Adherens junctions connect the actin cytoskeleton of neighboring cells through transmembrane cadherin receptors and a network of adaptor proteins. The interactions between these adaptors and cadherin as well as the activity of actin regulators localized to adherens junctions are tightly controlled to facilitate cell junction assembly or disassembly in response to changes in external or internal forces and/or signaling. Phosphorylation of tyrosine, serine, or threonine residues acts as a switch on the majority of adherens junction proteins, turning “on” or “off” their interactions with other proteins and/or their enzymatic activity. Here, we provide an overview of the kinases and phosphatases regulating phosphorylation of adherens junction proteins and bring examples of phosphorylation events leading to the assembly or disassembly of adherens junctions, highlighting the important role of phosphorylation switches in regulating their dynamics. 1. Introduction Adherens junctions (AJs) are cell-cell adhesion sites where calcium-dependent cadherin receptors bind with their extracellular domains to cadherins on opposing cells and with their cytoplasmic tails connect—via adaptors—to filamentous actin [1, 2]. By essentially providing a physical link between the actin cytoskeleton of neighboring cells AJs facilitate the integration of individual cells into a tissue. Additionally, AJs are instrumental in setting up and maintaining the apicobasal polarity of epithelial cells [3, 4], they function as mechanosensors [5] and serve as a nexus for signaling affecting important cell decisions, such as survival and differentiation [6]. During the development and lifetime of an organism, cells frequently change shape and position relative to their neighbors. Hence, the ability of cells to regulate their adhesive interactions plays a key role during tissue morphogenesis, repair, and renewal [3, 7, 8]. Defects in the adhesive characteristics of epithelial cells are pathological signs and loss of cell-cell adhesion can generate dedifferentiation and invasiveness of human carcinoma cells [9]. Thus, there is great interest in understanding the factors that affect assembly and disassembly of cell-cell adhesion at the molecular level. When considering regulatory mechanisms controlling AJ proteins, we distinguish between three subsequent steps of regulation: synthesis, localization, and activation. First, a cell controls whether proteins are synthesized or not. Indeed, transcriptional regulation of E-cadherin, notably by the snail transcription factor, plays an important role in
References
[1]
K. J. Green, S. Getsios, S. Troyanovsky, and L. M. Godsel, “Intercellular junction assembly, dynamics, and homeostasis,” Cold Spring Harbor Perspectives in Biology, vol. 2, no. 2, p. a000125, 2010.
[2]
M. Takeichi, “Cadherin cell adhesion receptors as a morphogenetic regulator,” Science, vol. 251, no. 5000, pp. 1451–1455, 1991.
[3]
B. Baum and M. Georgiou, “Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling,” Journal of Cell Biology, vol. 192, no. 6, pp. 907–917, 2011.
[4]
D. St Johnston and B. Sanson, “Epithelial polarity and morphogenesis,” Current Opinion in Cell Biology, vol. 23, no. 5, pp. 540–546, 2011.
[5]
S. Yonemura, Y. Wada, T. Watanabe, A. Nagafuchi, and M. Shibata, “α-Catenin as a tension transducer that induces adherens junction development,” Nature Cell Biology, vol. 12, no. 6, pp. 533–542, 2010.
[6]
T. Lecuit, “Adhesion remodeling underlying tissue morphogenesis,” Trends in Cell Biology, vol. 15, no. 1, pp. 34–42, 2005.
[7]
T. J. C. Harris, “Adherens junction assembly and function in the Drosophila embryo,” International Review of Cell and Molecular Biology, vol. 293, pp. 45–83, 2012.
[8]
A. M. Lynch and J. Hardin, “The assembly and maintenance of epithelial junctions in C. Elegans,” Frontiers in Bioscience, vol. 14, no. 4, pp. 1414–1432, 2009.
[9]
U. H. Frixen, J. Behrens, M. Sachs et al., “E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells,” Journal of Cell Biology, vol. 113, no. 1, pp. 173–185, 1991.
[10]
J. Yoshino, T. Monkawa, M. Tsuji, M. Inukai, H. Itoh, and M. Hayashi, “Snail1 is involved in the renal epithelial-mesenchymal transition,” Biochemical and Biophysical Research Communications, vol. 362, no. 1, pp. 63–68, 2007.
[11]
R. S. B. Clark, H. Bayir, and L. W. Jenkins, “Posttranslational protein modifications,” Critical Care Medicine, vol. 33, no. 12, pp. S407–S409, 2005.
[12]
S. Roura, S. Miravet, J. Piedra, A. García De Herreros, and M. Du？achl, “Regulation of E-cadherin/catenin association by tyrosine phosphorylation,” Journal of Biological Chemistry, vol. 274, no. 51, pp. 36734–36740, 1999.
[13]
R. Michalides, T. Volberg, and B. Geiger, “Augmentation of adherens junction formation in mesenchymal cells by co-expression of N-CAM or short-term stimulation of tyrosine-phosphorylation,” Cell Adhesion and Communication, vol. 2, no. 6, pp. 481–490, 1994.
[14]
V. G. Brunton, I. R. J. MacPherson, and M. C. Frame, “Cell adhesion receptors, tyrosine kinases and actin modulators: a complex three-way circuitry,” Biochimica et Biophysica Acta, vol. 1692, no. 2-3, pp. 121–144, 2004.
[15]
J. M. Daniel and A. B. Reynolds, “Tyrosine phosphorylation and cadherin/catenin function,” BioEssays, vol. 19, no. 10, pp. 883–891, 1997.
[16]
J. Lilien and J. Balsamo, “The regulation of cadherin-mediated adhesion by tyrosine phosphorylation/dephosphorylation of β-catenin,” Current Opinion in Cell Biology, vol. 17, no. 5, pp. 459–465, 2005.
[17]
T. J. C. Harris and M. Peifer, “Decisions, decisions: β-catenin chooses between adhesion and transcription,” Trends in Cell Biology, vol. 15, no. 5, pp. 234–237, 2005.
[18]
M.-H. Park, D.-J. Kim, S.-T. You et al., “Phosphorylation of β-catenin at serine 663 regulates its transcriptional activity,” Biochemical and Biophysical Research Communications, vol. 419, no. 3, pp. 543–549, 2012.
[19]
J. Balsamo, T. Leung, H. Ernst, M. K. B. Zanin, S. Hoffman, and J. Lilien, “Regulated binding of a PTP1B-like phosphatase to N-cadherin: control of cadherin-mediated adhesion by dephosphorylation of β-catenin,” Journal of Cell Biology, vol. 134, no. 3, pp. 801–813, 1996.
[20]
S. Tsukita, K. Oishi, T. Akiyama, Y. Yamanashi, T. Yamamoto, and S. Tsukita, “Specific proto-oncogenic tyrosine kinases of src family are enriched in cell-to-cell adherens junctions where the level of tyrosine phosphorylation is elevated,” Journal of Cell Biology, vol. 113, no. 4, pp. 867–879, 1991.
[21]
A. L. Smith, M. R. Dohn, M. V. Brown, and A. B. Reynolds, “Association of Rho-associated protein kinase 1 with E-cadherin complexes is mediated by p120-catenin,” Molecular Biology of the Cell, vol. 23, no. 1, pp. 99–110, 2012.
[22]
J. Jiang, D. Dean, R. C. Burghardt, and A. R. Parrish, “Disruption of cadherin/catenin expression, localization, and interactions during HgCl2-induced nephrotoxicity,” Toxicological Sciences, vol. 80, no. 1, pp. 170–182, 2004.
[23]
N. P. Y. Lee and C. Y. Cheng, “Protein kinases and adherens junction dynamics in the seminiferous epithelium of the rat testis,” Journal of Cellular Physiology, vol. 202, no. 2, pp. 344–360, 2005.
[24]
U. Baumeister, R. Funke, K. Ebnet, H. Vorschmitt, S. Koch, and D. Vestweber, “Association of Csk to VE-cadherin and inhibition of cell proliferation,” EMBO Journal, vol. 24, no. 9, pp. 1686–1695, 2005.
[25]
P. Sheth, A. Seth, K. J. Atkinson et al., “Acetaldehyde dissociates the PTP1B-E-cadherin-β-catenin complex in Caco-2 cell monolayers by a phosphorylation-dependent mechanism,” Biochemical Journal, vol. 402, no. 2, pp. 291–300, 2007.
[26]
S. P. S. Monga, W. M. Mars, P. Pediaditakis et al., “Hepatocyte growth factor induces Wnt-independent nuclear translocation of β-catenin after Met-β-catenin dissociation in hepatocytes,” Cancer Research, vol. 62, no. 7, pp. 2064–2071, 2002.
[27]
B. Aicher, M. M. Lerch, T. Müller, J. Schilling, and A. Ullrich, “Cellular redistribution of protein tyrosine phosphatases LAR and PTPσ by inducible proteolytic processing,” Journal of Cell Biology, vol. 138, no. 3, pp. 681–696, 1997.
[28]
W. H. Ziegler, U. Tigges, A. Zieseniss, and B. M. Jockusch, “A lipid-regulated docking site on vinculin for protein kinase C,” Journal of Biological Chemistry, vol. 277, no. 9, pp. 7396–7404, 2002.
[29]
T. Nishimura and M. Takeichi, “Shroom3-mediated recruitment of Rho kinases to the apical cell junctions regulates epithelial and neuroepithelial planar remodeling,” Development, vol. 135, no. 8, pp. 1493–1502, 2008.
[30]
M. Shindo, H. Wada, M. Kaido et al., “Dual function of Src in the maintenance of adherens junctions during tracheal epithelial morphogenesis,” Development, vol. 135, no. 7, pp. 1355–1364, 2008.
[31]
D. W. Owens, G. W. McLean, A. W. Wyke et al., “The catalytic activity of the Src family kinases is required to disrupt cadherin-dependent cell-cell contacts,” Molecular Biology of the Cell, vol. 11, no. 1, pp. 51–64, 2000.
[32]
H. Jin, B. Garmy-Susini, C. J. Avraamides, K. Stoletov, R. L. Klemke, and J. A. Varner, “A PKA-Csk-pp60Src signaling pathway regulates the switch between endothelial cell invasion and cell-cell adhesion during vascular sprouting,” Blood, vol. 116, no. 25, pp. 5773–5783, 2010.
[33]
W. Rengifo-Cam, A. Konishi, N. Morishita et al., “Csk defines the ability of integrin-mediated cell adhesion and migration in human colon cancer cells: implication for a potential role in cancer metastasis,” Oncogene, vol. 23, no. 1, pp. 289–297, 2004.
[34]
J. Piedra, S. Miravet, J. Casta？o et al., “p120 catenin-associated Fer and Fyn tyrosine kinases regulate β-catenin Tyr-142 phosphorylation and β-catenin-α-catenin interaction,” Molecular and Cellular Biology, vol. 23, no. 7, pp. 2287–2297, 2003.
[35]
R. Y. J. Huang, S. M. Wang, C. Y. Hsieh, and J. C. Wu, “Lysophosphatidic acid induces ovarian cancer cell dispersal by activating Fyn kinase associated with p120-catenin,” International Journal of Cancer, vol. 123, no. 4, pp. 801–809, 2008.
[36]
K. L. Hsu, H. J. Fan, Y. C. Chen et al., “Protein kinase C-Fyn kinase cascade mediates the oleic acid-induced disassembly of neonatal rat cardiomyocyte adherens junctions,” International Journal of Biochemistry and Cell Biology, vol. 41, no. 7, pp. 1536–1546, 2009.
[37]
N. L. Zandy, M. Playford, and A. M. Pendergast, “Abl tyrosine kinases regulate cell- cell adhesion through Rho GTPases,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 45, pp. 17686–17691, 2007.
[38]
E. E. Grevengoed, J. J. Loureiro, T. L. Jesse, and M. Peifer, “Abelson kinase regulates epithelial morphogenesis in Drosophila,” Journal of Cell Biology, vol. 155, no. 7, pp. 1185–1197, 2001.
[39]
R. M. Larive, S. Urbach, J. Poncet et al., “Phosphoproteomic analysis of Syk kinase signaling in human cancer cells reveals its role in cell-cell adhesion,” Oncogene, vol. 28, no. 24, pp. 2337–2347, 2009.
[40]
X. Zhang, U. Shrikhande, B. M. Alicie, Q. Zhou, and R. L. Geahlen, “Role of the protein tyrosine kinase Syk in regulating cell-cell adhesion and motility in breast cancer cells,” Molecular Cancer Research, vol. 7, no. 5, pp. 634–644, 2009.
[41]
J. D. Van Buul, E. C. Anthony, M. Fernandez-Borja, K. Burridge, and P. L. Hordijk, “Proline-rich tyrosine kinase 2 (Pyk2) mediates vascular endothelial-cadherin-based cell-cell adhesion by regulating β-catenin tyrosine phosphorylation,” Journal of Biological Chemistry, vol. 280, no. 22, pp. 21129–21136, 2005.
[42]
F. De Amicis, M. Lanzino, A. Kisslinger et al., “Loss of proline-rich tyrosine kinase 2 function induces spreading and motility of epithelial prostate cells,” Journal of Cellular Physiology, vol. 209, no. 1, pp. 74–80, 2006.
[43]
R. J. Cain, B. Vanhaesebroeck, and A. J. Ridley, “The PI3K p110α isoform regulates endothelial adherens junctions via Pyk2 and Rac1,” Journal of Cell Biology, vol. 188, no. 6, pp. 863–876, 2010.
[44]
R. Rosato, J. M. Veltmaat, J. Groffen, and N. Heisterkamp, “Involvement of the tyrosine kinase Fer in cell adhesion,” Molecular and Cellular Biology, vol. 18, no. 10, pp. 5762–5770, 1998.
[45]
H. Hoschuetzky, H. Aberle, and R. Kemler, “β-Catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor,” Journal of Cell Biology, vol. 127, no. 5, pp. 1375–1380, 1994.
[46]
G. Davies, W. G. Jiang, and M. D. Mason, “HGF/SF modifies the interaction between its receptor c-Met, and the E-cadherin/catenin complex in prostate cancer cells,” International Journal of Molecular Medicine, vol. 7, no. 4, pp. 385–388, 2001.
[47]
C. L. Williams and J. D. Noti, “Reduced expression of Wnt-1 and E-cadherin, and diminished beta-catenin stability in MCF-7 breast cancer cells that overexpress protein kinase C-alpha,” International Journal of Oncology, vol. 19, no. 6, pp. 1227–1233, 2001.
[48]
M. J. Boucher, P. Laprise, and N. Rivard, “Cyclic AMP-dependent protein kinase A negatively modulates adherens junction integrity and differentiation of intestinal epithelial cells,” Journal of Cellular Physiology, vol. 202, no. 1, pp. 178–190, 2005.
[49]
F. Leve, W. De Souza, and J. A. Morgado-Díaz, “A cross-link between protein kinase A and Rho-family GTPases signaling mediates cell-cell adhesion and actin cytoskeleton organization in epithelial cancer cells,” Journal of Pharmacology and Experimental Therapeutics, vol. 327, no. 3, pp. 777–788, 2008.
[50]
K. Taguchi, T. Ishiuchi, and M. Takeichi, “Mechanosensitive EPLIN-dependent remodeling of adherens junctions regulates epithelial reshaping,” Journal of Cell Biology, vol. 194, no. 4, pp. 643–656, 2011.
[51]
C. L. Chen and H. C. Chen, “Functional suppression of E-cadherin by protein kinase Cδ,” Journal of Cell Science, vol. 122, no. 4, pp. 513–523, 2009.
[52]
R. Singh, P. Lei, and S. T. Andreadis, “PKC-δ binds to E-cadherin and mediates EGF-induced cell scattering,” Experimental Cell Research, vol. 315, no. 17, pp. 2899–2913, 2009.
[53]
D. Casagolda, B. Del Valle-Pérez, G. Valls et al., “A p120-catenin-CK1ε complex regulates Wnt signaling,” Journal of Cell Science, vol. 123, no. 15, pp. 2621–2631, 2010.
[54]
H. Lickert, A. Bauer, R. Kemler, and J. Stappert, “Casein kinase II phosphorylation of E-cadherin increases E-cadherin/β- catenin interaction and strengthens cell-cell adhesion,” Journal of Biological Chemistry, vol. 275, no. 7, pp. 5090–5095, 2000.
[55]
C. Pirraglia, J. Walters, and M. M. Myat, “Pak1 control of E-cadherin endocytosis regulates salivary gland lumen size and shape,” Development, vol. 137, no. 24, pp. 4177–4189, 2010.
[56]
S. Elloul, O. Vaksman, H. T. Stavnes, C. G. Trope, B. Davidson, and R. Reich, “Mesenchymal-to-epithelial transition determinants as characteristics of ovarian carcinoma effusions,” Clinical and Experimental Metastasis, vol. 27, no. 3, pp. 161–172, 2010.
[57]
H. He, A. Shulkes, and G. S. Baldwin, “PAK1 interacts with β-catenin and is required for the regulation of the β-catenin signalling pathway by gastrins,” Biochimica et Biophysica Acta, vol. 1783, no. 10, pp. 1943–1954, 2008.
[58]
M. H. Lee, P. Koria, J. Qu, and S. T. Andreadis, “JNK phosphorylates β-catenin and regulates adherens junctions,” FASEB Journal, vol. 23, no. 11, pp. 3874–3883, 2009.
[59]
M. Jaggi, P. S. Rao, D. J. Smith et al., “E-cadherin phosphorylation by protein kinase D1/protein kinase Cμ is associated with altered cellular aggregation and motility in prostate cancer,” Cancer Research, vol. 65, no. 2, pp. 483–492, 2005.
[60]
A. Suzuki, T. Yamanaka, T. Hirose et al., “Atypical protein kinase C is involved in the evolutionarily conserved PAR protein complex and plays a critical role in establishing epithelia-specific junctional structures,” Journal of Cell Biology, vol. 152, no. 6, pp. 1183–1196, 2001.
[61]
M. Elbert, D. Cohen, and A. Müsch, “PAR1b promotes cell-cell adhesion and inhibits dishevelled-mediated transformation of Madin-Darby canine kidney cells,” Molecular Biology of the Cell, vol. 17, no. 8, pp. 3345–3355, 2006.
[62]
J. Balsamo, C. Arregui, T. Leung, and J. Lilien, “The nonreceptor protein tyrosine phosphatase PTP1B binds to the cytoplasmic domain of N-cadherin and regulates the cadherin-actin linkage,” Journal of Cell Biology, vol. 143, no. 2, pp. 523–532, 1998.
[63]
P. Pathre, C. Arregui, T. Wampler et al., “PTP1B regulates neurite extension mediated by cell-cell and cell-matrix adhesion molecules,” Journal of Neuroscience Research, vol. 63, no. 2, pp. 143–150, 2001.
[64]
M. V. Hernández, D. P. Wehrendt, and C. O. Arregui, “The protein tyrosine phosphatase PTP1B is required for efficient delivery of N-cadherin to the cell surface,” Molecular Biology of the Cell, vol. 21, no. 8, pp. 1387–1397, 2010.
[65]
J. Schnekenburger, J. Mayerle, B. Krüger et al., “Protein tyrosine phosphatase κ and SHP-1 are involved in the regulation of cell-cell contacts at adherens junctions in the exocrine pancreas,” Gut, vol. 54, no. 10, pp. 1445–1455, 2005.
[66]
J. A. Ukropec, M. K. Hollinger, S. M. Salva, and M. J. Woolkalis, “SHP2 association with VE-cadherin complexes in human endothelial cells is regulated by thrombin,” Journal of Biological Chemistry, vol. 275, no. 8, pp. 5983–5986, 2000.
[67]
R. Espejo, W. Rengifo-Cam, M. D. Schaller, B. M. Evers, and S. K. Sastry, “PTP-PEST controls motility, adherens junction assembly, and Rho GTPase activity in colon cancer cells,” American Journal of Physiology, vol. 299, no. 2, pp. C454–C463, 2010.
[68]
C. Wadham, J. R. Gamble, M. A. Vadas, and Y. Khew-Goodall, “The protein tyrosine phosphatase Pez is a major phosphatase of adherens junctions and dephosphorylates β-catenin,” Molecular Biology of the Cell, vol. 14, no. 6, pp. 2520–2529, 2003.
[69]
M. L. Taddei, P. Chiarugi, P. Cirri et al., “β-catenin interacts with low-molecular-weight protein tyrosine phosphatase leading to cadherin-mediated cell-cell adhesion increase,” Cancer Research, vol. 62, no. 22, pp. 6489–6499, 2002.
[70]
W. B. Fang, R. C. Ireton, G. Zhuang, T. Takahashi, A. Reynolds, and J. Chen, “Overexpression of EPHA2 receptor destabilizes adherens junctions via a RhoA-dependent mechanism,” Journal of Cell Science, vol. 121, no. 3, pp. 358–368, 2008.
[71]
L. J. Holsinger, K. Ward, B. Duffield, J. Zachwieja, and B. Jallal, “The transmembrane receptor protein tyrosine phosphatase DEP1 interacts with p120ctn,” Oncogene, vol. 21, no. 46, pp. 7067–7076, 2002.
[72]
G. C. M. Zondag, A. B. Reynolds, and W. H. Moolenaar, “Receptor protein-tyrosine phosphatase RPTPμ binds to and dephosphorylates the catenin p120(ctn),” Journal of Biological Chemistry, vol. 275, no. 15, pp. 11264–11269, 2000.
[73]
S. M. Brady-Kalnay, T. Mourton, J. P. Nixon et al., “Dynamic interactions of PTPμ with multiple cadherins in vivo,” Journal of Cell Biology, vol. 141, no. 1, pp. 287–296, 1998.
[74]
S. Hiscox and W. G. Jiang, “Association of PTPμ with catenins in cancer cells: a possible role for E-cadherin,” International Journal of Oncology, vol. 13, no. 5, pp. 1077–1080, 1998.
[75]
J. A. Besco, R. Hooft van Huijsduijnen, A. Frostholm, and A. Rotter, “Intracellular substrates of brain-enriched receptor protein tyrosine phosphatase rho (RPTPρ/PTPRT),” Brain Research, vol. 1116, no. 1, pp. 50–57, 2006.
[76]
H. X. Yan, Y. Q. He, H. Dong et al., “Physical and functional interaction between receptor-like protein tyrosine phosphatase PCP-2 and β-catenin,” Biochemistry, vol. 41, no. 52, pp. 15854–15860, 2002.
[77]
H. X. Yan, W. Yang, R. Zhang et al., “Protein-tyrosine phosphatase PCP-2 inhibits β-catenin signaling and increases E-cadherin-dependent cell adhesion,” Journal of Biological Chemistry, vol. 281, no. 22, pp. 15423–15433, 2006.
[78]
L. Novellino, A. De Filippo, P. Deho et al., “PTPRK negatively regulates transcriptional activity of wild type and mutated oncogenic β-catenin and affects membrane distribution of β-catenin/E-cadherin complexes in cancer cells,” Cellular Signalling, vol. 20, no. 5, pp. 872–883, 2008.
[79]
C. Wang, Z. Li, Z. Yang et al., “The effect of receptor protein tyrosine phosphatase kappa on the change of cell adhesion and proliferation induced by N-acetylglucosaminyltransferase V,” Journal of Cellular Biochemistry, vol. 109, no. 1, pp. 113–123, 2010.
[80]
R. M. Kypta, H. Su, and L. F. Reichardt, “Association between a transmembrane protein tyrosine phosphatase and the cadherin-catenin complex,” Journal of Cell Biology, vol. 134, no. 6, pp. 1519–1529, 1996.
[81]
J. R. Symons, C. M. Levea, and R. A. Mooney, “Expression of the leucocyte common antigen-related (LAR) tyrosine phosphatase is regulated by cell density through functional E-cadherin complexes,” Biochemical Journal, vol. 365, no. 2, pp. 513–519, 2002.
[82]
T. Müller, A. Choidas, E. Reichmann, and A. Ullrich, “Phosphorylation and free pool of β-catenin are regulated by tyrosine kinases and tyrosine phosphatases during epithelial cell migration,” Journal of Biological Chemistry, vol. 274, no. 15, pp. 10173–10183, 1999.
[83]
M. Nita-Lazar, I. Rebustini, J. Walker, and M. A. Kukuruzinska, “Hypoglycosylated E-cadherin promotes the assembly of tight junctions through the recruitment of PP2A to adherens junctions,” Experimental Cell Research, vol. 316, no. 11, pp. 1871–1884, 2010.
[84]
K. Suzuki and K. Takahashi, “Induction of E-cadherin endocytosis by loss of protein phosphatase 2A expression in human breast cancers,” Biochemical and Biophysical Research Communications, vol. 349, no. 1, pp. 255–260, 2006.
[85]
J. G？tz, A. Probst, C. Mistl, R. M. Nitsch, and E. Ehler, “Distinct role of protein phosphatase 2A subunit Cα in the regulation of E-cadherin and β-catenin during development,” Mechanisms of Development, vol. 93, no. 1-2, pp. 83–93, 2000.
[86]
S. Dupre-Crochet, A. Figueroa, C. Hogan et al., “Casein kinase 1 is a novel negative regulator of E-cadherin-based cell-cell contacts,” Molecular and Cellular Biology, vol. 27, no. 10, pp. 3804–3816, 2007.
[87]
J. Qi, J. Wang, O. Romanyuk, and C. H. Siu, “Involvement of Src family kinases in N-cadherin phosphorylation and β-catenin dissociation during transendothelial migration of melanoma cells,” Molecular Biology of the Cell, vol. 17, no. 3, pp. 1261–1272, 2006.
[88]
M. Kikyo, T. Matozaki, A. Kodama, H. Kawabe, H. Nakanishi, and Y. Takai, “Cell-cell adhesion-mediated tyrosine phosphorylation of nectin-2δ, an immunoglobulin-like cell adhesion molecule at adherens junctions,” Oncogene, vol. 19, no. 35, pp. 4022–4028, 2000.
[89]
M. Serres, C. Grangeasse, M. Haftek, Y. Durocher, B. Duclos, and D. Schmitt, “Hyperphosphorylation of β-catenin on serine-threonine residues and loss of cell-cell contacts induced by calyculin A and okadaic acid in human epidermal cells,” Experimental Cell Research, vol. 231, no. 1, pp. 163–172, 1997.
[90]
H. S. Moon, E. A. Choi, H. Y. Park et al., “Expression and tyrosine phosphorylation of E-cadherin, β- and γ-catenin, and epidermal growth factor receptor in cervical cancer cells,” Gynecologic Oncology, vol. 81, no. 3, pp. 355–359, 2001.
[91]
L. Heiska and O. Carpén, “Src phosphorylates ezrin at tyrosine 477 and induces a phosphospecific association between ezrin and a kelch-repeat protein family member,” Journal of Biological Chemistry, vol. 280, no. 11, pp. 10244–10252, 2005.
[92]
R. Zhou, X. Cao, C. Watson et al., “Characterization of protein kinase A-mediated phosphorylation of ezrin in gastric parietal cell activation,” Journal of Biological Chemistry, vol. 278, no. 37, pp. 35651–35659, 2003.
[93]
J. Chen, J. A. Cohn, and L. J. Mandel, “Dephosphorylation of ezrin as an early event in renal microvillar breakdown and anoxic injury,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 16, pp. 7495–7499, 1995.
[94]
D. J. Mariner, P. Anastasiadis, H. Keilhack, F. D. B？hmer, J. Wang, and A. B. Reynolds, “Identification of Src phosphorylation sites in the catenin p120 ctn,” Journal of Biological Chemistry, vol. 276, no. 30, pp. 28006–28013, 2001.
[95]
S. Alemà and A. M. Salvatore, “p120 catenin and phosphorylation: mechanisms and traits of an unresolved issue,” Biochimica et Biophysica Acta, vol. 1773, no. 1, pp. 47–58, 2007.
[96]
S. Miravet, J. Piedra, J. Casta？o et al., “Tyrosine phosphorylation of plakoglobin causes contrary effects on its association with desmosomes and adherens junction components and modulates β-catenin-mediated transcription,” Molecular and Cellular Biology, vol. 23, no. 20, pp. 7391–7402, 2003.
[97]
Y. Wang, D. Du, L. Fang et al., “Tyrosine phosphorylated Par3 regulates epithelial tight junction assembly promoted by EGFR signaling,” EMBO Journal, vol. 25, no. 21, pp. 5058–5070, 2006.
[98]
A. Traweger, G. Wiggin, L. Taylor, S. A. Tate, P. Metalnikov, and T. Pawson, “Protein phosphatase 1 regulates the phosphorylation state of the polarity scaffold Par-3,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 30, pp. 10402–10407, 2008.
[99]
J. Burks and Y. M. Agazie, “Modulation of α-catenin Tyr phosphorylation by SHP2 positively effects cell transformation induced by the constitutively active FGFR3,” Oncogene, vol. 25, no. 54, pp. 7166–7179, 2006.
[100]
H. Ji, J. Wang, H. Nika et al., “EGF-Induced ERK activation promotes CK2-mediated disassociation of α-catenin from β-catenin and transactivation of β-catenin,” Molecular Cell, vol. 36, no. 4, pp. 547–559, 2009.
[101]
S. Nakajo, K. Nakaya, and Y. Nakamura, “Phosphorylation of actin-binding proteins by casein kinases 1 and 2,” Biochemistry International, vol. 15, no. 2, pp. 321–327, 1987.
[102]
Z. Zhang, G. Izaguirre, S. Y. Lin, H. Y. Lee, E. Schaefer, and B. Haimovich, “The phosphorylation of vinculin on tyrosine residues 100 and 1065, mediated by Src kinases, affects cell spreading,” Molecular Biology of the Cell, vol. 15, no. 9, pp. 4234–4247, 2004.
[103]
M. Y. Han, H. Kosako, T. Watanabe, and S. Hattori, “Extracellular signal-regulated kinase/mitogen-activated protein kinase regulates actin organization and cell motility by phosphorylating the actin cross-linking protein EPLIN,” Molecular and Cellular Biology, vol. 27, no. 23, pp. 8190–8204, 2007.
[104]
M. Maruoka, M. Sato, Y. Yuan et al., “Abi-1-bridged tyrosine phosphorylation of VASP by Abelson kinase impairs association of VASP to focal adhesions and regulates leukaemic cell adhesion,” Biochemical Journal, vol. 441, no. 3, pp. 889–899, 2012.
[105]
D. M. Thomson, M. P. A. Ascione, J. Grange, C. Nelson, and M. D. H. Hansen, “Phosphorylation of VASP by AMPK alters actin binding and occurs at a novel site,” Biochemical and Biophysical Research Communications, vol. 414, no. 1, pp. 215–219, 2011.
[106]
A. Deguchi, J. W. Soh, H. Li, R. Pamukcu, W. J. Thompson, and I. B. Weinstein, “Vasodilator-stimulated phosphoprotein (VASP) phosphorylation provides a biomarker for the action of exisulind and related agents that activate protein kinase G.,” Molecular cancer therapeutics, vol. 1, no. 10, pp. 803–809, 2002.
[107]
S. F. Walk, M. E. March, and K. S. Ravichandran, “Roles of Lck, Syk and ZAP-70 tyrosine kinases in TCR-mediated phosphorylation of the adapter protein Shc,” European Journal of Immunology, vol. 28, no. 8, pp. 2265–2275, 1998.
[108]
P. Van Der Geer, S. Wiley, G. D. Gish, and T. Pawson, “The Shc adaptor protein is highly phosphorylated at conserved, twin tyrosine residues (Y239/240) that mediate protein-protein interactions,” Current Biology, vol. 6, no. 11, pp. 1435–1444, 1996.
[109]
M. Gr？nborg, T. Z. Kristiansen, A. Stensballe et al., “A mass spectrometry-based proteomic approach for identification of serine/threonine-phosphorylated proteins by enrichment with phospho-specific antibodies: identification of a novel protein, Frigg, as a protein kinase A substrate,” Molecular & Cellular Proteomics, vol. 1, no. 7, pp. 517–527, 2002.
[110]
H. Shao, C. Wu, and A. Wells, “Phosphorylation of α-actinin 4 upon epidermal growth factor exposure regulates its interaction with actin,” Journal of Biological Chemistry, vol. 285, no. 4, pp. 2591–2600, 2010.
[111]
W. Sangrar, Y. Gao, M. Scott, P. Truesdell, and P. A. Greer, “Fer-mediated cortactin phosphorylation is associated with efficient fibroblast migration and is dependent on reactive oxygen species generation during integrin-mediated cell adhesion,” Molecular and Cellular Biology, vol. 27, no. 17, pp. 6140–6152, 2007.
[112]
A. Grassart, V. Meas-Yedid, A. Dufour, J. C. Olivo-Marin, A. Dautry-Varsat, and N. Sauvonnet, “Pak1 phosphorylation enhances cortactin-N-WASP interaction in clathrin-caveolin-independent endocytosis,” Traffic, vol. 11, no. 8, pp. 1079–1091, 2010.
[113]
S. Van Delft, A. J. Verkleij, and J. Boonstra, “Epidermal growth factor induces serine phosphorylation of actin,” FEBS Letters, vol. 357, no. 3, pp. 251–254, 1995.
[114]
E. A. Papakonstanti and C. Stournaras, “Association of PI-3 kinase with PAK1 leads to actin phosphorylation and cytoskeletal reorganization,” Molecular Biology of the Cell, vol. 13, no. 8, pp. 2946–2962, 2002.
[115]
X. Liu, S. Shu, M. S. S. Hong, R. L. Levine, and E. D. Korn, “Phosphorylation of actin Tyr-53 inhibits filament nucleation and elongation and destabilizes filaments,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 37, pp. 13694–13699, 2006.
[116]
A. Arcaro, M. Aubert, M. E. Espinosa del Hierro et al., “Critical role for lipid raft-associated Src kinases in activation of PI3K-Akt signalling,” Cellular Signalling, vol. 19, no. 5, pp. 1081–1092, 2007.
[117]
A. Mitra and V. Radha, “F-actin-binding domain of c-Abl regulates localized phosphorylation of C3G: role of C3G in c-Abl-mediated cell death,” Oncogene, vol. 29, no. 32, pp. 4528–4542, 2010.
[118]
R. M. Wolf, J. J. Wilkes, M. V. Chao, and M. D. Resh, “Tyrosine phosphorylation of p190 RhoGAP by Fyn regulates oligodendrocyte differentiation,” Journal of Neurobiology, vol. 49, no. 1, pp. 62–78, 2001.
[119]
R. W. Roof, M. D. Haskell, B. D. Dukes, N. Sherman, M. Kinter, and S. J. Parsons, “Phosphotyrosine (p-Tyr)-dependent and -independent mechanisms of p190 RhoGAP-p120 RasGAP interaction: Tyr 1105 of p190, a substrate for c-Src, is the sole p-Tyr mediator of complex formation,” Molecular and Cellular Biology, vol. 18, no. 12, pp. 7052–7063, 1998.
[120]
S. Taniguchi, H. Liu, T. Nakazawa, K. Yokoyama, T. Tezuka, and T. Yamamoto, “p250GAP, a neural RhoGAP protein, is associated with and phosphorylated by Fyn,” Biochemical and Biophysical Research Communications, vol. 306, no. 1, pp. 151–155, 2003.
[121]
S. Y. Moon, H. Zang, and Y. Zheng, “Characterization of a brain-specific Rho GTPase-activating protein, p200RhoGAP,” Journal of Biological Chemistry, vol. 278, no. 6, pp. 4151–4159, 2003.
[122]
J. M. Servitja, M. J. Marinissen, A. Sodhi, X. R. Bustelo, and J. S. Gutkind, “Rac1 function is required for Src-induced transformation: evidence of a role for Tiam1 and Vav2 in Rac activation by Src,” Journal of Biological Chemistry, vol. 278, no. 36, pp. 34339–34346, 2003.
[123]
S. K. Sastry, Z. Rajfur, B. P. Liu, J. F. Cote, M. L. Tremblay, and K. Burridge, “PTP-PEST couples membrane protrusion and tail retraction via VAV2 and p190RhoGAP,” Journal of Biological Chemistry, vol. 281, no. 17, pp. 11627–11636, 2006.
[124]
S. R. Hubbard and J. H. Till, “Protein tyrosine kinase structure and function,” Annual Review of Biochemistry, vol. 69, pp. 373–398, 2000.
[125]
A. W. Stoker, “Protein tyrosine phosphatases and signalling,” Journal of Endocrinology, vol. 185, no. 1, pp. 19–33, 2005.
[126]
G. C. M. Zondag and W. H. Moolenaar, “Receptor protein tyrosine phosphatases: involvement in cell-cell interaction and signaling,” Biochimie, vol. 79, no. 8, pp. 477–483, 1997.
[127]
S. Dadke, A. Kusari, and J. Kusari, “Phosphorylation and activation of protein tyrosine phosphatase (PTP) 1B by insulin receptor,” Molecular and Cellular Biochemistry, vol. 221, no. 1-2, pp. 147–154, 2001.
[128]
K. Fujisawa, A. Fujita, T. Ishizaki, Y. Saito, and S. Narumiya, “Identification of the Rho-binding domain of p160(ROCK), a Rho-associated coiled-coil containing protein kinase,” Journal of Biological Chemistry, vol. 271, no. 38, pp. 23022–23028, 1996.
[129]
W. Lu and B. J. Mayer, “Mechanism of activation of Pak1 kinase by membrane localization,” Oncogene, vol. 18, no. 3, pp. 797–806, 1999.
[130]
T. Rosenzweig, S. Aga-Mizrachi, A. Bak, and S. R. Sampson, “Src tyrosine kinase regulates insulin-induced activation of protein kinase C (PKC) δ in skeletal muscle,” Cellular Signalling, vol. 16, no. 11, pp. 1299–1308, 2004.
[131]
K. Yoshida and D. Kufe, “Negative regulation of the SHPTP1 protein tyrosine phosphatase by protein kinase C δ in response to DNA damage,” Molecular Pharmacology, vol. 60, no. 6, pp. 1431–1438, 2001.
[132]
A. K. Somani, J. S. Bignon, G. B. Mills, K. A. Siminovitch, and D. R. Branch, “Src kinase activity is regulated by the SHP-1 protein-tyrosine phosphatase,” Journal of Biological Chemistry, vol. 272, no. 34, pp. 21113–21119, 1997.
[133]
Y. Obara, K. Labudda, T. J. Dillon, and P. J. S. Stork, “PKA phosphorylation of Src mediates Rap1 activation in NGF and cAMP signaling in PC12 cells,” Journal of Cell Science, vol. 117, no. 25, pp. 6085–6094, 2004.
[134]
T. Vang, K. M. Torgersen, V. Sundvold et al., “Activation of the COOH-terminal Src kinase (Csk) by cAMP-dependent protein kinase inhibits signaling through the T cell receptor,” Journal of Experimental Medicine, vol. 193, no. 4, pp. 497–507, 2001.
[135]
G. Superti-Furga, S. Fumagalli, M. Koegl, S. A. Courtneidge, and G. Draetta, “Csk inhibition of c-Src activity requires both the SH2 and SH3 domains of Src,” EMBO Journal, vol. 12, no. 7, pp. 2625–2634, 1993.
[136]
R. W. McLachlan and A. S. Yap, “Not so simple: the complexity of phosphotyrosine signaling at cadherin adhesive contacts,” Journal of Molecular Medicine, vol. 85, no. 6, pp. 545–554, 2007.
[137]
B. Nagar, O. Hantschel, M. A. Young et al., “Structural basis for the autoinhibition of c-Abl tyrosine kinase,” Cell, vol. 112, no. 6, pp. 859–871, 2003.
[138]
T. Y. El Sayegh, P. D. Arora, L. Fan et al., “Phosphorylation of N-cadherin-associated cortactin by Fer kinase regulates N-cadherin mobility and intercellular adhesion strength,” Molecular Biology of the Cell, vol. 16, no. 12, pp. 5514–5527, 2005.
[139]
N. L. Zandy and A. M. Pendergast, “Abl tyrosine kinases modulate cadherin-dependent adhesion upstream and downstream of Rho family GTPases,” Cell Cycle, vol. 7, no. 4, pp. 444–448, 2008.
[140]
C. K. Joo, H. S. Kim, J. Y. Park, Y. Seomun, M. J. Son, and J. T. Kim, “Ligand release-independent transactivation of epidermal growth factor receptor by transforming growth factor-β involves multiple signaling pathways,” Oncogene, vol. 27, no. 5, pp. 614–628, 2008.
[141]
T. Watanabe, K. Sato, and K. Kaibuchi, “Cadherin-mediated intercellular adhesion and signaling cascades involving small GTPases,” Cold Spring Harbor Perspectives in Biology, vol. 1, no. 3, p. a003020, 2009.
[142]
V. M. M. Braga and A. S. Yap, “The challenges of abundance: epithelial junctions and small GTPase signalling,” Current Opinion in Cell Biology, vol. 17, no. 5, pp. 466–474, 2005.
[143]
E. A. Burton, T. N. Oliver, and A. M. Pendergast, “Abl kinases regulate actin comet tail elongation via an N-WASP-dependent pathway,” Molecular and Cellular Biology, vol. 25, no. 20, pp. 8834–8843, 2005.
[144]
M. Martin, S. M. Ahern-Djamali, F. M. Hoffmann, and W. M. Saxton, “Abl tyrosine kinase and its substrate Ena/VASP have functional interactions with kinesin-1,” Molecular Biology of the Cell, vol. 16, no. 9, pp. 4225–4230, 2005.
[145]
Q. Lu, N. K. Mukhopadhyay, J. D. Griffin, M. Paredes, M. Medina, and K. S. Kosik, “Brain armadillo protein δ-catenin interacts with Abl tyrosine kinase and modulates cellular morphogenesis in response to growth factors,” Journal of Neuroscience Research, vol. 67, no. 5, pp. 618–624, 2002.
[146]
Z. Dai and A. M. Pendergast, “Abi-2, a novel SH3-containing protein interacts with the c-Abl tyrosine kinase and modulates c-Abl transforming activity,” Genes and Development, vol. 9, no. 21, pp. 2569–2582, 1995.
[147]
M. Mitsushima, H. Takahashi, T. Shishido, K. Ueda, and N. Kioka, “Abl kinase interacts with and phosphorylates vinexin,” FEBS Letters, vol. 580, no. 17, pp. 4288–4295, 2006.
[148]
P. D. McCrea, D. Gu, and M. S. Balda, “Junctional music that the nucleus hears: cell-cell contact signaling and the modulation of gene activity,” Cold Spring Harbor Perspectives in Biology, vol. 1, no. 4, p. a002923, 2009.
[149]
F. H. Brembeck, M. Rosário, and W. Birchmeier, “Balancing cell adhesion and Wnt signaling, the key role of β-catenin,” Current Opinion in Genetics and Development, vol. 16, no. 1, pp. 51–59, 2006.
[150]
W. J. Nelson and R. Nusse, “Convergence of Wnt, β-Catenin, and Cadherin pathways,” Science, vol. 303, no. 5663, pp. 1483–1487, 2004.
[151]
Y. Xu and G. Carpenter, “Identification of cadherin tyrosine residues that are phosphorylated and mediate Shc association,” Journal of Cellular Biochemistry, vol. 75, no. 2, pp. 264–271, 1999.
[152]
Z. Wang, S. Sandiford, C. Wu, and S. S. C. Li, “Numb regulates cell-cell adhesion and polarity in response to tyrosine kinase signalling,” EMBO Journal, vol. 28, no. 16, pp. 2360–2373, 2009.
[153]
M. D. Potter, S. Barbero, and D. A. Cheresh, “Tyrosine phosphorylation of VE-cadherin prevents binding of p120- and β-catenin and maintains the cellular mesenchymal state,” Journal of Biological Chemistry, vol. 280, no. 36, pp. 31906–31912, 2005.
[154]
S. Yonemura, T. Matsui, S. Tsukita, and S. Tsukita, “Rho-dependent and -indenpendent activation mechanisms of ezrin/radixin/moesin proteins: an essential role for polyphosphoinositides in vivo,” Journal of Cell Science, vol. 115, no. 12, pp. 2569–2580, 2002.
[155]
M. Amano, M. Ito, K. Kimura et al., “Phosphorylation and activation of myosin by Rho-associated kinase (Rho- kinase),” Journal of Biological Chemistry, vol. 271, no. 34, pp. 20246–20249, 1996.
[156]
J. H. Henson, S. E. Kolnik, C. A. Fried et al., “Actin-based centripetal flow: phosphatase inhibition by calyculin-A alters flow pattern, actin organization, and actomyosin distribution,” Cell Motility and the Cytoskeleton, vol. 56, no. 4, pp. 252–266, 2003.
[157]
T. Volberg, Y. Zick, R. Dror et al., “The effect of tyrosine-specific protein phosphorylation on the assembly of adherens-type junctions,” EMBO Journal, vol. 11, no. 5, pp. 1733–1742, 1992.
[158]
E. Calautti, S. Cabodi, P. L. Stein, M. Hatzfeld, N. Kedersha, and G. P. Dotto, “Tyrosine phosphorylation and Src family kinases control keratinocyte cell-cell adhesion,” Journal of Cell Biology, vol. 141, no. 6, pp. 1449–1465, 1998.
[159]
J. H. Pang, A. Kraemer, S. J. Stehbens, M. C. Frame, and A. S. Yap, “Recruitment of phosphoinositide 3-kinase defines a positive contribution of tyrosine kinase signaling to E-cadherin function,” Journal of Biological Chemistry, vol. 280, no. 4, pp. 3043–3050, 2005.
[160]
S. Shibamoto, M. Hayakawa, K. Takeuchi et al., “Tyrosine phosphorylation of β-catenin and plakoglobin enhanced by hepatocyte growth factor and epidermal growth factor in human carcinoma cells,” Cell Adhesion and Communication, vol. 1, no. 4, pp. 295–305, 1994.
[161]
K. Hatanaka, M. Simons, and M. Murakami, “Phosphorylation of VE-cadherin controls endothelial phenotypes via p120-catenin coupling and Rac1 activation,” American Journal of Physiology, vol. 300, no. 1, pp. H162–H172, 2011.
[162]
S. Pece and J. S. Gutkind, “E-cadherin and Hakai: signalling, remodeling or destruction?” Nature Cell Biology, vol. 4, no. 4, pp. E72–E74, 2002.
[163]
Y. Fujita, G. Krause, M. Scheffner et al., “Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex,” Nature Cell Biology, vol. 4, no. 3, pp. 222–231, 2002.
[164]
H. Keilhack, U. Hellman, J. Van Hengel, F. Van Roy, J. Godovac-Zimmermann, and F. D. B？hmer, “The protein-tyrosine phosphatase SHP-1 binds to and dephosphorylates p120 catenin,” Journal of Biological Chemistry, vol. 275, no. 34, pp. 26376–26384, 2000.
[165]
Y. Fukumoto, Y. Shintani, A. B. Reynolds, K. R. Johnson, and M. J. Wheelock, “The regulatory or phosphorylation domain of p120 catenin controls E-cadherin dynamics at the plasma membrane,” Experimental Cell Research, vol. 314, no. 1, pp. 52–67, 2008.
[166]
G. S. Call, J. Y. Chung, J. A. Davis et al., “Zyxin phosphorylation at serine 142 modulates the zyxin head-tail interaction to alter cell-cell adhesion,” Biochemical and Biophysical Research Communications, vol. 404, no. 3, pp. 780–784, 2011.
[167]
T. N. Nguyen, A. Uemura, W. Shih, and S. Yamada, “Zyxin-mediated actin assembly is required for efficient wound closure,” Journal of Biological Chemistry, vol. 285, no. 46, pp. 35439–35445, 2010.
[168]
M. D. H. Hansen and M. C. Beckerle, “Opposing roles of Zyxin/LPP ACTA repeats and the LIM domain region in cell-cell adhesion,” Journal of Biological Chemistry, vol. 281, no. 23, pp. 16178–16188, 2006.
[169]
E. Butt, K. Abel, M. Krieger et al., “cAMP- and cGMP-dependent protein kinase phosphorylation sites of the focal adhesion vasodilator-stimulated phosphoprotein (VASP) in vitro and in intact human platelets,” Journal of Biological Chemistry, vol. 269, no. 20, pp. 14509–14517, 1994.
[170]
K. Chitaley, L. Chen, A. Galler, U. Walter, G. Daum, and A. W. Clowes, “Vasodilator-stimulated phosphoprotein is a substrate for protein kinase C,” FEBS Letters, vol. 556, no. 1-3, pp. 211–215, 2004.
[171]
B. Harbeck, S. Hüttelmaier, K. Schlüter, B. M. Jockusch, and S. Illenberger, “Phosphorylation of the vasodilator-stimulated phosphoprotein regulates its interaction witn actin,” Journal of Biological Chemistry, vol. 275, no. 40, pp. 30817–30825, 2000.
[172]
M. Barzik, T. I. Kotova, H. N. Higgs et al., “Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins,” Journal of Biological Chemistry, vol. 280, no. 31, pp. 28653–28662, 2005.
[173]
V. Vasioukhin, C. Bauer, M. Yin, and E. Fuchs, “Directed actin polymerization is the driving force for epithelial cell- cell adhesion,” Cell, vol. 100, no. 2, pp. 209–219, 2000.
[174]
J. A. Scott, A. M. Shewan, N. R. Den Elzen, J. J. Loureiro, F. B. Gertler, and A. S. Yap, “Ena/VASP proteins can regulate distinct modes of actin organization at cadherin-adhesive contacts,” Molecular Biology of the Cell, vol. 17, no. 3, pp. 1085–1095, 2006.
[175]
E. Morais-de-Sá, V. Mirouse, and D. St Johnston, “aPKC phosphorylation of bazooka defines the apical/lateral border in Drosophila epithelial cells,” Cell, vol. 141, no. 3, pp. 509–523, 2010.
[176]
R. F. Walther and F. Pichaud, “Crumbs/DaPKC-dependent apical exclusion of bazooka promotes photoreceptor polarity remodeling,” Current Biology, vol. 20, no. 12, pp. 1065–1074, 2010.
[177]
Y.-C. Wang, Z. Khan, M. Kaschube, and E. F. Wieschaus, “Differential positioning of adherens junctions is associated with initiation of epithelial folding,” Nature, vol. 484, no. 7394, pp. 390–393, 2012.
[178]
P. V. Hornbeck, I. Chabra, J. M. Kornhauser, E. Skrzypek, and B. Zhang, “PhosphoSite: a bioinformatics resource dedicated to physiological protein phosphorylation,” Proteomics, vol. 4, no. 6, pp. 1551–1561, 2004.
[179]
A. M. E. Jones and T. S. Nühse, “Phosphoproteomics using iTRAQ,” Methods in Molecular Biology, vol. 779, pp. 287–302, 2011.
[180]
B. Eyrich, A. Sickmann, and R. P. Zahedi, “Catch me if you can: mass spectrometry-based phosphoproteomics and quantification strategies,” Proteomics, vol. 11, no. 4, pp. 554–570, 2011.
[181]
H. Imamura, N. Yachie, R. Saito, Y. Ishihama, and M. Tomita, “Towards the systematic discovery of signal transduction networks using phosphorylation dynamics data,” BMC Bioinformatics, vol. 11, article 232, 2010.
[182]
I. Martinez-Ferrando, R. Chaerkady, J. Zhong et al., “Identification of targets of c-Src tyrosine kinase by chemical complementation and phosphoproteomics,” Molecular and Cellular Proteomics. In press.
[183]
M. Hilger, T. Bonaldi, F. Gnad, and M. Mann, “Systems-wide analysis of a phosphatase knock-down by quantitative proteomics and phosphoproteomics,” Molecular and Cellular Proteomics, vol. 8, no. 8, pp. 1908–1920, 2009.
[184]
P. H. Huang, A. Mukasa, R. Bonavia et al., “Quantitative analysis of EGFRvIII cellular signaling networks reveals a combinatorial therapeutic strategy for glioblastoma,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 31, pp. 12867–12872, 2007.
[185]
H. Kozuka-Hata, S. Tasaki, and M. Oyama, “Phosphoproteomics-based systems analysis of signal transduction networks,” Frontiers in Physiology, vol. 2, no. 113, 2011.
[186]
A. Derouiche, C. Cousin, and I. Mijakovic, “Protein phosphorylation from the perspective of systems biology,” Current Opinion in Biotechnology. In press.
[187]
E. Sadot, M. Conacci-Sorrell, J. Zhurinsky et al., “Regulation of S33/S37 phosphorylated β-catenin in normal and transformed cells,” Journal of Cell Science, vol. 115, no. 13, pp. 2771–2780, 2002.
[188]
M. V. Brown, P. E. Burnett, M. F. Denning, and A. B. Reynolds, “PDGF receptor activation induces p120-catenin phosphorylation at serine 879 via a PKCα-dependent pathway,” Experimental Cell Research, vol. 315, no. 1, pp. 39–49, 2009.
[189]
G. Ren, F. M. Helwani, S. Verma, R. W. McLachlan, S. A. Weed, and A. S. Yap, “Cortactin is a functional target of E-cadherin-activated Src family kinases in MCF7 epithelial monolayers,” Journal of Biological Chemistry, vol. 284, no. 28, pp. 18913–18922, 2009.
[190]
P. M. Benz, C. Blume, S. Seifert et al., “Differential VASP phosphorylation controls remodeling of the actin cytoskeleton,” Journal of Cell Science, vol. 122, no. 21, pp. 3954–3965, 2009.
[191]
R. Zaidel-Bar, R. Milo, Z. Kam, and B. Geiger, “A paxillin tyrosine phosphorylation switch regulates the assembly and form of cell-matrix adhesions,” Journal of Cell Science, vol. 120, no. 1, pp. 137–148, 2007.
[192]
R. Zaidel-Bar and B. Geiger, “The switchable integrin adhesome,” Journal of Cell Science, vol. 123, no. 9, pp. 1385–1388, 2010.
