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The interaction of PTP-BL PDZ domains with RIL: An enigmatic role for the RIL LIM domain

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Abstract

PDZ domains are protein-protein interaction modules that are crucial for the assembly of structural and signaling complexes. PDZ domains specifically bind short carboxyl-terminal peptides and occasionally internal sequences that structurally resemble peptide termini. Previously, using yeast two-hybrid methodology, we studied the interaction of two PDZ domains present in the large submembranous protein tyrosine phosphatase PTP-BL with the C-terminal half of the LIM domain-containing protein RIL. Deletion of the extreme RIL C-terminus did not eliminate binding, suggesting the presence of a PDZ binding site within the RIL LIM moiety. We have now performed experiments in mammalian cell lysates and found that the RIL C-terminus proper, but not the RIL LIM domain, can interact with PTP-BL, albeit very weakly. However, this interaction with PTP-BL PDZ domains is greatly enhanced when the combined RIL LIM domain and C-terminus is used, pointing to synergistic effects. NMR titration experiments and site-directed mutagenesis indicate that this result is not dependent on specific interactions that require surface exposed residues on the RIL LIM domain, suggesting a stabilizing role in the association with PTP-BL.

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Abbreviations

ALP:

alpha-actinin 2-associated LIM protein

C-terminal:

carboxyl terminal

GFP:

green fluorescent protein

LIM:

acronym of Lin-11 Lsl-1 Mec-3

NMR:

nuclear magnetic resonance

PDZ:

acronym of PSD95/SAP90 DlgA ZO-1

PTP-BL:

Protein tyrosine phosphatase BAS-like

RIL:

reversion-induced LIM gene.

References

  1. Pawson T (2004) Cell 116: 191–203.

    Google Scholar 

  2. van Ham M & Hendriks W (2003) Mol. Biol. Rep. 30: 69–82.

    Google Scholar 

  3. Nourry C, Grant SG & Borg JP (2003) Sci. S.T.K.E. 2003: RE7.

    Google Scholar 

  4. Erdmann KS (2003) Eur. J. Biochem. 270: 4789–4798.

    Google Scholar 

  5. Doyle DA, Lee A, Lewis J, Kim E, Sheng M & MacKinnon R (1996) Cell 85: 1067–1076.

    Google Scholar 

  6. Tochio H, Hung F, Li M, Bredt DS & Zhang M (2000) J. Mol. Biol. 295: 225–237.

    Google Scholar 

  7. Schultz J, Hoffmüller U, Krause G, Ashurst J & Macias MJ (1998) Nat. Struct. Biol. 5: 19–24.

    Google Scholar 

  8. Hillier B, Christopherson K, Prehoda K, Bredt D & Lim W (1999) Science 284: 812–815.

    Article  CAS  PubMed  Google Scholar 

  9. Kang BS, Cooper DR, Devedjiev Y, Derewenda U & Derewenda ZS (2003) Structure 11: 845–853.

    Google Scholar 

  10. Im YJ, Lee JR, Park SH, Park SJ, Rho SH, Kang GB, Kim E & Eom SH (2003) J. Biol. Chem. 278: 48099–48104.

    Google Scholar 

  11. Feng W, Shi Y, Li M & Zhang M (2003) Nat. Struct. Biol. 10: 972–978.

    Google Scholar 

  12. Garrard SM, Capaldo CT, Gao L, Rosen MK, Macara IG & Tomchick DR (2003) EMBO J. 22: 1125–1133.

    Google Scholar 

  13. Feng W, Fan J, Jiang M, Shi Y & Zhang M (2002) J. Biol. Chem. 277: 41140–41146.

    Google Scholar 

  14. Xia H, Winokur ST, Kuo W-L, Altherr MR & Bredt DS (1997) J. Cell Biol. 139: 507–515.

    Google Scholar 

  15. Maekawa K, Imagawa N, Naito A, Harada S, Yoshie O & Takagi S (1999) Biochem. J. 337: 179–184.

    Google Scholar 

  16. Cuppen E, Gerrits H, Pepers B, Wieringa B & Hendriks W (1998) Mol. Biol. Cell 9: 671–683.

    Google Scholar 

  17. Cuppen E, van Ham M, Wansink DG, de Leeuw A, Wieringa B & Hendriks W (2000) Eur. J. Cell Biol. 79: 283–293.

    Google Scholar 

  18. van Ham M, Croes H, Schepens J, Fransen J, Wieringa B & Hendriks W (2003) Genes Cells 8: 631–644

    Google Scholar 

  19. Siemens J, Kazmierczak P, Reynolds A, Sticker M, Littlewood-Evans A & Muller U (2002) Proc. Natl. Acad. Sci. U.S.A. 99: 14946–14951.

    Google Scholar 

  20. Hurd TW, Gao L, Roh MH, Macara IG & Margolis B (2003) Nature Cell Biol. 5: 137–142.

    Google Scholar 

  21. Lou X, Yano H, Lee F, Chao MV & Farquhar MG (2001) Mol. Biol. Cell 12: 615–627.

    Google Scholar 

  22. Tochio H, Mok YK, Zhang Q, Kan HM, Bredt DS & Zhang M (2000) J. Mol. Biol. 303: 359–370.

    Google Scholar 

  23. Wong H-C, Bourdelas A, Krauss A, Lee H-J, Shao Y, Wu D, Mlodzik M, Shi D-L & Zheng, J (2003) Mol. Cell 12: 1251–1260.

    Google Scholar 

  24. Zimmermann P, Meerschaert K, Reekmans G, Leenaerts I, Small JV, Vandekerckhove J, David G & Gettemans J (2002) Mol. Cell 9: 1215–1225.

    Google Scholar 

  25. Harris BZ, Hillier BJ & Lim WA (2001) Biochemistry 40: 5921–5930.

    Google Scholar 

  26. Erdmann KS, Kuhlmann J, Lessmann V, Hermann L, Eulenburg V, Müller O & Heumann R (2000) Oncogene 19: 3894–3901.

    Google Scholar 

  27. Irie S, Hachiya T, Rabizadeh S, Maruyama W, Mukai J, Li Y, Reed JC, Bredesen DE & Sato TA (1999) FEBS Lett. 460: 191–198.

    Google Scholar 

  28. Cuppen E, Nagata S, Wieringa B & Hendriks, W (1997) J. Biol. Chem. 272: 30215–30220.

    Google Scholar 

  29. Sato T, Irie S, Kitada S & Reed JC (1995) Science 268: 411–415.

    Google Scholar 

  30. Saras J, Engström U, Gonez LJ & Heldin, C-H (1997) J. Biol. Chem. 272: 20979–20981.

    Google Scholar 

  31. Kiess M, Scharm B, Aguzzi A, Hajnal A, Klemenz R, Schwarte Waldhoff I & Schafer R (1995) Oncogene 10: 61–68.

    Google Scholar 

  32. Fu SL, Waha A & Vogt PK (2000) Oncogene 19: 3537–3545.

    Google Scholar 

  33. Omasu F, Ezura Y, Kajita M, Ishida R, Kodaira M, Yoshida H, Suzuki T, Hosoi T, Inoue S, Shiraki M, Orimo H & Emi M (2003) J. Hum. Genet. 48: 342–345.

    Google Scholar 

  34. Vallenius T, Scharm B, Vesikansa A, Luukko K, Schäfer R & Mäkelä TP (2004) Exp. Cell Res. 293: 117–128.

    Google Scholar 

  35. Sadler I, Crawford A, Michelsen J & Beckerle M (1992) J. Cell Biol. 119: 1573–1587.

    Google Scholar 

  36. Dawid IB, Toyama R & Taira M (1995) C.R. Acad. Sci. 318: 295–306.

    Google Scholar 

  37. Walma T, Spronk CAEM, Tessari M, Aelen J, Schepens J, Hendriks W & Vuister GW (2002) J. Mol. Biol. 316: 1101–1110.

    Google Scholar 

  38. Cuppen E, van Ham M, Pepers B, Wieringa B & Hendriks W (1999) FEBS Lett. 459: 291–298.

    Google Scholar 

  39. Tanaka M, Gupta R & Mayer BJ (1995) Mol. Cell Biol. 15: 6829–6837.

    Google Scholar 

  40. Yon J & Fried M (1989) Nucl. Acids Res. 17: 4895.

    Google Scholar 

  41. Kreis TE (1986) EMBO J. 5: 931–941.

    Google Scholar 

  42. Koradi R, Billeter M & Wuthrich K (1996) J. Mol. Graph. 14: 51–55.

    Google Scholar 

  43. Gyuris J, Golemis E, Chertkov H & Brent R (1993) Cell 75: 791–803.

    Google Scholar 

  44. Finley RL, Jr. & Brent R (1994) Proc. Natl. Acad. Sci. USA 91: 12980–12984.

    Google Scholar 

  45. Klein Gunnewiek JMT, Hussein RI, van Aarssen Y, Palacios D, de Jong R, van Venrooij WJ & Gunderson SI (2000) Mol. Cell. Biol. 20: 2209–2217.

    Google Scholar 

  46. Shevchenko A, Wilm M, Vorm O & Mann M (1996) Anal. Chem. 68: 850–858.

    Google Scholar 

  47. Grootjans JJ, Reekmans G, Ceulemans H & David G (2000) J. Biol. Chem. 275: 19933–19941.

    Google Scholar 

  48. Feuerstein R, Wang X, Song D, Cooke NE & Liebhaber SA (1994) Proc. Natl. Acad. Sci. USA 91: 10655–10659.

    Google Scholar 

  49. Walker J, Crowley P, Moreman AD & Barrett J (1993) Mol. Biochem. Parasitol. 61: 255–64.

    Google Scholar 

  50. Konrat R, Weiskirchen R, Krautler B & Bister K (1997) J. Biol. Chem. 272: 12001–12007.

    Google Scholar 

  51. Kontaxis G, Konrat R, Krautler B, Weiskirchen R & Bister K (1998) Biochemistry 37: 7127–7134.

    Google Scholar 

  52. Konrat R, Kräutler B, Weiskirchen R & Bister K (1998) J. Biol. Chem. 273: 23233–23240.

    Google Scholar 

  53. Saras J, Franzén P, Aspenström P, Hellman U, Gonez LJ & Heldin C-H (1997) J. Biol. Chem. 272: 24333–24338.

    Google Scholar 

  54. Lin D, Gish GD, Songyang Z & Pawson T (1999) J. Biol. Chem. 274: 3726–3733.

    Google Scholar 

  55. Bach I (2000) Mech. Dev. 91: 5–17.

    Google Scholar 

  56. Murthy KK, Clark K, Fortin Y, Shen S-H & Banville D (1999) J. Biol. Chem. 274: 20679–20687.

    Google Scholar 

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Correspondence to Wiljan J. A. J. Hendriks.

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van den Berk, L.C.J., van Ham, M.A., te Lindert, M.M. et al. The interaction of PTP-BL PDZ domains with RIL: An enigmatic role for the RIL LIM domain. Mol Biol Rep 31, 203–215 (2005). https://doi.org/10.1007/s11033-005-1407-8

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  • DOI: https://doi.org/10.1007/s11033-005-1407-8

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