NMR studies of tandem WW domains of Nedd4 in complex with a PY motif- containing region of the epithelial sodium channel

Biochemistry and Cell Biology

Volumn 76, Issue 2-3, 1998, Pages 341-350

  Kanelis, Voula ^a,b   Farrow, Neil A ^c,d   Kay, Lewis E ^c   Rotin, Daniela ^a,b   Forman Kay, Julie D ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d DUPONT COMPANY   (United States)

Author keywords

ENaC; Nedd4; NMR; PY motif; WW domain

Indexed keywords

DYSTROGLYCAN; SODIUM CHANNEL;

ARTICLE; BINDING AFFINITY; ENZYME ACTIVITY; NUCLEAR MAGNETIC RESONANCE; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; STRUCTURE ACTIVITY RELATION;

EID: 0007902080     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/o98-042     Document Type: Article

References (51)

1. Alexandropoulos, K., Cheng, G., and Baltimore, D. 1995. Proline-rich sequences that bind to Src homology 3 domains with individual specificities. Proc. Natl. Acad. Sci. U.S.A. 92: 3110-3114.
2. André, B., and Springael, J.-Y. 1994. WWP, a new amino acid motif present in single or multiple copies in various proteins including dystrophin and the SH3-binding Yes-associated protein YAP65. Biochem. Biophys. Res. Commun. 205: 1201-1205.
3. Bedford, M.T., Chan, D.C., and Leder, P. 1997. FBP WW domains and the Ab1 SH3 domain bind to a specific class of proline-rich ligands. EMBO J. 16: 2376-2383.
4. Bork, P., and Sudol, M. 1994. The WW domain: a signalling site in dystrophin. Trends Biochem. Sci. 19: 531-533.
5. Canessa, C.M., Horisberger, J.-D., and Rossier, B.C. 1993. Epithelial sodium channel related to proteins involved in neurodegeneration. Nature (London), 361: 467-470.
6. + channel is made of three homologous subunits. Nature (London), 367: 463-467.
7. Chan, D.C., Bedford, M.T., and Leder, P. 1996. Formin binding proteins bear WW/WWP domains that bind proline-rich peptides and functionally resemble SH3 domains. EMBO J. 15: 1045-1054.
8. Chen, H.I., and Sudol, M. 1995. The WW domain of Yes-associated protein binds a proline rich ligand that differs from the consensus established for Src homology 3-binding modules. Proc. Natl. Acad. Sci. U.S.A. 92: 7819-7823.
9. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J., and Bax, A. 1995. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR, 6: 277-293.
10. Ermekova, KS., Zambrano, N., Linn, H., Minopoli, G., Gerder, F., Russo, T., and Sudol, M. 1997. The WW domain of neural protein FE65 interacts with proline-rich motif in Mena, the mammalian homolog of Drosophila Enabled. J. Biol. Chem. 272: 32 869-32 877.
11. Firsov, D., Schild, L., Gautschi, I., Merillat, A.M., Schneeberger, E., and Rossier, B.C. 1996. Cell surface expression of the epithelial Na channel and a mutant causing Liddle syndrome: a quantitative approach. Proc. Natl. Acad. Sci. U.S.A. 93: 10 946-10 952.
12. Firsov, D., Gautschi, I., Merillat, A., Rossier, B., and Schild, L. 1998. The heterotetrameric architecture of the epithelial sodium channel (ENaC). EMBO J. 17: 344-352.
13. Gertler, F.B., Niebuhr, K., Reinhard, M., Wehland, J., and Soriano, P. 1996. Mena, a relative of VASP and Drosophila Enabled, is implicated in the control of microfilament dynamics. Cell, 87: 227-239.
14. Grzesiek, S., and Bax, A. 1992. Correlating backbone amide and side chain resonances in larger proteins by multiple relayed triple resonance NMR. J. Am. Chem. Soc. 114: 6291-6293.
15. 13C magnetization. J. Magn. Reson. Ser. B, 101: 114-119.
16. Hansson, J.H., Nelson-Williams, C., Suzuki, H., Schild, L., Shimkets, R., Lu, Y., Canessa, C.M., Iwasaki, T., Rossier, B.C., and Lifton, R.P. 1995a. Hypertension caused by a truncated epithelial sodium channel γ subunit: genetic heterogeneity of Liddle syndrome. Nat. Genet. 11: 76-82.
17. Hansson, J.H., Schild, L., Lu, Y., Wilson, R., Shimkets, R., Nelson-Williams, C., Rossier, B.C., and Lifton, R.P. 1995b. A de novo missence mutation of the β subunit of the epithelial sodium channel causes hypertension and Liddle's syndrome, identifying a proline-rich segment critical for regulation of channel activity. Proc. Natl. Acad. Sci. U.S.A. 92: 11 495-11 499.
18. Hofmann, K., and Bucher, P. 1995. The rsp5-domain is shared by proteins of diverse functions. FEBS Lett. 358: 153-157.
19. Johnson, B.A., and Blevins, R.A. 1994. NMRView: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR, 4: 603-614.
20. Jung, D., Yang, B., Meyer, J., Chamberlain, J.S., and Campbell, K.P. 1995. Identification and characterization of the dystrophin anchoring site on β-dystroglycan. J. Biol. Chem. 270: 27 305-27 310.
21. 2O. J. Am. Chem. Soc. 115: 2055-2057.
22. Kay, L., Wittekind, M., McCoy, M., Friedrichs, M., Bell, A., Ernst, E., Lavoie, T., and Mueller, L. 1992. 4D NMR triple-resonance experiments for assignment of protein backbone nuclei using shared constant-time evolution periods. J. Magn. Reson. 98: 443-350.
23. 2O saturation. J. Magn. Reson. Ser. A, 109: 129-133.
24. Kumar, S., Tomooka, Y., and Noda, M. 1992. Identification of a set of genes with developmentally down-regulated expression in the mouse brain. Biochem. Biophys. Res. Commun. 185: 1155-1161.
25. Liddle, G.W., Bledsoe, M.T., and Coppage, W.S., Jr. 1963. A familial disorder simulating primary aldosteroneism, but with negligible aldosterone secretion. Trans. Assoc. Am. Physicians, 76: 199-213.
26. Lim, W.A., Hodel, A., Sauer, R.T., and Richards, F.M. 1994. The crystal structure of a mutant protein with altered but improved hydrophobic core packing. Proc. Natl. Acad. Sci. U.S.A. 91: 423-427.
27. Logan, T.M., Olejniczak, E.T., Xu, R.X., and Fesik, S.W. 1992. Side chain and backbone assignments in isotopically labeled proteins from two heteronuclear triple resonance experiments. FEBS Lett. 314: 413-418.
28. Macias, M.J., Hyvonen, M., Baraldi, E., Schultz, J., Sudol, M., Saraste, M., and Oschkinat, H. 1996. Structure of the WW domain of a kinase-associated protein complexed with a proline rich peptide. Nature (London), 382: 646-649.
29. 15N NMR assignments and global folding pattern. Biochemistry, 32: 13 818-13 829.
30. Pawson, T. 1995. Protein modules and signaling networks. Nature (London), 373: 573-579.
31. Pirozzi, G., McConnell, S.J., Uveges, A.J., Carter, J.M., Sparks, A.B., Kay, B.K., and Fowlkes, D.M. 1997. Identification of novel human WW domain-containing proteins by cloning of ligand targets. J. Biol. Chem. 272: 14 611-14 616.
32. 2+-dependent plasma membrane localization. J. Biol. Chem. 272: 32 329-32 336.
33. Ranganathan, R., Lu, K., Hunter, T., and Noel, J.P. 1997. Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent. Cell, 89: 875-886.
34. Rotin, D., Bar-Sagi, D., O'Brodovich, H., Merilainen, J., Lebto, V.P., Canessa, C.M., Rossier, B.C., and Downey, G.P. 1994. An SH3 binding region in the epithelial Na+ channel (αrENaC) mediates its localization at the apical membrane. EMBO J. 13: 4440-4450.
35. Rozakis-Adcock, M., Fernley, R., Wade, J., Pawson, T., and Bowtell, D. 1993. The SH2 and SH3 domains of mammalian Grb2 couple the EGF receptor to the Ras activator mSosl. Nature (London), 363: 83-85.
36. Schild, L., Canessa, C.M., Shimkets, R.A., Warnock, D.G., Lifton, R.P., and Rossier, B.C. 1995. A mutation in the epithelial sodium channel causing Liddle's disease increases channel activity in the Xenopus oocyte expression system. Proc. Natl. Acad. Sci. U.S.A. 92: 5699-5703.
37. Schild, L, Lu, Y., Gautschi, I., Schneeberger, E., Lifton, R.P., and Rossier, B.C. 1996. Identification of a PY motif in the epithelial Na channel subunits as a target sequence for mutations causing channel activation found in Liddle syndrome. EMBO J. 15: 2381-2387.
38. Seavey, B.R., Farr, E.A., Westler, W.M., and Markley, J.L. 1991. A relational database for sequence-specific protein NMR data. J. Biomol. NMR, 1: 217-236.
39. Shimkets, R.A., Warnock, D.G., Bostis, C.M., Nelson-Williams, C., Hansson, J.H., Schambelan, M., Gill, J.R., Jr., Ulick, S., Milora, R.V., Finding, J.W., Canessa, C.M., Rossier, B.C., and Lifton, R.P. 1994. Liddle's syndrome: heritable human hypertension caused by mutations in the β subunit of the epithelial sodium channel. Cell, 79: 407-414.
40. + channel. Cell, 83: 969-978.
41. 13Cβ nuclear magnetic resonance chemical shifts. J. Am. Chem. Soc. 113: 5490-5492.
42. Staub, O., and Rotin, D. 1996. WW domains. Structure (London), 4: 495-499.
43. + channel deleted in Liddle's syndrome. EMBO J. 15: 2371-2380.
44. + channel (ENaC) by ubiquitination. EMBO J. 16: 6325-6336.
45. Studier, F.W., Rosenberg, A.H., Dunn, J.J., and Dubendorff, J.W. 1990. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185: 60-89.
46. Tamura, H., Schild, L., Enomoto, N., Matsui, N., Marumo, F., Rossier, B.C., and Sesaki, S. 1996. Liddle disease caused by missence mutations of β subunit of epithelial sodium channel gene. J. Clin. Invest. 97: 1780-1784.
47. Teresawa, H., Kohda, D., Hatanaka, H., Tsuchiya, S., Ogura, K., Nagata, K., Ishii, S., Mandiyan, B., Ullrich, A., Schlessinger, J., and Inagaki, F. 1994. Structure of the N-terminal SH3 domain of GRB2 complexed with a peptide from the guanine nucleotide releasing factor Sos. Nat. Struct. Biol. 1: 891-897.
48. Wittekind, M., and Mueller, L. 1993. HNCACB, a high sensitivity 3D NMR experiment to correlate amide proton and nitrogen resonances with the α-and β-carbon resonances in proteins. J. Magn. Reson. Ser. B, 101: 201-205.
49. Wittekind, M., Mapelli, C., Farmer, B., II, Suen, K.-L., Goldfarb, V., Tsao, J., Lavoie, T., Barbacid, M., Meyers, C., and Mueller, L. 1994. Orientation of peptide fragments from Sos proteins bound to the N-terminal SH3 domain of Grb2 determined by NMR spectroscopy. Biochemistry, 33: 13 531-13 539.
50. Yu, H., Chen, J.K., Feng, S., Dalgarno, D.C., Brauer, A.W., and Schreiber, S.L. 1994. Structural basis for the binding of proline-rich peptides to SH3 domains. Cell, 76: 933-945.
51. 15N resonance assignments of the N-terminal SH3 domain of drk in folded and unfolded states using enhanced-sensitivity pulsed field gradient NMR techniques. J. Biomol. NMR, 4: 845-858.