitemid 28069266)
35. Bukhtiyarova, M. et al. Improved expression, purifcation, and crystallization of p38α MAP kinase. Protein Expr. Purif. 37, 154-161 (2004). (Pubitemid 39027255)
36. Delaglio, F. et al. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).
37. Johnson, B.A. & Blevins, R.A. NMR View: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4, 603-614 (1994).
38. Bartels, C., Xia, T.H., Billeter, M., Guntert, P. & Wuthrich, K. The program XEASY for computer-supported NMR spectral analysis of biological macromolecules. J. Biomol. NMR 6, 1-10 (1995).
39. Pervushin, K., Riek, R., Wider, G. & Wuthrich, K. Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc. Natl. Acad. Sci. USA 94, 12366-12371 (1997).
40. Palmer, A.G. III, Fairbrother, W.J., Cavanagh, J., Wright, P.E. & Rance, M. Improved resolution in three-dimensional constant-time triple resonance NMR spectroscopy of proteins. J. Biomol. NMR 2, 103-108 (1992).
41. Schleucher, J. et al. A general enhancement scheme in heteronuclear multidimensional NMR employing pulsed feld gradients. J. Biomol. NMR 4, 301-306 (1994).
42. Foster, M.P., McElroy, C.A. & Amero, C.D. Solution NMR of large molecules and assemblies. Biochemistry 46, 331-340 (2007). (Pubitemid 46115942)
43. Martino, L. et al. Analysis of the interaction with the hepatitis C virus mRNA reveals an alternative mode of RNA recognition by the human La protein. Nucleic Acids Res. 40, 1381-1394 (2012).
44. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
45. McCoy, A.J., Grosse-Kunstleve, R.W., Storoni, L.C. & Read, R.J. Likelihood-enhanced fast translation functions. Acta Crystallogr. D Biol. Crystallogr. 61, 458-464 (2005). (Pubitemid 43934606)
46. Koeberle, S.C. et al. Skepinone-L is a selective p38 mitogen-activated protein kinase inhibitor. Nat. Chem. Biol. 8, 141-143 (2012).
47. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004). (Pubitemid 41742764)
48. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refnement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997). (Pubitemid 27235885)
49. Bellahcene, M. et al. Activation of p38 mitogen-activated protein kinase contributes to the early cardiodepressant action of tumor necrosis factor. J. Am. Coll. Cardiol. 48, 545-555 (2006). (Pubitemid 44093944)