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Structural basis for polyproline recognition by the FE65 WW domain.

Meiyappan M, Birrane G, Ladias JAA
J Mol Biol 372 970-980 (2007)
Related entries: 2idh, 2oei

Cited: 41 times
EuropePMC logo PMID: 17686488

Abstract

The neuronal protein FE65 functions in brain development and amyloid precursor protein (APP) signaling through its interaction with the mammalian enabled (Mena) protein and APP, respectively. The recognition of short polyproline sequences in Mena by the FE65 WW domain has a central role in axon guidance and neuronal positioning in the developing brain. We have determined the crystal structures of the human FE65 WW domain (residues 253-289) in the apo form and bound to the peptides PPPPPPLPP and PPPPPPPPPL, which correspond to human Mena residues 313-321 and 347-356, respectively. The FE65 WW domain contains two parallel ligand-binding grooves, XP (formed by residues Y269 and W280) and XP2 (formed by Y269 and W271). Both Mena peptides adopt a polyproline helical II conformation and bind to the WW domain in a forward (N-C) orientation through selection of the PPPPP motif by the XP and XP2 grooves. This mode of ligand recognition is strikingly similar to polyproline interaction with SH3 domains. Importantly, comparison of the FE65 WW structures in the apo and liganded forms shows that the XP2 groove is formed by an induced-fit mechanism that involves movements of the W271 and Y269 side-chains upon ligand binding. These structures elucidate the molecular determinants underlying polyproline ligand selection by the FE65 WW domain and provide a framework for the design of small molecules that would interfere with FE65 WW-ligand interaction and modulate neuronal development and APP signaling.

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Articles citing this publication (20)

  1. CFL1, a WW domain protein, regulates cuticle development by modulating the function of HDG1, a class IV homeodomain transcription factor, in rice and Arabidopsis. Wu R, Li S, He S, Wassmann F, Yu C, Qin G, Schreiber L, Qu LJ, Gu H. Plant Cell 23 3392-3411 (2011)
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  3. Another role of proline: stabilization interactions in proteins and protein complexes concerning proline and tryptophane. Biedermannova L, E Riley K, Berka K, Hobza P, Vondrasek J. Phys Chem Chem Phys 10 6350-6359 (2008)
  4. Structure and function of the two tandem WW domains of the pre-mRNA splicing factor FBP21 (formin-binding protein 21). Huang X, Beullens M, Zhang J, Zhou Y, Nicolaescu E, Lesage B, Hu Q, Wu J, Bollen M, Shi Y. J Biol Chem 284 25375-25387 (2009)
  5. The proline-rich domain of TonB possesses an extended polyproline II-like conformation of sufficient length to span the periplasm of Gram-negative bacteria. Köhler SD, Weber A, Howard SP, Welte W, Drescher M. Protein Sci 19 625-630 (2010)
  6. Degradation of mutant huntingtin via the ubiquitin/proteasome system is modulated by FE65. Chow WN, Luk HW, Chan HY, Lau KF. Biochem J 443 681-689 (2012)
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  8. Selection of a high-affinity WW domain against the extracellular region of VEGF receptor isoform-2 from a combinatorial library using CIS display. Patel S, Mathonet P, Jaulent AM, Ullman CG. Protein Eng Des Sel 26 307-315 (2013)
  9. A WW Tandem-Mediated Dimerization Mode of SAV1 Essential for Hippo Signaling. Lin Z, Xie R, Guan K, Zhang M. Cell Rep 32 108118 (2020)
  10. Effects of the Pentapeptide P33 on Memory and Synaptic Plasticity in APP/PS1 Transgenic Mice: A Novel Mechanism Presenting the Protein Fe65 as a Target. Szögi T, Schuster I, Borbély E, Gyebrovszki A, Bozsó Z, Gera J, Rajkó R, Sántha M, Penke B, Fülöp L. Int J Mol Sci 20 E3050 (2019)
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  13. Crystal structure of the first WW domain of human YAP2 isoform. Martinez-Rodriguez S, Bacarizo J, Luque I, Camara-Artigas A. J Struct Biol 191 381-387 (2015)
  14. Sjögren syndrome/scleroderma autoantigen 1 is a direct Tankyrase binding partner in cancer cells. Perdreau-Dahl H, Progida C, Barfeld SJ, Guldsten H, Thiede B, Arntzen M, Bakke O, Mills IG, Krauss S, Morth JP. Commun Biol 3 123 (2020)
  15. Structural and functional characterization of a novel FE65 protein product up-regulated in cognitively impaired FE65 knockout mice. Cool BH, Zitnik G, Martin GM, Hu Q. J Neurochem 112 410-419 (2010)
  16. The structure of the first representative of Pfam family PF09836 reveals a two-domain organization and suggests involvement in transcriptional regulation. Das D, Grishin NV, Kumar A, Carlton D, Bakolitsa C, Miller MD, Abdubek P, Astakhova T, Axelrod HL, Burra P, Chen C, Chiu HJ, Chiu M, Clayton T, Deller MC, Duan L, Ellrott K, Ernst D, Farr CL, Feuerhelm J, Grzechnik A, Grzechnik SK, Grant JC, Han GW, Jaroszewski L, Jin KK, Johnson HA, Klock HE, Knuth MW, Kozbial P, Krishna SS, Marciano D, McMullan D, Morse AT, Nigoghossian E, Nopakun A, Okach L, Oommachen S, Paulsen J, Puckett C, Reyes R, Rife CL, Sefcovic N, Tien HJ, Trame CB, van den Bedem H, Weekes D, Wooten T, Xu Q, Hodgson KO, Wooley J, Elsliger MA, Deacon AM, Godzik A, Lesley SA, Wilson IA. Acta Crystallogr Sect F Struct Biol Cryst Commun 66 1174-1181 (2010)
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  18. Letter Allosteric modulation of the binding affinity between PQBP1 and the spliceosomal protein U5-15kD. Mizuguchi M, Obita T, Kajiyama A, Kozakai Y, Nakai T, Nabeshima Y, Okazawa H. FEBS Lett 590 2221-2231 (2016)
  19. Identification of novel functional mini-receptors by combinatorial screening of split-WW domains. Neitz H, Paul NB, Häge FR, Lindner C, Graebner R, Kovermann M, Thomas F. Chem Sci 13 9079-9090 (2022)
  20. Molecular Interactions between Two LMP2A PY Motifs of EBV and WW Domains of E3 Ubiquitin Ligase AIP4. Seo MD, Seok SH, Kim JH, Choi JW, Park SJ, Lee BJ. Life (Basel) 11 379 (2021)


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