Synergistic control of cell adhesion by integrins and syndecans (original) (raw)
Hynes, R. O. Integrins: bidirectional, allosteric signaling machines. Cell110, 673–687 (2002). ArticleCASPubMed Google Scholar
Humphries, J. D., Byron, A. & Humphries, M. J. Integrin ligands at a glance. J. Cell Sci.119, 3901–3903 (2006). CASPubMed Google Scholar
Bouvard, D. et al. Functional consequences of integrin gene mutations in mice. Circ. Res.89, 211–223 (2001). CASPubMed Google Scholar
Bokel, C. & Brown, N. H. Integrins in development: moving on, responding to, and sticking to the extracellular matrix. Dev. Cell3, 311–321 (2002). CASPubMed Google Scholar
Bernfield, M. et al. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem.68, 729–777 (1999). CASPubMed Google Scholar
Fuster, M. M. et al. Genetic alteration of endothelial heparan sulfate selectively inhibits tumor angiogenesis. J. Cell Biol.177, 539–549 (2007). CASPubMedPubMed Central Google Scholar
Mahalingam, Y., Gallagher, J. T. & Couchman, J. R. Cellular adhesion responses to the heparin-binding (HepII) domain of fibronectin require heparan sulfate with specific properties. J. Biol. Chem.282, 3221–3230 (2007). CASPubMed Google Scholar
Beauvais, D. M., Burbach, B. J. & Rapraeger, A. C. The syndecan-1 ectodomain regulates αvβ3 integrin activity in human mammary carcinoma cells. J. Cell Biol.167, 171–181 (2004). Describes the ability of syndecan-1 to modulate αVβ3ligand-binding affinity, particularly highlighting the role of the ectodomain of syndecan. CASPubMedPubMed Central Google Scholar
McQuade, K. J., Beauvais, D. M., Burbach, B. J. & Rapraeger, A. C. Syndecan-1 regulates αvβ5 integrin activity in B82L fibroblasts. J. Cell Sci.119, 2445–2456 (2006). CASPubMed Google Scholar
Whiteford, J. R. & Couchman, J. R. A conserved NXIP motif is required for cell adhesion properties of the syndecan-4 ectodomain. J. Biol. Chem.281, 32156–32163 (2006). CASPubMed Google Scholar
Bloom, L., Ingham, K. C. & Hynes, R. O. Fibronectin regulates assembly of actin filaments and focal contacts in cultured cells via the heparin-binding site in repeat III13 . Mol. Biol. Cell10, 1521–1536 (1999). CASPubMedPubMed Central Google Scholar
Woods, A., Couchman, J. R., Johansson, S. & Hook, M. Adhesion and cytoskeletal organisation of fibroblasts in response to fibronectin fragments. EMBO J.5, 665–670 (1986). CASPubMedPubMed Central Google Scholar
Hozumi, K., Suzuki, N., Nielsen, P. K., Nomizu, M. & Yamada, Y. Laminin α1 chain LG4 module promotes cell attachment through syndecans and cell spreading through integrin α2β1. J. Biol. Chem.281, 32929–32940 (2006). CASPubMed Google Scholar
Ogawa, T., Tsubota, Y., Hashimoto, J., Kariya, Y. & Miyazaki, K. The short arm of laminin γ2 chain of laminin-5 (laminin-332) binds syndecan-1 and regulates cellular adhesion and migration by suppressing phosphorylation of integrin β4 chain. Mol. Biol. Cell18, 1621–1633 (2007). CASPubMedPubMed Central Google Scholar
Garcia-Alvarez, B. et al. Structural determinants of integrin recognition by talin. Mol. Cell11, 49–58 (2003). CASPubMed Google Scholar
Tadokoro, S. et al. Talin binding to integrin β tails: a final common step in integrin activation. Science302, 103–106 (2003). CASPubMed Google Scholar
Kim, M., Carman, C. V. & Springer, T. A. Bidirectional transmembrane signaling by cytoplasmic domain separation in integrins. Science301, 1720–1725 (2003). CASPubMed Google Scholar
Arias-Salgado, E. G., Lizano, S., Shattil, S. J. & Ginsberg, M. H. Specification of the direction of adhesive signaling by the integrin β cytoplasmic domain. J. Biol. Chem.280, 29699–29707 (2005). CASPubMed Google Scholar
Koo, B. K. et al. Structural basis of syndecan-4 phosphorylation as a molecular switch to regulate signaling. J. Mol. Biol.355, 651–663 (2006). This paper stands out from a large body of literature dealing with the importance of oligomerization of the cytoplasmic tail of syndecan-4 in the regulation of PKCα by resolving the structural details of oligomerization and comparing the positive regulatory effect of PtdIns(4,5)P2with the negative effect of phosphorylation of the cytoplasmic tail. CASPubMed Google Scholar
Grootjans, J. J. et al. Syntenin, a PDZ protein that binds syndecan cytoplasmic domains. Proc. Natl Acad. Sci. USA94, 13683–13688 (1997). CASPubMedPubMed Central Google Scholar
Kinnunen, T. et al. Cortactin-Src kinase signaling pathway is involved in N-syndecan-dependent neurite outgrowth. J. Biol. Chem.273, 10702–10708 (1998). CASPubMed Google Scholar
Yoo, J., Jeong, M. J., Cho, H. J., Oh, E. S. & Han, M. Y. Dynamin II interacts with syndecan-4, a regulator of focal adhesion and stress-fiber formation. Biochem. Biophys. Res. Commun.328, 424–431 (2005). CASPubMed Google Scholar
Burridge, K. & Wennerberg, K. Rho and Rac take center stage. Cell116, 167–179 (2004). CASPubMed Google Scholar
Mitra, S. K. & Schlaepfer, D. D. Integrin-regulated FAK–Src signaling in normal and cancer cells. Curr. Opin. Cell Biol.18, 516–523 (2006). CASPubMed Google Scholar
Renshaw, M. W., Price, L. S. & Schwartz, M. A. Focal adhesion kinase mediates the integrin signaling requirement for growth factor activation of MAP kinase. J. Cell Biol.147, 611–618 (1999). CASPubMedPubMed Central Google Scholar
Oh, E. S., Woods, A. & Couchman, J. R. Syndecan-4 proteoglycan regulates the distribution and activity of protein kinase C. J. Biol. Chem.272, 8133–8136 (1997). CASPubMed Google Scholar
Murakami, M., Horowitz, A., Tang, S., Ware, J. A. & Simons, M. Protein kinase C (PKC)δ regulates PKCα activity in a syndecan-4-dependent manner. J. Biol. Chem.277, 20367–20371 (2002). CASPubMed Google Scholar
Mostafavi-Pour, Z. et al. Integrin-specific signaling pathways controlling focal adhesion formation and cell migration. J. Cell Biol.161, 155–167 (2003). CASPubMedPubMed Central Google Scholar
Ng, T. et al. PKCα regulates β1 integrin-dependent cell motility through association and control of integrin traffic. EMBO J.18, 3909–3923 (1999). CASPubMedPubMed Central Google Scholar
Han, J. et al. Reconstructing and deconstructing agonist-induced activation of integrin αIIbβ3. Curr. Biol.16, 1796–1806 (2006). CASPubMed Google Scholar
Tkachenko, E., Lutgens, E., Stan, R. V. & Simons, M. Fibroblast growth factor 2 endocytosis in endothelial cells proceed via syndecan-4-dependent activation of Rac1 and a Cdc42-dependent macropinocytic pathway. J. Cell Sci.117, 3189–3199 (2004). CASPubMed Google Scholar
Zimmermann, P. et al. Syndecan recycling is controlled by syntenin-PIP2 interaction and Arf6. Dev. Cell9, 377–388 (2005). Describes the process of syndecan recycling and identifies key roles for the PDZ-domain protein, syntenin, PtdIns(4,5)P2and Arf6. CASPubMed Google Scholar
Disatnik, M. H. et al. The bi-directional translocation of MARCKS between membrane and cytosol regulates integrin-mediated muscle cell spreading. J. Cell Sci.117, 4469–4479 (2004). CASPubMed Google Scholar
Ott, V. L. & Rapraeger, A. C. Tyrosine phosphorylation of syndecan-1 and -4 cytoplasmic domains in adherent B82 fibroblasts. J. Biol. Chem.273, 35291–35298 (1998). CASPubMed Google Scholar
Kim, J., Han, I., Kim, Y., Kim, S. & Oh, E. S. C-terminal heparin-binding domain of fibronectin regulates integrin-mediated cell spreading but not the activation of mitogen-activated protein kinase. Biochem. J.360, 239–245 (2001). CASPubMedPubMed Central Google Scholar
Wilcox-Adelman, S. A., Denhez, F. & Goetinck, P. F. Syndecan-4 modulates focal adhesion kinase phosphorylation. J. Biol. Chem.277, 32970–32977 (2002). CASPubMed Google Scholar
Ezratty, E. J., Partridge, M. A. & Gundersen, G. G. Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nature Cell Biol.7, 581–590 (2005). CASPubMed Google Scholar
Raftopoulou, M. & Hall, A. Cell migration: Rho GTPases lead the way. Dev. Biol.265, 23–32 (2004). CASPubMed Google Scholar
Del Pozo, M. A., Price, L. S., Alderson, N. B., Ren, X. D. & Schwartz, M. A. Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J.19, 2008–2014 (2000). CASPubMedPubMed Central Google Scholar
Hirsch, E. et al. Defective Rac-mediated proliferation and survival after targeted mutation of the β1 integrin cytodomain. J. Cell Biol.157, 481–492 (2002). CASPubMedPubMed Central Google Scholar
Bass, M. D. et al. Syndecan-4-dependent Rac1 regulation determines directional migration in response to the extracellular matrix. J. Cell Biol.177, 527–538 (2007). Establishes that functional synergy between α5β1integrin and syndecan-4 is necessary for the regulation of Rac1 and contributes towards the regulation of RhoA. This paper also demonstrates that the regulation of Rac1 by these adhesion receptors has a major influence on directional migration. CASPubMedPubMed Central Google Scholar
Marcoux, N. & Vuori, K. EGF receptor mediates adhesion-dependent activation of the Rac GTPase: a role for phosphatidylinositol 3-kinase and Vav2. Oncogene22, 6100–6106 (2003). CASPubMed Google Scholar
Tkachenko, E., Elfenbein, A., Tirziu, D. & Simons, M. Syndecan-4 clustering induces cell migration in a PDZ-dependent manner. Circ. Res.98, 1398–1404 (2006). CASPubMed Google Scholar
Clark, R. A., An, J. Q., Greiling, D., Khan, A. & Schwarzbauer, J. E. Fibroblast migration on fibronectin requires three distinct functional domains. J. Invest. Dermatol.121, 695–705 (2003). CASPubMed Google Scholar
Saoncella, S. et al. Syndecan-4 regulates ATF-2 transcriptional activity in a Rac1-dependent manner. J. Biol. Chem.279, 47172–47176 (2004). CASPubMed Google Scholar
Pankov, R. et al. A Rac switch regulates random versus directionally persistent cell migration. J. Cell Biol.170, 793–802 (2005). Describes the role of Rac1 in determining directional migration and characterizes the effect of the three-dimensional architecture of the ECM on this process. CASPubMedPubMed Central Google Scholar
Wheeler, A. P. et al. Rac1 and Rac2 regulate macrophage morphology but are not essential for migration. J. Cell Sci.119, 2749–2757 (2006). CASPubMed Google Scholar
Dovas, A., Yoneda, A. & Couchman, J. R. PKCβ-dependent activation of RhoA by syndecan-4 during focal adhesion formation. J. Cell Sci.119, 2837–2846 (2006). CASPubMed Google Scholar
Saoncella, S. et al. Syndecan-4 signals cooperatively with integrins in a Rho-dependent manner in the assembly of focal adhesions and actin stress fibers. Proc. Natl Acad. Sci. USA96, 2805–2810 (1999). CASPubMedPubMed Central Google Scholar
Danen, E. H. et al. Integrins control motile strategy through a Rho–cofilin pathway. J. Cell Biol.169, 515–526 (2005). CASPubMedPubMed Central Google Scholar
Del Pozo, M. A. et al. Integrins regulate Rac targeting by internalization of membrane domains. Science303, 839–842 (2004). Describes the effect of integrin clustering on the localization of GTP–Rac1 to caveolin-rich membrane microdomains which, in combination with the effects of syndecan-4 on GTP-loading described elsewhere, might indicate a convergence point of signals downstream of α5β1integrin and syndecan-4. CASPubMed Google Scholar
Hertle, M. D., Kubler, M. D., Leigh, I. M. & Watt, F. M. Aberrant integrin expression during epidermal wound healing and in psoriatic epidermis. J. Clin. Invest.89, 1892–1901 (1992). CASPubMedPubMed Central Google Scholar
Cavani, A. et al. Distinctive integrin expression in the newly forming epidermis during wound healing in humans. J. Invest. Dermatol.101, 600–604 (1993). CASPubMed Google Scholar
Christofidou-Solomidou, M., Bridges, M., Murphy, G. F., Albelda, S. M. & DeLisser, H. M. Expression and function of endothelial cell αv integrin receptors in wound-induced human angiogenesis in human skin/SCID mice chimeras. Am. J. Pathol.151, 975–983 (1997). CASPubMedPubMed Central Google Scholar
Reynolds, L. E. et al. Accelerated re-epithelialization in β3-integrin-deficient mice is associated with enhanced TGF-β1 signaling. Nature Med.11, 167–174 (2005). CASPubMed Google Scholar
Zambruno, G. et al. Transforming growth factor-β1 modulates β1 and β5 integrin receptors and induces the de novo expression of the αvβ6 heterodimer in normal human keratinocytes: implications for wound healing. J. Cell Biol.129, 853–865 (1995). CASPubMed Google Scholar
Gallo, R., Kim, C., Kokenyesi, R., Adzick, N. S. & Bernfield, M. Syndecans-1 and -4 are induced during wound repair of neonatal but not fetal skin. J. Invest. Dermatol.107, 676–683 (1996). CASPubMed Google Scholar
Echtermeyer, F. et al. Delayed wound repair and impaired angiogenesis in mice lacking syndecan-4. J. Clin. Invest.107, R9–R14 (2001). Reports the generation of the syndecan-4-knockout mouse and describes for the first time the role of syndecan-4 in efficient wound healing through cell migration. CASPubMedPubMed Central Google Scholar
Tscharntke, M. et al. Impaired epidermal wound healing in vivo upon inhibition or deletion of Rac1. J. Cell Sci.120, 1480–1490 (2007). CASPubMed Google Scholar
Hayashi, K. et al. Immunocytochemistry of cell surface heparan sulfate proteoglycan in mouse tissues. A light and electron microscopic study. J. Histochem. Cytochem.35, 1079–1088 (1987). CASPubMed Google Scholar
Elenius, K. et al. Induced expression of syndecan in healing wounds. J. Cell Biol.114, 585–595 (1991). CASPubMed Google Scholar
Trautman, M. S., Kimelman, J. & Bernfield, M. Developmental expression of syndecan, an integral membrane proteoglycan, correlates with cell differentiation. Development111, 213–220 (1991). CASPubMed Google Scholar
Subramanian, S. V., Fitzgerald, M. L. & Bernfield, M. Regulated shedding of syndecan-1 and -4 ectodomains by thrombin and growth factor receptor activation. J. Biol. Chem.272, 14713–14720 (1997). CASPubMed Google Scholar
Stepp, M. A. et al. Defects in keratinocyte activation during wound healing in the syndecan-1-deficient mouse. J. Cell Sci.115, 4517–4531 (2002). Describes the generation and characterization of syndecan-1-deficient mice that, although viable and developmentally normal, exhibit aberrant epithelial and corneal wound healing. CASPubMed Google Scholar
Elenius, V., Gotte, M., Reizes, O., Elenius, K. & Bernfield, M. Inhibition by the soluble syndecan-1 ectodomains delays wound repair in mice overexpressing syndecan-1. J. Biol. Chem.279, 41928–41935 (2004). CASPubMed Google Scholar
Hodivala-Dilke, K. M., Reynolds, A. R. & Reynolds, L. E. Integrins in angiogenesis: multitalented molecules in a balancing act. Cell Tissue Res.314, 131–144 (2003). CASPubMed Google Scholar
Stupack, D. G. & Cheresh, D. A. Integrins and angiogenesis. Curr. Top. Dev. Biol.64, 207–238 (2004). CASPubMed Google Scholar
Yang, J. T., Rayburn, H. & Hynes, R. O. Embryonic mesodermal defects in α5 integrin-deficient mice. Development119, 1093–1105 (1993). CASPubMed Google Scholar
Ishiguro, K. et al. Syndecan-4 deficiency impairs the fetal vessels in the placental labyrinth. Dev. Dyn.219, 539–544 (2000). CASPubMed Google Scholar
Chen, E., Hermanson, S. & Ekker, S. C. Syndecan-2 is essential for angiogenic sprouting during zebrafish development. Blood103, 1710–1719 (2004). CASPubMed Google Scholar
Brooks, P. C., Clark, R. A. & Cheresh, D. A. Requirement of vascular integrin αvβ3 for angiogenesis. Science264, 569–571 (1994). CASPubMed Google Scholar
Brooks, P. C. et al. Integrin αvβ3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell79, 1157–1164 (1994). CASPubMed Google Scholar
Brooks, P. C. et al. Antiintegrin αvβ3 blocks human breast cancer growth and angiogenesis in human skin. J. Clin. Invest.96, 1815–1822 (1995). CASPubMedPubMed Central Google Scholar
Kim, S., Bakre, M., Yin, H. & Varner, J. A. Inhibition of endothelial cell survival and angiogenesis by protein kinase A. J. Clin. Invest.110, 933–941 (2002). CASPubMedPubMed Central Google Scholar
Stupack, D. G., Puente, X. S., Boutsaboualoy, S., Storgard, C. M. & Cheresh, D. A. Apoptosis of adherent cells by recruitment of caspase-8 to unligated integrins. J. Cell Biol.155, 459–470 (2001). Demonstrates that adherent cells undergo apoptosis in the absence of αVβ3integrin engagement as a consequence of membrane recruitment and activation of caspase-8. CASPubMedPubMed Central Google Scholar
Reynolds, L. E. et al. Enhanced pathological angiogenesis in mice lacking β3 integrin or β3 and β5 integrins. Nature Med.8, 27–34 (2002). CASPubMed Google Scholar
Reynolds, A. R. et al. Elevated Flk1 (vascular endothelial growth factor receptor 2) signaling mediates enhanced angiogenesis in β3-integrin-deficient mice. Cancer Res.64, 8643–8650 (2004). Shows that β3-deficient mice exhibit enhanced pathological angiogenesis as a result of elevated phosphorylation of VEGFR2and downstream signalling in endothelial cells. CASPubMed Google Scholar
De, S. et al. VEGF-integrin interplay controls tumor growth and vascularization. Proc. Natl Acad. Sci. USA102, 7589–7594 (2005). CASPubMedPubMed Central Google Scholar
Mahabeleshwar, G. H., Feng, W., Phillips, D. R. & Byzova, T. V. Integrin signaling is critical for pathological angiogenesis. J. Exp. Med.203, 2495–2507 (2006). Through the generation of transgenic mice that express mutant β3integrin cytoplasmic domains, the authors show that β3phosphorylation is required for VEGFR2–β3complex formation, VEGFR2 phosphorylation and pathological, but not developmental, angiogenesis. CASPubMedPubMed Central Google Scholar
Mahabeleshwar, G. H., Feng, W., Reddy, K., Plow, E. F. & Byzova, T. V. Mechanisms of integrin-vascular endothelial growth factor receptor cross-activation in angiogenesis. Circ. Res.101, 570–580 (2007). CASPubMedPubMed Central Google Scholar
Beauvais, D. M. & Rapraeger, A. C. Syndecan-1-mediated cell spreading requires signaling by αvβ3 integrins in human breast carcinoma cells. Exp. Cell Res.286, 219–232 (2003). CASPubMed Google Scholar
Fears, C. Y. & Woods, A. The role of syndecans in disease and wound healing. Matrix Biol.25, 443–456 (2006). CASPubMed Google Scholar
Jakobsson, L. et al. Heparan sulfate in trans potentiates VEGFR-mediated angiogenesis. Dev. Cell10, 625–634 (2006). CASPubMed Google Scholar
Gotte, M. et al. Role of syndecan-1 in leukocyte-endothelial interactions in the ocular vasculature. Invest. Ophthalmol. Vis. Sci.43, 1135–1141 (2002). PubMed Google Scholar
Yuan, K., Hong, T. M., Chen, J. J., Tsai, W. H. & Lin, M. T. Syndecan-1 up-regulated by ephrinB2/EphB4 plays dual roles in inflammatory angiogenesis. Blood104, 1025–1033 (2004). CASPubMed Google Scholar
Andersen, N. F. et al. Syndecan-1 and angiogenic cytokines in multiple myeloma: correlation with bone marrow angiogenesis and survival. Br. J. Haematol.128, 210–217 (2005). CASPubMed Google Scholar
Wang, A., Nomura, M., Patan, S. & Ware, J. A. Inhibition of protein kinase Cα prevents endothelial cell migration and vascular tube formation in vitro and myocardial neovascularization in vivo. Circ. Res.90, 609–616 (2002). CASPubMed Google Scholar
Bokhari, S. M., Zhou, L., Karasek, M. A., Paturi, S. G. & Chaudhuri, V. Regulation of skin microvasculature angiogenesis, cell migration, and permeability by a specific inhibitor of PKCα. J. Invest. Dermatol.126, 460–467 (2006). CASPubMed Google Scholar
Peng, X. et al. Overexpression of focal adhesion kinase in vascular endothelial cells promotes angiogenesis in transgenic mice. Cardiovasc. Res.64, 421–430 (2004). CASPubMed Google Scholar
Shen, T. L. et al. Conditional knockout of focal adhesion kinase in endothelial cells reveals its role in angiogenesis and vascular development in late embryogenesis. J. Cell Biol.169, 941–952 (2005). CASPubMedPubMed Central Google Scholar
Halder, J. et al. Focal adhesion kinase targeting using in vivo short interfering RNA delivery in neutral liposomes for ovarian carcinoma therapy. Clin. Cancer Res.12, 4916–4924 (2006). CASPubMedPubMed Central Google Scholar
Kornberg, L. J., Shaw, L. C., Spoerri, P. E., Caballero, S. & Grant, M. B. Focal adhesion kinase overexpression induces enhanced pathological retinal angiogenesis. Invest. Ophthalmol. Vis. Sci.45, 4463–4469 (2004). PubMed Google Scholar
Dormond, O., Foletti, A., Paroz, C. & Ruegg, C. NSAIDs inhibit αvβ3 integrin-mediated and Cdc42/Rac-dependent endothelial-cell spreading, migration and angiogenesis. Nature Med.7, 1041–1047 (2001). CASPubMed Google Scholar
Connolly, J. O., Simpson, N., Hewlett, L. & Hall, A. Rac regulates endothelial morphogenesis and capillary assembly. Mol. Biol. Cell13, 2474–2485 (2002). CASPubMedPubMed Central Google Scholar
Lee, T. K. et al. Rac activation is associated with hepatocellular carcinoma metastasis by up-regulation of vascular endothelial growth factor expression. Clin. Cancer Res.12, 5082–5089 (2006). CASPubMed Google Scholar
Toba, Y. et al. Expression and immunohistochemical localization of heparan sulphate proteoglycan N-syndecan in the migratory pathway from the rat olfactory placode. Eur. J. Neurosci.15, 1461–1473 (2002). PubMed Google Scholar
Hienola, A., Tumova, S., Kulesskiy, E. & Rauvala, H. N-syndecan deficiency impairs neural migration in brain. J. Cell Biol.174, 569–580 (2006). CASPubMedPubMed Central Google Scholar
Schmid, R. S. et al. α3β1 integrin modulates neuronal migration and placement during early stages of cerebral cortical development. Development131, 6023–6031 (2004). CASPubMed Google Scholar
Tate, M. C. et al. Specific β1 integrins mediate adhesion, migration, and differentiation of neural progenitors derived from the embryonic striatum. Mol. Cell Neurosci.27, 22–31 (2004). CASPubMed Google Scholar
Steigemann, P., Molitor, A., Fellert, S., Jackle, H. & Vorbruggen, G. Heparan sulfate proteoglycan syndecan promotes axonal and myotube guidance by slit/robo signaling. Curr. Biol.14, 225–230 (2004). Shows thatD. melanogastersyndecan colocalizes with Robo in cells adjacent to Slit-expressing cells and regulates localization and diffusion of Slit. Also shows that disruption of syndecan expression perturbs the biological activity of Slit. CASPubMed Google Scholar
Johnson, K. G. et al. Axonal heparan sulfate proteoglycans regulate the distribution and efficiency of the repellent slit during midline axon guidance. Curr. Biol.14, 499–504 (2004). CASPubMed Google Scholar
Rhiner, C., Gysi, S., Frohli, E., Hengartner, M. O. & Hajnal, A. Syndecan regulates cell migration and axon guidance in C. elegans. Development132, 4621–4633 (2005). CASPubMed Google Scholar
Stevens, A. & Jacobs, J. R. Integrins regulate responsiveness to Slit repellent signals. J. Neurosci.22, 4448–4455 (2002). CASPubMedPubMed Central Google Scholar
Wang, B. et al. Induction of tumor angiogenesis by Slit–Robo signaling and inhibition of cancer growth by blocking Robo activity. Cancer Cell4, 19–29 (2003). PubMed Google Scholar
Powell, E. M., Mercado, M. L., Calle-Patino, Y. & Geller, H. M. Protein kinase C mediates neurite guidance at an astrocyte boundary. Glia33, 288–297 (2001). CASPubMed Google Scholar
Wu, D. Y., Zheng, J. Q., McDonald, M. A., Chang, B. & Twiss, J. L. PKC isozymes in the enhanced regrowth of retinal neurites after optic nerve injury. Invest. Ophthalmol. Vis. Sci.44, 2783–2790 (2003). PubMed Google Scholar
Sakaue, Y., Sanada, M., Sasaki, T., Kashiwagi, A. & Yasuda, H. Amelioration of retarded neurite outgrowth of dorsal root ganglion neurons by overexpression of PKCδ in diabetic rats. Neuroreport14, 431–436 (2003). PubMed Google Scholar
Rico, B. et al. Control of axonal branching and synapse formation by focal adhesion kinase. Nature Neurosci.7, 1059–1069 (2004). CASPubMed Google Scholar
Zhao, Y. L. et al. Active Src expression is induced after rat peripheral nerve injury. Glia42, 184–193 (2003). PubMed Google Scholar
Itoh, B. et al. SRC-1, a non-receptor type of protein tyrosine kinase, controls the direction of cell and growth cone migration in C. elegans. Development132, 5161–5172 (2005). CASPubMed Google Scholar
Chun, J. T., Crispino, M. & Tocco, G. The dual response of protein kinase Fyn to neural trauma: early induction in neurons and delayed induction in reactive astrocytes. Exp. Neurol.185, 109–119 (2004). CASPubMed Google Scholar
Saito, R., Fujita, N. & Nagata, S. Overexpression of Fyn tyrosine kinase causes abnormal development of primary sensory neurons in Xenopus laevis embryos. Dev. Growth Differ.43, 229–238 (2001). CASPubMed Google Scholar
Ng, J. et al. Rac GTPases control axon growth, guidance and branching. Nature416, 442–447 (2002). CASPubMed Google Scholar
Lundquist, E. A., Reddien, P. W., Hartwieg, E., Horvitz, H. R. & Bargmann, C. I. Three C. elegans Rac proteins and several alternative Rac regulators control axon guidance, cell migration and apoptotic cell phagocytosis. Development128, 4475–4488 (2001). CASPubMed Google Scholar
Hing, H., Xiao, J., Harden, N., Lim, L. & Zipursky, S. L. Pak functions downstream of Dock to regulate photoreceptor axon guidance in Drosophila. Cell97, 853–863 (1999). CASPubMed Google Scholar
Lucanic, M., Kiley, M., Ashcroft, N., L'Etoile, N. & Cheng, H. J. The Caenorhabditis elegans P21-activated kinases are differentially required for UNC-6/netrin-mediated commissural motor axon guidance. Development133, 4549–4559 (2006). CASPubMed Google Scholar
Daniels, R. H., Hall, P. S. & Bokoch, G. M. Membrane targeting of p21-activated kinase 1 (PAK1) induces neurite outgrowth from PC12 cells. EMBO J.17, 754–764 (1998). CASPubMedPubMed Central Google Scholar
Ng, J. & Luo, L. Rho GTPases regulate axon growth through convergent and divergent signaling pathways. Neuron44, 779–793 (2004). CASPubMed Google Scholar
Chakravarti, R. & Adams, J. C. Comparative genomics of the syndecans defines an ancestral genomic context associated with matrilins in vertebrates. BMC Genomics7, 83 (2006). PubMedPubMed Central Google Scholar
Geiger, B., Bershadsky, A., Pankov, R. & Yamada, K. M. Transmembrane crosstalk between the extracellular matrix–cytoskeleton crosstalk. Nature Rev. Mol. Cell Biol.2, 793–805 (2001). CAS Google Scholar
Pankov, R. et al. Integrin dynamics and matrix assembly: tensin-dependent translocation of α5β1 integrins promotes early fibronectin fibrillogenesis. J. Cell Biol.148, 1075–1090 (2000). CASPubMedPubMed Central Google Scholar
Zaidel-Bar, R., Cohen, M., Addadi, L. & Geiger, B. Hierarchical assembly of cell-matrix adhesion complexes. Biochem. Soc. Trans.32, 416–420 (2004). CASPubMed Google Scholar
Zamir, E. et al. Dynamics and segregation of cell-matrix adhesions in cultured fibroblasts. Nature Cell Biol.2, 191–196 (2000). CASPubMed Google Scholar
Turner, C. E., Kramarcy, N., Sealock, R. & Burridge, K. Localization of paxillin, a focal adhesion protein, to smooth muscle dense plaques, and the myotendinous and neuromuscular junctions of skeletal muscle. Exp. Cell Res.192, 651–655 (1991). CASPubMed Google Scholar
Cukierman, E., Pankov, R., Stevens, D. R. & Yamada, K. M. Taking cell-matrix adhesions to the third dimension. Science294, 1708–1712 (2001). CASPubMed Google Scholar
Springer, T. A. & Wang, J. H. The three-dimensional structure of integrins and their ligands, and conformational regulation of cell adhesion. Adv. Protein Chem.68, 29–63 (2004). CASPubMed Google Scholar
Arnaout, M. A., Mahalingam, B. & Xiong, J. P. Integrin structure, allostery, and bidirectional signaling. Annu. Rev. Cell Dev. Biol.21, 381–410 (2005). CASPubMed Google Scholar
Drake, C. J., Cheresh, D. A. & Little, C. D. An antagonist of integrin αvβ3 prevents maturation of blood vessels during embryonic neovascularization. J. Cell Sci.108, 2655–2661 (1995). CASPubMed Google Scholar