Tes, a Specific Mena Interacting Partner, Breaks the Rules for EVH1 Binding

Molecular Cell

Volumn 28, Issue 6, 2007, Pages 1071-1082

  Boëda, Batiste ^a   Briggs, David C ^a,b   Higgins, Theresa ^a   Garvalov, Boyan K ^c   Fadden, Andrew J ^a   McDonald, Neil Q ^a,d   Way, Michael ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^d UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

SIGNALING

Indexed keywords

CYTOSKELETON PROTEIN; LAMELLIPODIN; LIM PROTEIN; LIM3 PROTEIN; PROTEIN EVL; PROTEIN MENA; PROTEIN TES; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN; VINCULIN; ZYXIN;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

3T3 CELLS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL LINE; CELL MOVEMENT; CYTOPLASM; GREEN FLUORESCENT PROTEINS; HELA CELLS; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOBLOTTING; MICE; MICROFILAMENT PROTEINS; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TUMOR SUPPRESSOR PROTEINS;

EID: 37349034970     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.10.033     Document Type: Article

References (45)

1. Arakawa Y., Cordeiro J.V., and Way M. F11L-mediated inhibition of RhoA-mDia signaling stimulates microtubule dynamics during vaccinia virus infection. Cell Host Microbe 1 (2007) 213-226
2. Bachmann C., Fischer L., Walter U., and Reinhard M. The EVH2 domain of the vasodilator-stimulated phosphoprotein mediates tetramerization, F-actin binding, and actin bundle formation. J. Biol. Chem. 274 (1999) 23549-23557
3. Ball L.J., Kuhne R., Hoffmann B., Hafner A., Schmieder P., Volkmer-Engert R., Hof M., Wahl M., Schneider-Mergener J., Walter U., et al. Dual epitope recognition by the VASP EVH1 domain modulates polyproline ligand specificity and binding affinity. EMBO J. 19 (2000) 4903-4914
4. Ball L.J., Jarchau T., Oschkinat H., and Walter U. EVH1 domains: structure, function and interactions. FEBS Lett. 513 (2002) 45-52
5. Barzik M., Kotova T.I., Higgs H.N., Hazelwood L., Hanein D., Gertler F.B., and Schafer D.A. Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins. J. Biol. Chem. 280 (2005) 28653-28662
6. Bear J.E., Loureiro J.J., Libova I., Fassler R., Wehland J., and Gertler F.B. Negative regulation of fibroblast motility by Ena/VASP proteins. Cell 101 (2000) 717-728
7. Bear J.E., Svitkina T.M., Krause M., Schafer D.A., Loureiro J.J., Strasser G.A., Maly I.V., Chaga O.Y., Cooper J.A., Borisy G., and Gertler F.B. Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109 (2002) 1-20
8. Carl U.D., Pollmann M., Orr E., Gertlere F.B., Chakraborty T., and Wehland J. Aromatic and basic residues within the EVH1 domain of VASP specify its interaction with proline-rich ligands. Curr. Biol. 9 (1999) 715-718
9. Coutts A.S., MacKenzie E., Griffith E., and Black D.M. TES is a novel focal adhesion protein with a role in cell spreading. J. Cell Sci. 116 (2003) 897-906
10. Di Modugno F., Bronzi G., Scanlan M.J., Del Bello D., Cascioli S., Venturo I., Botti C., Nicotra M.R., Mottolese M., Natali P.G., et al. Human Mena protein, a serex-defined antigen overexpressed in breast cancer eliciting both humoral and CD8+ T-cell immune response. Int. J. Cancer 109 (2004) 909-918
11. Di Modugno F., Mottolese M., Di Benedetto A., Conidi A., Novelli F., Perracchio L., Venturo I., Botti C., Jager E., Santoni A., et al. The cytoskeleton regulatory protein hMena (ENAH) is overexpressed in human benign breast lesions with high risk of transformation and human epidermal growth factor receptor-2-positive/hormonal receptor-negative tumors. Clin. Cancer Res. 12 (2006) 1470-1478
12. Di Modugno F., Demonte L., Balsamo M., Bronzi G., Nicotra M.R., Alessio M., Jager E., Condeelis J.S., Santoni A., Natali P.G., and Nistico P. Molecular cloning of hMena (ENAH) and its splice variant hMena+11a: epidermal growth factor increases their expression and stimulates hMena+11a phosphorylation in breast cancer cell lines. Cancer Res. 67 (2007) 2657-2665
13. Drees B., Friederich E., Fradelizi J., Louvard D., Beckerle M.C., and Golsteyn R.M. Characterization of the interaction between zyxin and members of the Ena/vasodilator-stimulated phosphoprotein family of proteins. J. Biol. Chem. 275 (2000) 22503-22511
14. Drusco A., Zanesi N., Roldo C., Trapasso F., Farber J.L., Fong L.Y., and Croce C.M. Knockout mice reveal a tumor suppressor function for Testin. Proc. Natl. Acad. Sci. USA 102 (2005) 10947-10951
15. Fedorov A.A., Fedorov E., Gertler F., and Almo S.C. Structure of EVH1, a novel proline-rich ligand-binding module involved in cytoskeletal dynamics and neural function. Nat. Struct. Biol. 6 (1999) 661-665
16. Gareus R., Di Nardo A., Rybin V., and Witke W. Mouse profilin 2 regulates endocytosis and competes with SH3 ligand binding to dynamin 1. J. Biol. Chem. 281 (2006) 2803-2811
17. Garvalov B.K., Higgins T.E., Sutherland J.D., Zettl M., Scaplehorn N., Kocher T., Piddini E., Griffiths G., and Way M. The conformational state of Tes regulates its zyxin-dependent recruitment to focal adhesions. J. Cell Biol. 161 (2003) 33-39
18. Griffith E., Coutts A.S., and Black D.M. Characterisation of chicken TES and its role in cell spreading and motility. Cell Motil. Cytoskeleton 57 (2004) 133-142
19. Hoffman L.M., Jensen C.C., Kloeker S., Wang C.L., Yoshigi M., and Beckerle M.C. Genetic ablation of zyxin causes Mena/VASP mislocalization, increased motility, and deficits in actin remodeling. J. Cell Biol. 172 (2006) 771-782
20. Huttelmaier S., Harbeck B., Steffens O., Messerschmidt T., Illenberger S., and Jockusch B.M. Characterization of the actin binding properties of the vasodilator-stimulated phosphoprotein VASP. FEBS Lett. 451 (1999) 68-74
21. Jenzora A., Behrendt B., Small J.V., Wehland J., and Stradal T.E. PREL1 provides a link from Ras signalling to the actin cytoskeleton via Ena/VASP proteins. FEBS Lett. 579 (2005) 455-463
22. Kadrmas J.L., and Beckerle M.C. The LIM domain: from the cytoskeleton to the nucleus. Nat. Rev. Mol. Cell Biol. 5 (2004) 920-931
23. Krause M., Dent E.W., Bear J.E., Loureiro J.J., and Gertler F.B. Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu. Rev. Cell Dev. Biol. 19 (2003) 541-564
24. Krause M., Leslie J.D., Stewart M., Lafuente E.M., Valderrama F., Jagannathan R., Strasser G.A., Rubinson D.A., Liu H., Way M., et al. Lamellipodin, an Ena/VASP ligand, is implicated in the regulation of lamellipodial dynamics. Dev. Cell 7 (2004) 571-583
25. Lafuente E.M., van Puijenbroek A.A., Krause M., Carman C.V., Freeman G.J., Berezovskaya A., Constantine E., Springer T.A., Gertler F.B., and Boussiotis V.A. RIAM, an Ena/VASP and Profilin ligand, interacts with Rap1-GTP and mediates Rap1-induced adhesion. Dev. Cell 7 (2004) 585-595
26. Laurent V., Loisel T.P., Harbeck B., Wehman A., Grobe L., Jockusch B.M., Wehland J., Gertler F.B., and Carlier M.F. Role of proteins of the Ena/VASP family in actin-based motility of Listeria monocytogenes. J. Cell Biol. 144 (1999) 1245-1258
27. Legg J.A., and Machesky L.M. MRL proteins: leading Ena/VASP to Ras GTPases. Nat. Cell Biol. 6 (2004) 1015-1017
28. Loureiro J.J., Rubinson D.A., Bear J.E., Gretchen A., Kwiatkowski A.V., and Gertler F.B. Critical roles of phosphorylation and actin binding motifs, but not the central proline-rich region, for Ena/VASP function during cell migration. Mol. Biol. Cell 13 (2002) 2533-2546
29. Mueller W., Nutt C.L., Ehrich M., Riemenschneider M.J., von Deimling A., van den Boom D., and Louis D.N. Downregulation of RUNX3 and TES by hypermethylation in glioblastoma. Oncogene 26 (2006) 583-593
30. Niebuhr K., Ebel F., Frank R., Reinhard M., Domann E., Carl U.D., Walter U., Gertler F.B., Wehland J., and Chakraborty T. A novel proline-rich motif present in ActA of Listeria monocytogenes and cytoskeletal proteins is the ligand for the EVH1 domain, a protein module present in the Ena/VASP family. EMBO J. 16 (1997) 5433-5444
31. Prehoda K.E., Lee D.J., and Lim W.A. Structure of the Enabled/VASP homology 1 domain-peptide complex: a key component in the spatial control of actin assembly. Cell 97 (1999) 471-480
32. CCP4 (Collaborative Computational Project, Number 4). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50 (1994) 760-763
33. Quinn C.C., Pfeil D.S., Chen E., Stovall E.L., Harden M.V., Gavin M.K., Forrester W.C., Ryder E.F., Soto M.C., and Wadsworth W.G. UNC-6/netrin and SLT-1/slit guidance cues orient axon outgrowth mediated by MIG-10/RIAM/lamellipodin. Curr. Biol. 16 (2006) 845-853
34. Renfranz P.J., and Beckerle M.C. Doing (F/L)PPPPs: EVH1 domains and their proline-rich partners in cell polarity and migration. Curr. Opin. Cell Biol. 14 (2002) 88-103
35. Rottner K., Krause M., Gimona M., Small J.V., and Wehland J. Zyxin is not colocalized with vasodilator-stimulated phosphoprotein (VASP) at lamellipodial tips and exhibits different dynamics to vinculin, paxillin, and VASP in focal adhesions. Mol. Biol. Cell 12 (2001) 3103-3113
36. Sarti M., Sevignani C., Calin G.A., Aqeilan R., Shimizu M., Pentimalli F., Picchio M.C., Godwin A., Rosenberg A., Drusco A., et al. Adenoviral transduction of TESTIN gene into breast and uterine cancer cell lines promotes apoptosis and tumor reduction in vivo. Clin. Cancer Res. 11 (2005) 806-813
37. Tanoue T., and Takeichi M. New insights into Fat cadherins. J. Cell Sci. 118 (2005) 2347-2353
38. Tatarelli C., Linnenbach A., Mimori K., and Croce C.M. Characterization of the human TESTIN gene localized in the FRA7G region at 7q31.2. Genomics 68 (2000) 1-12
39. Tobias E.S., Hurlstone A.F., MacKenzie E., McFarlane R., and Black D.M. The TES gene at 7q31.1 is methylated in tumours and encodes a novel growth-suppressing LIM domain protein. Oncogene 20 (2001) 2844-2853
40. Todaro G.J., and Green H. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 17 (1963) 299-313
41. Walders-Harbeck B., Khaitlina S.Y., Hinssen H., Jockusch B.M., and Illenberger S. The vasodilator-stimulated phosphoprotein promotes actin polymerisation through direct binding to monomeric actin. FEBS Lett. 529 (2002) 275-280
42. Wang W., Goswami S., Lapidus K., Wells A.L., Wyckoff J.B., Sahai E., Singer R.H., Segall J.E., and Condeelis J.S. Identification and testing of a gene expression signature of invasive carcinoma cells within primary mammary tumors. Cancer Res. 64 (2004) 8585-8594
43. Wang W., Wyckoff J.B., Goswami S., Wang Y., Sidani M., Segall J.E., and Condeelis J.S. Coordinated regulation of pathways for enhanced cell motility and chemotaxis is conserved in rat and mouse mammary tumors. Cancer Res. 67 (2007) 3505-3511
44. Zarrinpar A., Bhattacharyya R.P., and Lim W.A. The structure and function of proline recognition domains. Sci. STKE 2003 (2003) RE8
45. Zarrinpar A., Park S.H., and Lim W.A. Optimization of specificity in a cellular protein interaction network by negative selection. Nature 426 (2003) 676-680