The differential regulation of p38α by the neuronal kinase interaction motif protein tyrosine phosphatases, a detailed molecular study

Structure

Volumn 21, Issue 9, 2013, Pages 1612-1623

  Francis, Dana May ^a   Kumar, Ganesan Senthil ^a   Koveal, Dorothy ^b   Tortajada, Antoni ^b   Page, Rebecca ^b   Peti, Wolfgang ^a,c  

^a BROWN UNIVERSITY   (United States)

^b BROWN UNIVERSITY   (United States)

^c BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 14; PROTEIN TYROSINE PHOSPHATASE;

ARTICLE; BINDING SITE; CATALYSIS; DEPHOSPHORYLATION; ENZYME PHOSPHORYLATION; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; X RAY CRYSTALLOGRAPHY;

CATALYTIC DOMAIN; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 14; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN TYROSINE PHOSPHATASES, NON-RECEPTOR; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 7; SCATTERING, SMALL ANGLE; THERMODYNAMICS; X-RAY DIFFRACTION;

EID: 84883487536     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.07.003     Document Type: Article

References (45)

1. R. Akella, X. Min, Q. Wu, K.H. Gardner, and E.J. Goldsmith The third conformation of p38α MAP kinase observed in phosphorylated p38α and in solution Structure 18 2010 1571 1578
2. M.C. Balasu, L.N. Spiridon, S. Miron, C.T. Craescu, A.J. Scheidig, A.J. Petrescu, and S.E. Szedlacsek Interface analysis of the complex between ERK2 and PTP-SL PLoS ONE 4 2009 e5432
3. C. Blanco-Aparicio, J. Torres, and R. Pulido A novel regulatory mechanism of MAP kinases activation and nuclear translocation mediated by PKA and the PTP-SL tyrosine phosphatase J. Cell Biol. 147 1999 1129 1136
4. C.I. Chang, B.E. Xu, R. Akella, M.H. Cobb, and E.J. Goldsmith Crystal structures of MAP kinase p38 complexed to the docking sites on its nuclear substrate MEF2A and activator MKK3b Mol. Cell 9 2002 1241 1249
5. R.G. Chirivi, G. Dilaver, R. van de Vorstenbosch, B. Wanschers, J. Schepens, H. Croes, J. Fransen, and W. Hendriks Characterization of multiple transcripts and isoforms derived from the mouse protein tyrosine phosphatase gene Ptprr Genes Cells 9 2004 919 933
6. S.J. de Vries, A.D. van Dijk, M. Krzeminski, M. van Dijk, A. Thureau, V. Hsu, T. Wassenaar, and A.M. Bonvin HADDOCK versus HADDOCK: new features and performance of HADDOCK2.0 on the CAPRI targets Proteins 69 2007 726 733
7. B. Dérijard, J. Raingeaud, T. Barrett, I.H. Wu, J. Han, R.J. Ulevitch, and R.J. Davis Independent human MAP-kinase signal transduction pathways defined by MEK and MKK isoforms Science 267 1995 682 685
8. R. Diskin, D. Engelberg, and O. Livnah A novel lipid binding site formed by the MAP kinase insert in p38 alpha J. Mol. Biol. 375 2008 70 79
9. C. Dominguez, R. Boelens, and A.M. Bonvin HADDOCK: a protein-protein docking approach based on biochemical or biophysical information J. Am. Chem. Soc. 125 2003 1731 1737
10. J. Eswaran, J.P. von Kries, B. Marsden, E. Longman, J.E. Debreczeni, E. Ugochukwu, A. Turnbull, W.H. Lee, S. Knapp, and A.J. Barr Crystal structures and inhibitor identification for PTPN5, PTPRR and PTPN7: a family of human MAPK-specific protein tyrosine phosphatases Biochem. J. 395 2006 483 491
11. D.M. Francis, B. Różycki, D. Koveal, G. Hummer, R. Page, and W. Peti Structural basis of p38α regulation by hematopoietic tyrosine phosphatase Nat. Chem. Biol. 7 2011 916 924
12. D.M. Francis, B. Różycki, A. Tortajada, G. Hummer, W. Peti, and R. Page Resting and active states of the ERK2:HePTP complex J. Am. Chem. Soc. 133 2011 17138 17141
13. D.M. Francis, R. Page, and W. Peti Sequence-specific backbone (1)H, (13)C and (15)N assignments of the 34 kDa catalytic domain of PTPN5 (STEP) Biomol. NMR Assign. 2013
14. A. Garai, A. Zeke, G. Gógl, I. Töro, F. Fördos, H. Blankenburg, T. Bárkai, J. Varga, A. Alexa, and D. Emig Specificity of linear motifs that bind to a common mitogen-activated protein kinase docking groove Sci. Signal. 5 2012 ra74
15. J.J. Gills, S.S. Castillo, C. Zhang, P.A. Petukhov, R.M. Memmott, M. Hollingshead, N. Warfel, J. Han, A.P. Kozikowski, and P.A. Dennis Phosphatidylinositol ether lipid analogues that inhibit AKT also independently activate the stress kinase, p38alpha, through MKK3/6-independent and -dependent mechanisms J. Biol. Chem. 282 2007 27020 27029
16. W. Hendriks, J. Schepens, C. Brugman, P. Zeeuwen, and B. Wieringa A novel receptor-type protein tyrosine phosphatase with a single catalytic domain is specifically expressed in mouse brain Biochem. J. 305 1995 499 504
17. E.K. Kim, and E.J. Choi Pathological roles of MAPK signaling pathways in human diseases Biochim. Biophys. Acta 1802 2010 396 405
18. P.V. Konarev, V.V. Volkov, A.V. Sokolova, M.H.J. Koch, and D.I. Svergun PRIMUS: a Windows PC-based system for small-angle scattering data analysis J. Appl. Cryst. 36 2003 1277 1282
19. M.B. Kozin, and D.I. Svergun Automated matching of high- and low-resolution structural models J. Appl. Cryst. 34 2001 33 41
20. M.A. Larkin, G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, F. Valentin, I.M. Wallace, A. Wilm, and R. Lopez Clustal W and Clustal X version 2.0 Bioinformatics 23 2007 2947 2948
21. P.J. Lombroso, G. Murdoch, and M. Lerner Molecular characterization of a protein-tyrosine-phosphatase enriched in striatum Proc. Natl. Acad. Sci. USA 88 1991 7242 7246
22. P.J. Lombroso, J.R. Naegele, E. Sharma, and M. Lerner A protein tyrosine phosphatase expressed within dopaminoceptive neurons of the basal ganglia and related structures J. Neurosci. 13 1993 3064 3074
23. J.J. Muñoz, C. Tárrega, C. Blanco-Aparicio, and R. Pulido Differential interaction of the tyrosine phosphatases PTP-SL, STEP and HePTP with the mitogen-activated protein kinases ERK1/2 and p38alpha is determined by a kinase specificity sequence and influenced by reducing agents Biochem. J. 372 2003 193 201
24. T. Mustelin, L. Tautz, and R. Page Structure of the hematopoietic tyrosine phosphatase (HePTP) catalytic domain: structure of a KIM phosphatase with phosphate bound at the active site J. Mol. Biol. 354 2005 150 163
25. G. Nielsen, and H. Schwalbe NMR spectroscopic investigations of the activated p38α mitogen-activated protein kinase ChemBioChem 12 2011 2599 2607
26. P.A. Nony, S.B. Kennett, W.C. Glasgow, K. Olden, and J.D. Roberts 15S-Lipoxygenase-2 mediates arachidonic acid-stimulated adhesion of human breast carcinoma cells through the activation of TAK1, MKK6, and p38 MAPK J. Biol. Chem. 280 2005 31413 31419
27. A. Ortega, D. Amorós, and J. García de la Torre Prediction of hydrodynamic and other solution properties of rigid proteins from atomic- and residue-level models Biophys. J. 101 2011 892 898
28. J.J. Perry, R.M. Harris, D. Moiani, A.J. Olson, and J.A. Tainer p38alpha MAP kinase C-terminal domain binding pocket characterized by crystallographic and computational analyses J. Mol. Biol. 391 2009 1 11
29. W. Peti, and R. Page Strategies to maximize heterologous protein expression in Escherichia coli with minimal cost Protein Expr. Purif. 51 2007 1 10
30. A. Piserchio, D.M. Francis, D. Koveal, K.N. Dalby, R. Page, W. Peti, and R. Ghose Docking interactions of hematopoietic tyrosine phosphatase with MAP kinases ERK2 and p38α Biochemistry 51 2012 8047 8049
31. R. Poddar, I. Deb, S. Mukherjee, and S. Paul NR2B-NMDA receptor mediated modulation of the tyrosine phosphatase STEP regulates glutamate induced neuronal cell death J. Neurochem. 115 2010 1350 1362
32. M. Saxena, S. Williams, K. Taskén, and T. Mustelin Crosstalk between cAMP-dependent kinase and MAP kinase through a protein tyrosine phosphatase Nat. Cell Biol. 1 1999 305 311
33. D. Svergun Determination of the regularization parameter in indirect-transform methods using perceptual criteria J. Appl. Cryst. 25 1992 495 503
34. D.I. Svergun, M.V. Petoukhov, and M.H. Koch Determination of domain structure of proteins from X-ray solution scattering Biophys. J. 80 2001 2946 2953
35. S.E. Szedlacsek, A.R. Aricescu, T.A. Fulga, L. Renault, and A.J. Scheidig Crystal structure of PTP-SL/PTPBR7 catalytic domain: implications for MAP kinase regulation J. Mol. Biol. 311 2001 557 568
36. C. Tárrega, C. Blanco-Aparicio, J.J. Muñoz, and R. Pulido Two clusters of residues at the docking groove of mitogen-activated protein kinases differentially mediate their functional interaction with the tyrosine phosphatases PTP-SL and STEP J. Biol. Chem. 277 2002 2629 2636
37. N. Tzarum, Y. Eisenberg-Domovich, J.J. Gills, P.A. Dennis, and O. Livnah Lipid molecules induce p38α activation via a novel molecular switch J. Mol. Biol. 424 2012 339 353
38. A.M. Van Den Maagdenberg, D. Bächner, J.T. Schepens, W. Peters, J.A. Fransen, B. Wieringa, and W.J. Hendriks The mouse Ptprr gene encodes two protein tyrosine phosphatases, PTP-SL and PTPBR7, that display distinct patterns of expression during neural development Eur. J. Neurosci. 11 1999 3832 3844
39. M. Vogtherr, K. Saxena, S. Grimme, M. Betz, U. Schieborr, B. Pescatore, T. Langer, and H. Schwalbe NMR backbone assignment of the mitogen-activated protein (MAP) kinase p38 J. Biomol. NMR 32 2005 175
40. V.V. Volkov, and D.I. Svergun Uniqueness of ab initio shape determination in small-angle scattering J. Appl. Cryst. 36 2003 860 864
41. Z. Wang, P.C. Harkins, R.J. Ulevitch, J. Han, M.H. Cobb, and E.J. Goldsmith The structure of mitogen-activated protein kinase p38 at 2.1-A resolution Proc. Natl. Acad. Sci. USA 94 1997 2327 2332
42. J. Xu, P. Kurup, Y. Zhang, S.M. Goebel-Goody, P.H. Wu, A.H. Hawasli, M.L. Baum, J.A. Bibb, and P.J. Lombroso Extrasynaptic NMDA receptors couple preferentially to excitotoxicity via calpain-mediated cleavage of STEP J. Neurosci. 29 2009 9330 9343
43. B. Zanke, H. Suzuki, K. Kishihara, L. Mizzen, M. Minden, A. Pawson, and T.W. Mak Cloning and expression of an inducible lymphoid-specific, protein tyrosine phosphatase (HePTPase) Eur. J. Immunol. 22 1992 235 239
44. Y.Y. Zhang, J.W. Wu, and Z.X. Wang Mitogen-activated protein kinase (MAPK) phosphatase 3-mediated cross-talk between MAPKs ERK2 and p38alpha J. Biol. Chem. 286 2011 16150 16162
45. T. Zhou, L. Sun, J. Humphreys, and E.J. Goldsmith Docking interactions induce exposure of activation loop in the MAP kinase ERK2 Structure 14 2006 1011 1019