A novel PKC-regulated mechanism controls CD44–ezrin association and directional cell motility (original) (raw)

• Lesley, J., Hyman, R. & Kincade, P. W. CD44 and its interaction with extracellular matrix. Adv. Immunol. 54, 271–335 (1993).
  Article CAS PubMed Google Scholar
• Naor, D., Sionov, R. V. & Ish-Shalom, D. CD44: structure, function and association with the malignant process. Adv. Cancer Res. 71, 241–319 (1997).
  Article CAS PubMed Google Scholar
• Bajorath, J. Molecular organization, structural features and ligand binding characteristics of CD44, a highly variable cell surface glycoprotein with multiple functions. Proteins 39, 103–111 (2000).
  Article CAS PubMed Google Scholar
• Bretscher, A. Regulation of cortical structure by the ezrin-radixin-moesin protein family. Curr. Opin. Cell Biol. 11, 109–116 (1999).
  Article CAS PubMed Google Scholar
• Mangeat, P., Roy, C. & Martin, M. ERM proteins in cell adhesion and membrane dynamics. Trends Cell Biol. 9, 187–192 (1999).
  Article CAS PubMed Google Scholar
• Tsukita, S. & Yonemura, S. Cortical actin organization: Lessons from ERM (ezrin/radixin/moesin) proteins. J. Biol. Chem. 274, 34507–34510 (1999).
  Article CAS PubMed Google Scholar
• Matsui, T. et al. Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J. Cell Biol. 140, 647–657 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Huang, L., Wong, T. Y. W., Lin, R. C. C. & Furthmayr, H. Replacement of threonine 558, a critical site of phosphorylation of moesin in vivo, with aspartate activates F-actin binding of moesin. Regulation by conformational change. J. Biol. Chem. 274, 12803–12810 (1999).
  Article CAS PubMed Google Scholar
• Pearson, M. A., Reczek, D., Bretscher, A. & Karplus, P. A. Structure of the ERM protein moesin reveals the FERM domain fold masked by an extended actin binding tail domain. Cell 101, 259–270 (2000).
  Article CAS PubMed Google Scholar
• Barret, C., Roy, C., Montcourrier, P., Mangeat, P. & Niggli, V. Mutagenesis of the phosphatidylinositol 4,5-bisphosphate (PIP2) binding site in the NH2-terminal domain of ezrin correlates with its altered cellular distribution. J. Cell Biol. 151, 1067–1080 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Mackay, D. J. G., Esch, F., Furthmayr, H. & Hall, A. Rho- and Rac- dependent assembly of focal adhesion complexes and actin filaments in permeabilized fibroblasts: an essential role for ezrin/radixin/moesin proteins. J. Cell Biol. 138, 927–938 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Takahashi, K. et al. Direct interaction of the Rho GDP dissociation inhibitor with ezrin/radixin/moesin initiates the activation of the Rho small G protein. J. Biol. Chem. 272, 23371–23375 (1997).
  Article CAS PubMed Google Scholar
• Gautreau, A., Louvard, D. & Arpin, M. Morphogenic effects of ezrin require a phosphorylation-induced transition from oligomers to monomers at the plasma membrane. J. Cell Biol. 150, 193–203 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Shaw, R. J. et al. The Nf2 tumor suppressor, merlin, functions in Rac-dependent signaling. Dev. Cell 1, 63–72 (2001).
  Article CAS PubMed Google Scholar
• Crepaldi, T., Gautreau, A., Comoglio, P. M., Louvard, D. & Arpin, M. Ezrin is an effector of hepatocyte growth factor-mediated migration and morphogenesis in epithelial cells. J. Cell Biol. 138, 423–434 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Lamb, R. F. et al. Essential functions of ezrin in maintenance of cell shape and lamellipodial extension in normal and transformed fibroblasts. Curr. Biol. 7, 682–688 (1997).
  Article CAS PubMed Google Scholar
• Castelo, L. & Jay, D. G. Radixin is involved in lamellipodial stability during nerve growth cone motility. Mol. Biol. Cell 10, 1511–1520 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Ng, T. et al. Ezrin is a downstream effector of trafficking PKC-integrin complexes involved in the control of cell motility. EMBO J. 20, 2723–2741 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Legg, J. W. & Isacke, C. M. Identification and functional analysis of the ezrin-binding site in the hyaluronan receptor, CD44. Curr. Biol. 8, 705–708 (1998).
  Article CAS PubMed Google Scholar
• Yonemura, S. et al. Ezrin/radixin/moesin (ERM) proteins bind to a positively charged amino acid cluster in the juxta-membrane cytoplasmic domain of CD44, CD43 and ICAM-2. J. Cell Biol. 140, 885–895 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Morrison H. et al. The NF2 tumor suppressor gene product, merlin, mediates contact inhibition of growth through interactions with CD44. Genes Dev. 15, 968–980 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Peck, D. & Isacke, C. M. Hyaluronan-dependent cell migration can be blocked by a CD44 cytoplasmic domain peptide containing a phosphoserine at position 325. J. Cell Sci. 111, 1595–1601 (1998).
  CAS PubMed Google Scholar
• Lewis, C. A., Townsend, P. A. & Isacke, C. M. Ca2+/calmodulin-dependent protein kinase mediates the phosphorylation of CD44 required for cell migration on hyaluronan. Biochem. J. 357, 843–850 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Peck, D. & Isacke, C. M. CD44 phosphorylation regulates melanoma cell and fibroblast migration on, but not attachment to, a hyaluronan substratum. Curr. Biol. 6, 884–890 (1996).
  Article CAS PubMed Google Scholar
• Kalomiris, E. L. & Bourguignon, L. Y. Lymphoma protein kinase C is associated with the transmembrane glycoprotein GP85 and may function in GP85-ankyrin binding. J. Biol. Chem. 264, 8113–8119 (1989).
  CAS PubMed Google Scholar
• Camp, R. L., Kraus, T. A. & Puré, E. Variations in the cytoskeletal interaction and post-translational modification of the CD44 homing receptor in macrophages. J. Cell. Biol. 115, 1283–1292 (1991).
  Article CAS PubMed Google Scholar
• Neame, S. J. & Isacke, C. M. Phosphorylation of CD44 in vivo requires both Ser323 and Ser325, but does not regulate membrane localisation or cytoskeletal interaction in epithelial cells. EMBO J. 11, 4733–4738 (1992).
  Article CAS PubMed PubMed Central Google Scholar
• Ng, T. et al. PKCα regulates β1 integrin-dependent motility, through association and control of integrin traffic. EMBO J. 18, 3909–3923 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Ng, T. et al. Imaging protein kinase Cα activation in cells. Science 283, 2085–2089 (1999).
  Article CAS PubMed Google Scholar
• Parsons, M. & Ng, T. Intracellular coupling of adhesion receptors: molecular proximity measurements. In Adams, J. (ed.) Methods in Cell-Matrix Adhesion. Academic Press, San Diego (in press).
• Herreros, J., Ng, T. & Schiavo, G. Lipid rafts act as specialized domains for tetanus toxin binding and internalization into neurons. Mol. Biol. Cell 12, 2947–2960 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Squire, A. & Bastiaens, P. I. Three dimensional image restoration in fluorescence lifetime imaging microscopy. J. Microsc. 193, 36–49 (1999).
  Article CAS PubMed Google Scholar
• Bastiaens, P. I. & Squire, A. Fluorescence lifetime imaging microscopy: spatial resolution of biochemical processes in the cell. Trends Cell Biol. 9, 48–52 (1999).
  Article CAS PubMed Google Scholar
• Selvin, P. R. The renaissance of fluorescence resonance energy transfer. Nature Struct. Biol. 7, 730–734 (2000).
  Article CAS PubMed Google Scholar
• Potter, L. R. & Hunter T. Activation of protein kinase C stimulates the dephosphorylation of natriuretic peptide receptor-B at a single serine residue. J. Biol. Chem. 275, 31099–31106 (2000).
  Article CAS PubMed Google Scholar
• Levy, M., Jing, J., Chikvashvili, D., Thornhill, W. B. & Lotan, I. Activation of a metabotropic glutamate receptor and protein kinase C reduce the extent of inactivation of the K+ channel Kv1.1/Kvβ1.1 via dephosphorylation of Kv1.1. J. Biol. Chem. 273, 6495–6502 (1998).
  Article CAS PubMed Google Scholar
• Rigot, V. et al. Integrin ligation and PKC activation are required for migration of colon carcinoma cells. J. Cell Sci. 111, 3119–3127 (1998).
  CAS PubMed Google Scholar
• Thomas, L., Etoh, T., Stamenkovic, I., Mihm, M. C. & Byers, H. R. Migration of human melanoma cells on hyaluronate is related to CD44 expression. J. Invest. Dermatol. 100, 115–120 (1993).
  Article CAS PubMed Google Scholar
• Göebeler, M., Kaufmann, D., Brocker, E.-B. & Klein, C. E. Migration of highly aggressive melanoma cells on hyaluronic acid is associated with functional changes, increased turnover and shedding of CD44 receptors. J. Cell Sci. 109, 1957–1964 (1996).
  PubMed Google Scholar
• Herrera-Gayol, A. & Jothy, S. CD44 modulates Hs578T human breast cancer cell adhesion, migration, and invasiveness. Exp. Mol. Pathol. 66, 99–108 (1999).
  Article CAS PubMed Google Scholar
• Bourguignon, L. Y, Zhu, H., Shao, L. & Chen, Y. W. CD44 interaction with tiam1 promotes Rac1 signaling and hyaluronic acid-mediated breast tumor cell migration. J. Biol. Chem. 275, 1829–1838 (2000).
  Article CAS PubMed Google Scholar
• Ballestrem, C., Wehrle-Haller, B., Hinz, B. & Imhof, B. A. Actin-dependent lamellipodia formation and microtubule-dependent tail retraction control-directed cell migration. Mol. Biol. Cell 11, 2999–3012 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Imamura, H. et al. Rho and Rab small G proteins coordinately reorganize stress fibers and focal adhesions in MDCK cells. Mol. Biol. Cell 9, 2561–2575 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Taunton, J. et al. Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP. J. Cell Biol. 148, 519–530 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Parekh, D. B. et al. β1-integrin and PTEN control the phosphorylation of protein kinase C. Biochem. J. 352, 425–433(2000).
  Article CAS PubMed PubMed Central Google Scholar
• Bastiaens, P. I. H. & Jovin, T. M. Fluorescence resonance energy transfer microscopy. In Celis, J. (ed.) Cell Biology: A Laboratory Handbook. Academic Press, New York, pp. 136–146 (1998).
  Google Scholar
• Neame, S. J. & Isacke, C. M. The cytoplasmic tail of CD44 is required for basolateral localisation in epithelial MDCK cells but does not mediate association with the detergent insoluble cytoskeleton of fibroblasts. J. Cell Biol. 121, 1299–1310 (1993).
  Article CAS PubMed Google Scholar
• Lamb, R. F. et al. AP-1-mediated invasion requires increased expression of the hyaluronan receptor CD44. Mol. Cell. Biol. 17, 963–976 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Zarkowska, T., U, S., Harlow, E. & Mittnacht, S. Monoclonal antibodies specific for underphosphorylated retinoblastoma protein identify a cell cycle regulated phosphorylation site targeted by CDKs. Oncogene 14, 249–254 (1997).
  Article CAS PubMed Google Scholar
• Zicha, D., Dunn, G. & Jones, G. Analyzing chemotaxis using the Dunn direct-viewing chamber. Methods Mol. Biol. 75, 449–457 (1997).
  CAS PubMed Google Scholar