journal article Feb 23, 2011

Adhesion molecule signalling: not always a sticky business

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References
77
[1]
Bazzoni, G. & Dejana, E. Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol. Rev. 84, 869–901 (2004). 10.1152/physrev.00035.2003
[2]
Vestweber, D. VE-cadherin: the major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler. Thromb. Vasc. Biol. 28, 223–232 (2008). 10.1161/atvbaha.107.158014
[3]
Wallez, Y. & Huber, P. Endothelial adherens and tight junctions in vascular homeostasis, inflammation and angiogenesis. Biochim. Biophys. Acta 1778, 794–809 (2008). 10.1016/j.bbamem.2007.09.003
[4]
Dejana, E., Tournier-Lasserve, E. & Weinstein, B. M. The control of vascular integrity by endothelial cell junctions: molecular basis and pathological implications. Dev. Cell 16, 209–221 (2009). 10.1016/j.devcel.2009.01.004
[5]
Takai, Y., Ikeda, W., Ogita, H. & Rikitake, Y. The immunoglobulin-like cell adhesion molecule nectin and its associated protein afadin. Annu. Rev. Cell Dev. Biol. 24, 309–342 (2008). 10.1146/annurev.cellbio.24.110707.175339
[6]
Takai, Y., Miyoshi, J., Ikeda, W. & Ogita, H. Nectins and nectin-like molecules: roles in contact inhibition of cell movement and proliferation. Nature Rev. Mol. Cell Biol. 9, 603–615 (2008). 10.1038/nrm2457
[7]
McCrea, P. D., Gu, D. & Balda, M. S. Junctional music that the nucleus hears: cell-cell contact signaling and the modulation of gene activity. Cold Spring Harb. Perspect. Biol. 1, a002923 (2009). 10.1101/cshperspect.a002923
[8]
Furuse, M. Molecular basis of the core structure of tight junctions. Cold Spring Harb. Perspect. Biol. 2, a002907 (2010). 10.1101/cshperspect.a002907
[9]
Loers, G. & Schachner, M. Recognition molecules and neural repair. J. Neurochem. 101, 865–882 (2007). 10.1111/j.1471-4159.2006.04409.x
[10]
Francavilla, C. et al. The binding of NCAM to FGFR1 induces a specific cellular response mediated by receptor trafficking. J. Cell Biol. 187, 1101–1116 (2009). This paper provides a prototypical example of an Ig-CAM, NCAM, acting as a noncanonical ligand for a growth factor receptor, FGFR. Of note, both the signalling cascade and the intracellular fate of NCAM-stimulated FGFR are different from those induced by FGF. 10.1083/jcb.200903030
[11]
Taddei, A. et al. Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5. Nature Cell Biol. 10, 923–934 (2008). The authors describe a molecular mechanism underlying the crosstalk between adherens and tight junctions in endothelial cells, implicating VE-cadherin in the negative regulation of FOXO1 and β-catenin, two factors that inhibit the expression of the tight junction component claudin-5. 10.1038/ncb1752
[12]
Comoglio, P. M., Boccaccio, C. & Trusolino, L. Interactions between growth factor receptors and adhesion molecules: breaking the rules. Curr. Opin. Cell Biol. 15, 565–571 (2003). 10.1016/s0955-0674(03)00096-6
[13]
Desgrosellier, J. S. & Cheresh, D. A. Integrins in cancer: biological implications and therapeutic opportunities. Nature Rev. Cancer 10, 9–22 (2010). 10.1038/nrc2748
[14]
Adherens and tight junctions: Structure, function and connections to the actin cytoskeleton

Andrea Hartsock, W. James Nelson

Biochimica et Biophysica Acta (BBA) - Biomembranes 2008 10.1016/j.bbamem.2007.07.012
[15]
Meng, W. & Takeichi, M. Adherens junction: molecular architecture and regulation. Cold Spring Harb. Perspect. Biol. 1, a002899 (2009). 10.1101/cshperspect.a002899
[16]
Stepniak, E., Radice, G. L. & Vasioukhin, V. Adhesive and signaling functions of cadherins and catenins in vertebrate development. Cold Spring Harb. Perspect. Biol. 1, a002949 (2009). 10.1101/cshperspect.a002949
[17]
Harris, T. J. & Tepass, U. Adherens junctions: from molecules to morphogenesis. Nature Rev. Mol. Cell Biol. 11, 502–514 (2010). 10.1038/nrm2927
[18]
Komarova, Y. & Malik, A. B. Regulation of endothelial permeability via paracellular and transcellular transport pathways. Annu. Rev. Physiol. 72, 463–493 (2010). 10.1146/annurev-physiol-021909-135833
[19]
Macara, I. G. & Mili, S. Polarity and differential inheritance — universal attributes of life? Cell 135, 801–812 (2008). 10.1016/j.cell.2008.11.006
[20]
Lampugnani, M. G. et al. CCM1 regulates vascular-lumen organization by inducing endothelial polarity. J. Cell Sci. 123, 1073–1080 (2010). 10.1242/jcs.059329
[21]
Aricescu, A. R. & Jones, E. Y. Immunoglobulin superfamily cell adhesion molecules: zippers and signals. Curr. Opin. Cell Biol. 19, 543–550 (2007). 10.1016/j.ceb.2007.09.010
[22]
Ditlevsen, D. K. & Kolkova, K. Signaling pathways involved in NCAM-induced neurite outgrowth. Adv. Exp. Med. Biol. 663, 151–168 (2010). 10.1007/978-1-4419-1170-4_10
[23]
Maness, P. F. & Schachner, M. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nature Neurosci. 10, 19–26 (2007). 10.1038/nn1827
[24]
Lampugnani, M. G. et al. Contact inhibition of VEGF-induced proliferation requires vascular endothelial cadherin, beta-catenin, and the phosphatase DEP-1/CD148. J. Cell Biology 161, 793–804 (2003). 10.1083/jcb.200209019
[25]
Lampugnani, M. G., Orsenigo, F., Gagliani, M. C., Tacchetti, C. & Dejana, E. Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments. J. Cell Biol. 174, 593–604 (2006). In this paper, VE-cadherin is shown to interfere with the VEGF-stimulated internalization of VEGFR2 and with its signalling from the endosomal compartment. This process underlies the role of VE-cadherin in contact-mediated inhibition of endothelial cell proliferation. 10.1083/jcb.200602080
[26]
Shay-Salit, A. et al. VEGF receptor 2 and the adherens junction as a mechanical transducer in vascular endothelial cells. Proc. Natl Acad. Sci. USA 99, 9462–9467 (2002). 10.1073/pnas.142224299
[27]
Tzima, E. et al. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437, 426–431 (2005). In references 26–27, the authors report a mechanosensory role of VE-cadherin during shear stress. VE-cadherin acts as an adaptor between PECAM1 and VEGFR2, allowing the formation of a mechanosensory complex and the stimulation of signalling cascades that regulate integrin activation, cytoskeletal reorganization and the induction of the NF-κB pathway. 10.1038/nature03952
[28]
Knights, V. & Cook, S. J. De-regulated FGF receptors as therapeutic targets in cancer. Pharmacol. Ther. 125, 105–117 (2010). 10.1016/j.pharmthera.2009.10.001
[29]
Williams, E. J., Furness, J., Walsh, F. S. & Doherty, P. Activation of the FGF receptor underlies neurite outgrowth stimulated by L1, N-CAM, and N-cadherin. Neuron 13, 583–594 (1994). This is the first report implicating FGFR signalling downstream of different cell adhesion molecules, and describing a molecular mechanism underlying CAM-induced neurite outgrowth. 10.1016/0896-6273(94)90027-2
[30]
Williams, E. J. et al. Identification of an N-cadherin motif that can interact with the fibroblast growth factor receptor and is required for axonal growth. J. Biol. Chem. 276, 43879–43886 (2001). 10.1074/jbc.m105876200
[31]
Utton, M. A., Eickholt, B., Howell, F. V., Wallis, J. & Doherty, P. Soluble N-cadherin stimulates fibroblast growth factor receptor dependent neurite outgrowth and N-cadherin and the fibroblast growth factor receptor co-cluster in cells. J. Neurochem. 76, 1421–1430 (2001). 10.1046/j.1471-4159.2001.00140.x
[32]
Nieman, M. T., Prudoff, R. S., Johnson, K. R. & Wheelock, M. J. N-cadherin promotes motility in human breast cancer cells regardless of their E-cadherin expression. J. Cell Biol. 147, 631–644 (1999). 10.1083/jcb.147.3.631
[33]
Suyama, K., Shapiro, I., Guttman, M. & Hazan, R. B. A signaling pathway leading to metastasis is controlled by N-cadherin and the FGF receptor. Cancer Cell 2, 301–314 (2002). 10.1016/s1535-6108(02)00150-2
[34]
Cavallaro, U., Niedermeyer, J., Fuxa, M. & Christofori, G. NCAM modulates tumour-cell adhesion to matrix by inducing FGF-receptor signalling. Nature Cell Biol. 3, 650–657 (2001). This paper showed the interaction of NCAM with FGFR in tumour cells, in which it regulates adhesion to the extracellular matrix. 10.1038/35083041
[35]
Francavilla, C. et al. Neural cell adhesion molecule regulates the cellular response to fibroblast growth factor. J. Cell Sci. 120, 4388–4394 (2007). 10.1242/jcs.010744
[36]
Kiselyov, V. V. et al. Structural basis for a direct interaction between FGFR1 and NCAM and evidence for a regulatory role of ATP. Structure (Camb.) 11, 691–701 (2003). 10.1016/s0969-2126(03)00096-0
[37]
Christensen, C., Lauridsen, J. B., Berezin, V., Bock, E. & Kiselyov, V. V. The neural cell adhesion molecule binds to fibroblast growth factor receptor 2. FEBS Lett. 580, 3386–3390 (2006). 10.1016/j.febslet.2006.05.008
[38]
Kulahin, N. et al. Direct demonstration of NCAM cis-dimerization and inhibitory effect of palmitoylation using the BRET(2) technique. FEBS Lett. 585, 58–64 (2011). 10.1016/j.febslet.2010.11.043
[39]
Soroka, V. et al. Structure and interactions of NCAM Ig1-2-3 suggest a novel zipper mechanism for homophilic adhesion. Structure (Camb.) 11, 1291–1301 (2003). 10.1016/j.str.2003.09.006
[40]
Kirschbaum, K., Kriebel, M., Kranz, E. U., Potz, O. & Volkmer, H. Analysis of non-canonical fibroblast growth factor receptor 1 (FGFR1) interaction reveals regulatory and activating domains of neurofascin. J. Biol. Chem. 284, 28533–28542 (2009). 10.1074/jbc.m109.004440
[41]
Owczarek, S. et al. Neuroplastin-55 binds to and signals through the fibroblast growth factor receptor. FASEB J. 24, 1139–1150 (2010). 10.1096/fj.09-140509
[42]
Getsios, S. et al. Desmoglein 1-dependent suppression of EGFR signaling promotes epidermal differentiation and morphogenesis. J. Cell Biol. 185, 1243–1258 (2009). 10.1083/jcb.200809044
[43]
Lacouture, M. E. Mechanisms of cutaneous toxicities to EGFR inhibitors. Nature Rev. Cancer 6, 803–812 (2006). 10.1038/nrc1970
[44]
Anastasiadis, P. Z. p120-ctn: a nexus for contextual signaling via Rho GTPases. Biochim. Biophys. Acta 1773, 34–46 (2007). 10.1016/j.bbamcr.2006.08.040
[45]
Gavert, N. et al. L1, a novel target of β-catenin signaling, transforms cells and is expressed at the invasive front of colon cancers. J. Cell Biol. 168, 633–642 (2005). 10.1083/jcb.200408051
[46]
Geismann, C. et al. Up-regulation of L1CAM in pancreatic duct cells is transforming growth factor β1- and slug-dependent: role in malignant transformation of pancreatic cancer. Cancer Res. 69, 4517–4526 (2009). 10.1158/0008-5472.can-08-3493
[47]
Gast, D. et al. L1 augments cell migration and tumor growth but not β3 integrin expression in ovarian carcinomas. Int. J. Cancer 115, 658–665 (2005). 10.1002/ijc.20869
[48]
Zecchini, S. et al. The differential role of L1 in ovarian carcinoma and normal ovarian surface epithelium. Cancer Res. 68, 1110–1118 (2008). 10.1158/0008-5472.can-07-2897
[49]
Meier, F. et al. The adhesion molecule L1 (CD171) promotes melanoma progression. Int. J. Cancer 119, 549–555 (2006). 10.1002/ijc.21880
[50]
Gavert, N., Ben-Shmuel, A., Lemmon, V., Brabletz, T. & Ben-Ze'ev, A. Nuclear factor-κB signaling and ezrin are essential for L1-mediated metastasis of colon cancer cells. J. Cell Sci. 123, 2135–2143 (2010). 10.1242/jcs.069542

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Citations
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Published
Feb 23, 2011
Vol/Issue
12(3)
Pages
189-197
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Cite This Article
Ugo Cavallaro, Elisabetta Dejana (2011). Adhesion molecule signalling: not always a sticky business. Nature Reviews Molecular Cell Biology, 12(3), 189-197. https://doi.org/10.1038/nrm3068
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