Molecular basis of the PED/PEA15 interaction with the C-terminal fragment of phospholipase D1 revealed by NMR spectroscopy

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1834, Issue 8, 2013, Pages 1572-1580

  Farina, Biancamaria ^a   Doti, Nunzianna ^a   Pirone, Luciano ^a   Malgieri, Gaetano ^b   Pedone, Emilia M ^a   Ruvo, Menotti ^a   Fattorusso, Roberto ^b  

^a CNR   (Italy)

^b SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

Chemical shift perturbation; Death domain; NMR; PED PEA15 protein; Protein protein interaction

Indexed keywords

D4 ALPHA PROTEIN; PHOSPHOLIPASE D1; PHOSPHOPROTEIN; PHOSPHOPROTEIN ENRICHED IN ASTROCYTE 15; PHOSPHOPROTEIN ENRICHED IN DIABETES; PROTEIN KINASE C ALPHA; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG; PEA15 PROTEIN, HUMAN; PEPTIDE FRAGMENT; PHOSPHOLIPASE D; SIGNAL PEPTIDE;

ALLOSTERISM; ARTICLE; BINDING SITE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; CHEMISTRY; HUMAN; METABOLISM; PROTEIN CONFORMATION;

ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDE FRAGMENTS; PHOSPHOLIPASE D; PHOSPHOPROTEINS; PROTEIN CONFORMATION;

EID: 84879048177     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2013.04.012     Document Type: Article

References (40)

1. H. Araujo, N. Danziger, J. Cordier, J. Glowinski, H. Chneiweiss, Characterization of PEA-15, a major substrate for protein kinase C in astrocytes, J. Biol. Chem. 268 (1993) 5911-5920. (Pubitemid 23090927)
2. A. Estellés, M. Yokoyama, F. Nothias, J.D. Vincent, J. Glowinski, P. Vernier, H. Chneiweiss, The major astrocytic phosphoprotein PEA-15 is encoded by two mRNAs conserved on their full length in mouse and human, J. Biol. Chem. 271 (1996) 14800-14806. (Pubitemid 26194960)
3. J.M. Hill, H. Vaidyanathan, J.W. Ramos, M.H. Ginsberg, M.H. Werner, Recognition of ERK MAP kinase by PEA-15 reveals a common docking site within the death domain and death effector domain, EMBO J. 21 (2002) 6494-6504. (Pubitemid 35448427)
4. E.C. Twomey, Y. Wei, High-definition NMR structure of PED/PEA-15 death effector domain reveals details of key polar side chain interactions, Biochem. Biophys. Res. Commun. 424 (2012) 141-146.
5. F. Fiory, P. Formisano, G. Perruolo, F. Beguinot, Frontiers: PED/PEA-15, a multifunctional protein controlling cell survival and glucose metabolism, Am. J. Physiol. Endocrinol. Metab. 297 (2009) 592-601.
6. G. Condorelli, G. Vigliotta, C. Iavarone, M. Caruso, C.G. Tocchetti, F. Andreozzi, A. Cafieri, M.F. Tecce, P. Formisano, L. Beguinot, F. Beguinot, PED/PEA-15 gene controls glucose transport and is overexpressed in type 2 diabetes mellitus, EMBO J. 17 (1998) 3858-3866. (Pubitemid 28333972)
7. R. Valentino, G.A. Lupoli, G.A. Raciti, F. Oriente, E. Farinaro, E. Della Valle, M. Salomone, G. Riccardi, O. Vaccaro, G. Donnarumma, G. Sesti, M.L. Hribal, M. Cardellini, C. Miele, P. Formisano, F. Beguinot, The PEA15 gene is overexpressed and related to insulin resistance in healthy first-degree relatives of patients with type 2 diabetes, Diabetologia 49 (2006) 3058-3066. (Pubitemid 44730310)
8. P. Ungaro, R. Teperino, P. Mirra, A. Cassese, F. Fiory, G. Perruolo, C. Miele, M. Laakso, P. Formisano, F. Beguinot, Molecular cloning and characterization of the human PED/PEA-15 gene promoter reveals antagonistic regulation by HNF-4alpha and COUP-TFII, J. Biol. Chem. 283 (2008) 30970-30979.
9. G. Vigliotta, C. Miele, S. Santopietro, G. Portella, A. Perfetti, M.A. Maitan, A. Cassese, F. Oriente, A. Trencia, F. Fiory, C. Romano, C. Tiveron, L. Tatangelo, G. Troncone, P. Formisano, F. Beguinot, Overexpression of the PED/PEA-15 gene causes diabetes by impairing glucose-stimulated insulin secretion in addition to insulin action, Mol. Cell. Biol. 24 (2004) 5005-5015. (Pubitemid 38668062)
10. C. Miele, G.A. Raciti, A. Cassese, C. Romano, F. Giacco, F. Oriente, F. Paturzo, F. Andreozzi, A. Zabatta, G. Troncone, F. Bosch, A. Pujol, H. Chneiweiss, P. Formisano, F. Beguinot, PED/PEA-15 regulates glucose-induced insulin secretion by restraining potassium channel expression inpancreatic beta-cells, Diabetes 56 (2007) 622-633. (Pubitemid 46348454)
11. Y. Zhang, O. Redina, Y.M. Altshuller, M. Yamazaki, J. Ramos, H. Chneiweiss, Y. Kanaho, M.A. Frohman, Regulation of expression of phospholipase D1 and D2 by PEA-15, a novel protein that interacts with them, J. Biol. Chem. 275 (2000) 35224-35232.
12. F. Viparelli, A. Cassese, N. Doti, F. Paturzo, D. Marasco, N.A. Dathan, S.M. Monti, G. Basile, P. Ungaro, M. Sabatella, C. Miele, R. Teperino, E. Consiglio, C. Pedone, F. Beguinot, P. Formisano, M. Ruvo, Targeting of PED/PEA-15 molecular interaction with phospholipase D1 enhances insulin sensitivity in skeletal muscle cells, J. Biol. Chem. 283 (2008) 21769-21778.
13. N. Doti, A. Cassese, D. Marasco, F. Paturzo, M. Sabatella, F. Viparelli, N. Dathan, S.M. Monti, C. Miele, P. Formisano, F. Beguinot, M. Ruvo, Residues 762-801 of PLD1 mediate the interaction with PED/PEA15, Mol. Biosyst. 6 (2010) 2039-2048.
14. M. Mayer, B. Meyer, Group epitope mapping by saturation transfer difference NMR to identify segments of a ligand in direct contact with a protein receptor, J. Am. Chem. Soc. 123 (2001) 6108-6117. (Pubitemid 32888480)
15. M. Mayer, B. Meyer, Characterization of ligand binding bysaturation transfer difference NMR spectroscopy, Angew. Chem. Int. Ed. 38 (1999) 1784-1788. (Pubitemid 29290947)
16. B. Farina, L. Pirone, L. Russo, F. Viparelli, N. Doti, C. Pedone, E.M. Pedone, R. Fattorusso, NMR backbone dynamics studies of human PED/PEA-15 outline protein functional sites, FEBS J. 277 (2010) 4229-4240.
17. F. Viparelli, N. Doti, A. Sandomenico, D. Marasco, N.A. Dathan, C. Miele, F. Beguinot, S.M. Monti, M. Ruvo, Expression and purification of the D4 region of PLD1 and characterization of its interaction with PED-PEA15, Protein Expr. Purif. 59 (2008) 302-308.
18. G.B. Fields, R.L. Noble, Solid phase peptide synthesis utilizing 9-fluorenylmethoxycarbonyl amino acids, Int. J. Pept. Protein Res. 35 (1990) 161-214. (Pubitemid 20126875)
19. C.N. Pace, F. Vajdos, L. Fee, G. Grimsley, T. Gray, How to measure and predict the molar absorption coefficient of a protein, Protein Sci. 4 (1995) 2411-2423.
20. C. Stan Tsai, Biomacromolecules: Introduction to Structure, Function and Informatics, J. Wiley and sons, Hoboken, NJ, 2007. 183-209.
21. D. Marion, M. Ikura, R. Tschudin, A. Bax, Rapid recording of 2D NMR spectra without phase-cycling. Application to the study of hydrogen exchange in proteins, J. Magn. Reson. 85 (1989) 393-399.
22. M. Piotto, V. Saudek, V. Sklenar, Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions, J. Biomol. NMR 2 (1992) 661-665.
23. V. Sklenar, M. Piotto, R. Leppik, V. Saudek, Gradient-tailored water suppression for 1H-15N HSQC experiments optimized to retain full sensitivity, J. Magn. Reson. A 102 (1993) 241-245.
24. L. Braunschweiler, R.R. Ernst, Coherence transfer by isotropic mixing: application to proton correlation spectroscopy, J. Magn. Reson. 53 (1983) 521-528.
25. R.R. Anil-Kumar, K. Wüthrich Ernst, A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules, Biochem. Biophys. Res. Commun. 95 (1980) 1-6.
26. T.L. Hwang, A.J. Shaka, Water suppression that works: excitation sculpting using arbitrary wave-forms and pulsed-field gradients, J. Magn. Reson. A 112 (1995) 275-279.
27. C. Dalvit, Efficient multiple-solvent suppression for the study of the interactions of organic solvents with biomolecules, J. Biomol. NMR 11 (1998) 437-444. (Pubitemid 128512224)
28. ACD/NMR Processor Freeware, Version 12.01, Advanced Chemistry Development, Inc., Toronto, ON, Canada, 2012., (www.acdlabs.com).
29. R.L.J. Keller, The Computer Aided Resonance Assignment Tutorial, CANTINA Verlag, 2004.
30. K. Gunasekaran, B. Ma, R. Nussinov, Is allostery an intrinsic property of all dynamic proteins? Proteins 57 (2004) 433-443. (Pubitemid 39390799)
31. X. Niu, Q. Chen, J. Zhang, W. Shen, Y. Shi, J. Wu, Interesting structural and dynamical behaviors exhibitedbythe AF-6 PDZ domain upon Bcr peptide binding, Biochemistry 46 (2007) 15042-15053. (Pubitemid 350308896)
32. E.C. Twomey, D.F. Cordasco, Y. Wei, Profound conformational changes of PED/PEA-15 in ERK2 complex revealed by NMR backbone dynamics, BBA prot. and proteomics 1824 (2012) 1382-1393.
33. K. Kersse, J. Verspurten, T. VandenBerghe, P. Vandenabeele, The death-fold superfamily of homotypic interaction motifs, Trends Biochem. Sci. 36 (2011) 541-552.
34. F.Y. Li, P.D. Jeffrey, J.W. Yu, Y. Shi, Crystal structure of MC159 reveals molecular mechanism of DISC assembly and FLIP inhibition, J. Biol. Chem. 281 (2006) 2960-2968.
35. J.K. Yang, L. Wang, L. Zheng, F. Wan, M. Ahmed, Crystal structure of MC159 reveals molecular mechanism of DISC assembly and FLIP inhibition, Mol. Cell 20 (2005) 939-949. (Pubitemid 41814882)
36. C. Bagnéris, A.V. Ageichik, N. Cronin, B. Wallace, M. Collins, C. Boshoff, G. Waksman, T. Barrett, Crystal structure of a vFlip-IKK gamma complex: insights into viral activation of the IKK signalosome, Mol. Cell 30 (2008) 620-631. (Pubitemid 351755065)
37. H. Qin, S.M. Srinivasula, G. Wu, T. Fernandes-Alnemri, E.S. Alnemri, Y. Shi, Structural basis of procaspase-9 recruitment by the apoptotic protease-activating factor 1, Nature 399 (1999) 547-555.
38. T. Srimathi, S.L. Robbins, R.L. Dubas, H. Chang, H. Cheng, H. Roder, Y.C. Park, Mapping of POP1-binding site on pyrin domain of ASC, J. Biol. Chem. 283 (2008) 15390-15398.
39. Y. Kam, J.H. Exton, Dimerization of phospholipase d isozymes, Biochem. Biophys. Res. Commun. 290 (2002) 375-380. (Pubitemid 34694509)
40. R. Koradi, M. Billenter, K. Wutrich, MOLMOL: a program for display and analysis of macromolecular structures, J. Mol. Graphics 14 (1996) 51-55. (Pubitemid 26152976)