A protein interaction map for cell-cell adhesion regulators identifies DUSP23 as a novel phosphatase for β-catenin

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Gallegos, Lisa Leon ^a   Ng, Mei Rosa ^a,b   Sowa, Mathew E ^a,c   Selfors, Laura M ^a   White, Anne ^a   Zervantonakis, Ioannis K ^a   Singh, Pragya ^a   Dhakal, Sabin ^a   Harper, J Wade ^a   Brugge, Joan S ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c Warp Drive Bio LLC ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CATENIN; BETA CATENIN; CADHERIN; CDH1 PROTEIN, HUMAN; DUAL SPECIFICITY PHOSPHATASE; DUSP23 PROTEIN, HUMAN; PROTEIN BINDING; TYROSINE;

ADHERENS JUNCTION; CELL ADHESION; CELL LINE; CHEMISTRY; DOWN REGULATION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; PHOSPHORYLATION; PROCEDURES; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION;

ADHERENS JUNCTIONS; ALPHA CATENIN; BETA CATENIN; CADHERINS; CELL ADHESION; CELL LINE; DOWN-REGULATION; DUAL-SPECIFICITY PHOSPHATASES; HEK293 CELLS; HUMANS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN INTERACTION MAPS; TYROSINE;

EID: 84973308393     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep27114     Document Type: Article

References (44)

1. Harris, T. J. & Tepass, U. Adherens junctions: from molecules to morphogenesis. Nat. Rev. Mol. Cell Biol. 11, 502-514, doi: 10.1038/ nrm2927 (2010).
2. Zaidel-Bar, R. Cadherin adhesome at a glance. J. Cell Sci. 126, 373-378, doi: 10.1242/jcs.111559 (2013).
3. Macara, I. G., Guyer, R., Richardson, G., Huo, Y. & Ahmed, S. M. Epithelial homeostasis. Curr. Biol. 24, R815-825, doi: 10.1016/j. cub.2014.06.068 (2014).
4. McClatchey, A. I. & Yap, A. S. Contact inhibition (of proliferation) redux. Curr. Opin. Cell Biol. 24, 685-694, doi: 10.1016/j. ceb.2012.06.009 (2012).
5. Takeichi, M. Dynamic contacts: rearranging adherens junctions to drive epithelial remodelling. Nat. Rev. Mol. Cell Biol. 15, 397-410, doi: 10.1038/nrm3802 (2014).
6. Brennan, D. et al. Suprabasal Dsg2 expression in transgenic mouse skin confers a hyperproliferative and apoptosis-resistant phenotype to keratinocytes. J. Cell Sci. 120, 758-771, doi: 10.1242/jcs.03392 (2007).
7. Green, K. J., Getsios, S., Troyanovsky, S. & Godsel, L. M. Intercellular junction assembly, dynamics, and homeostasis. Cold Spring Harb. Perspect. Biol. 2, a000125, doi: 10.1101/cshperspect.a000125 (2010).
8. Sevilla, L. M., Nachat, R., Groot, K. R. & Watt, F. M. Kazrin regulates keratinocyte cytoskeletal networks, intercellular junctions and differentiation. J. Cell Sci. 121, 3561-3569, doi: 10.1242/jcs.029538 (2008).
9. Johnson, J. L., Najor, N. A. & Green, K. J. Desmosomes: Regulators of Cellular Signaling and Adhesion in Epidermal Health and Disease. Cold Spring Harb. Perspect. Med. 4, doi: 10.1101/cshperspect.a015297 (2014).
10. Toret, C. P., D'Ambrosio, M. V., Vale, R. D., Simon, M. A. & Nelson, W. J. A genome-wide screen identifies conserved protein hubs required for cadherin-mediated cell-cell adhesion. J. Cell Biol. 204, 265-279, doi: 10.1083/jcb.201306082 (2014).
11. Guo, Z. et al. E-cadherin interactome complexity and robustness resolved by quantitative proteomics. Sci. Signal. 7, rs7, doi: 10.1126/ scisignal.2005473 (2014).
12. Van Itallie, C. M. et al. Biotin ligase tagging identifies proteins proximal to E-cadherin, including lipoma preferred partner, a regulator of epithelial cell-cell and cell-substrate adhesion. J. Cell Sci. 127, 885-895, doi: 10.1242/jcs.140475 (2014).
13. Simpson, K. J. et al. Identification of genes that regulate epithelial cell migration using an siRNA screening approach. Nat. Cell Biol. 10, 1027-1038, doi: 10.1038/ncb1762 (2008).
14. Sowa, M. E., Bennett, E. J., Gygi, S. P. & Harper, J. W. Defining the human deubiquitinating enzyme interaction landscape. Cell 138, 389-403, doi: 10.1016/j.cell.2009.04.042 (2009).
15. Behrends, C., Sowa, M. E., Gygi, S. P. & Harper, J. W. Network organization of the human autophagy system. Nature 466, 68-76, doi: 10.1038/nature09204 (2010).
16. le Duc, Q. et al. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J. Cell Biol. 189, 1107-1115, doi: 10.1083/jcb.201001149 (2010).
17. Yonemura, S., Wada, Y., Watanabe, T., Nagafuchi, A. & Shibata, M. alpha-Catenin as a tension transducer that induces adherens junction development. Nat. Cell Biol. 12, 533-542, doi: 10.1038/ncb2055 (2010).
18. Lizcano, J. M. et al. LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J. 23, 833-843, doi: 10.1038/sj.emboj.7600110 (2004).
19. DerMardirossian, C. & Bokoch, G. M. GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell Biol. 15, 356-363, doi: 10.1016/j.tcb.2005.05.001 (2005).
20. Mouneimne, G. et al. Differential remodeling of actin cytoskeleton architecture by profilin isoforms leads to distinct effects on cell migration and invasion. Cancer cell 22, 615-630, doi: 10.1016/j.ccr.2012.09.027 (2012).
21. Burridge, K. & Mangeat, P. An interaction between vinculin and talin. Nature 308, 744-746 (1984).
22. Cohen, D., Brennwald, P. J., Rodriguez-Boulan, E. & Musch, A. Mammalian PAR-1 determines epithelial lumen polarity by organizing the microtubule cytoskeleton. J. Cell Biol. 164, 717-727, doi: 10.1083/jcb.200308104 (2004).
23. Huveneers, S. & de Rooij, J. Mechanosensitive systems at the cadherin-F-actin interface. J. Cell Sci. 126, 403-413, doi: 10.1242/ jcs.109447 (2013).
24. Manning, D. K. et al. Loss of the ciliary kinase Nek8 causes left-right asymmetry defects. J. Am. Soc. Neph. 24, 100-112, doi: 10.1681/ ASN.2012050490 (2013).
25. Frank, V. et al. Mutations in NEK8 link multiple organ dysplasia with altered Hippo signalling and increased c-MYC expression. Hum. Mol. Genet. 22, 2177-2185, doi: 10.1093/hmg/ddt070 (2013).
26. Taddei, M. L. et al. Beta-catenin interacts with low-molecular-weight protein tyrosine phosphatase leading to cadherin-mediated cell-cell adhesion increase. Cancer Res. 62, 6489-6499 (2002).
27. Sallee, J. L., Wittchen, E. S. & Burridge, K. Regulation of cell adhesion by protein-tyrosine phosphatases: II. Cell-cell adhesion. J. Biol. Chem. 281, 16189-16192, doi: 10.1074/jbc.R600003200 (2006).
28. Barcellos, K. S. et al. ARHGAP21 protein, a new partner of alpha-tubulin involved in cell-cell adhesion formation and essential for epithelial-mesenchymal transition. J. Biol. Chem. 288, 2179-2189, doi: 10.1074/jbc.M112.432716 (2013).
29. Sing, A. et al. The atypical cadherin fat directly regulates mitochondrial function and metabolic state. Cell 158, 1293-1308, doi: 10.1016/j.cell.2014.07.036 (2014).
30. Roura, S., Miravet, S., Piedra, J., Garcia de Herreros, A. & Dunach, M. Regulation of E-cadherin/Catenin association by tyrosine phosphorylation. J. Biol. Chem. 274, 36734-36740 (1999).
31. Piedra, J. et al. p120 Catenin-associated Fer and Fyn tyrosine kinases regulate beta-catenin Tyr-142 phosphorylation and betacatenin- alpha-catenin Interaction. Mol. Cell. Biol. 23, 2287-2297 (2003).
32. Volberg, T. et al. The effect of tyrosine-specific protein phosphorylation on the assembly of adherens-type junctions. EMBO J. 11, 1733-1742 (1992).
33. Lilien, J. & Balsamo, J. The regulation of cadherin-mediated adhesion by tyrosine phosphorylation/dephosphorylation of betacatenin. Curr. Opin. Cell Biol. 17, 459-465, doi: 10.1016/j.ceb.2005.08.009 (2005).
34. Agarwal, R., Burley, S. K. & Swaminathan, S. Structure of human dual specificity protein phosphatase 23, VHZ, enzyme-substrate/ product complex. J. Biol. Chem. 283, 8946-8953, doi: doi: 10.1074/jbc.M708945200 (2008).
35. Wu, Q. et al. Molecular cloning and characterization of a novel dual-specificity phosphatase 23 gene from human fetal brain. Int. J. Biochem. Cell Biol. 36, 1542-1553, doi: 10.1016/j.biocel.2003.12.014 (2004).
36. Tominaga, J., Fukunaga, Y., Abelardo, E. & Nagafuchi, A. Defining the function of beta-catenin tyrosine phosphorylation in cadherin-mediated cell-cell adhesion. Genes Cells. 13, 67-77, doi: 10.1111/j.1365-2443.2007.01149.x (2008).
37. Vasioukhin, V., Bauer, C., Yin, M. & Fuchs, E. Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100, 209-219 (2000).
38. Ng, M. R., Besser, A., Danuser, G. & Brugge, J. S. Substrate stiffness regulates cadherin-dependent collective migration through myosin-II contractility. J. Cell Biol. 199, 545-563, doi: 10.1083/jcb.201207148 (2012).
39. Brembeck, F. H. et al. Essential role of BCL9-2 in the switch between beta-catenin's adhesive and transcriptional functions. Genes Dev. 18, 2225-2230, doi: 10.1101/gad.317604 (2004).
40. Berx, G. & van Roy, F. Involvement of members of the cadherin superfamily in cancer. Cold Spring Harb. Perspect. Biol. 1, a003129, doi: 10.1101/cshperspect.a003129 (2009).
41. Jeanes, A., Gottardi, C. J. & Yap, A. S. Cadherins and cancer: how does cadherin dysfunction promote tumor progression? Oncogene 27, 6920-6929, doi: 10.1038/onc.2008.343 (2008).
42. Leung, C. T. & Brugge, J. S. Outgrowth of single oncogene-expressing cells from suppressive epithelial environments. Nature 482, 410-413, doi: 10.1038/nature10826 (2012).
43. Eng, J. K., McCormack, A. L. & Yates, J. R. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Amer. Soc. Mass Spectrom. 5, 976-989, doi: 10.1016/1044-0305(94)80016-2 (1994).
44. Higgins, J. M. et al. Direct and regulated interaction of integrin alphaEbeta7 with E-cadherin. J. Cell Biol. 140, 197-210 (1998).