Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling (original) (raw)

• Lemmon, M. A. Phosphoinositide recognition domains. Traffic 4, 201–213 (2003).
  Article CAS PubMed Google Scholar
• Simonsen, A., Wurmser, A. E., Emr, S. D. & Stenmark, H. The role of phosphoinositides in membrane transport. Curr. Opin. Cell Biol. 13, 485–492 (2001).
  Article CAS PubMed Google Scholar
• Comer, F. I. & Parent, C. A. PI 3-kinases and PTEN: how opposites chemoattract. Cell 109, 541–544 (2002).
  Article CAS PubMed Google Scholar
• Simons, K. & Toomre, D. Lipid rafts and signal transduction. Nature Rev. Mol. Cell Biol. 1, 31–39 (2000). This review and references 5, 9 and 129 (also reviews) present various models for the formation of lipid rafts.
  Article CAS Google Scholar
• Mayor, S. & Riezman, H. Sorting GPI-anchored proteins. Nature Rev. Mol. Cell Biol. 5, 110–120 (2004).
  Article CAS Google Scholar
• Jacob, R. et al. Annexin II is required for apical transport in polarized epithelial cells. J. Biol. Chem. 279, 3680–3684 (2004).
  Article CAS PubMed Google Scholar
• Hancock, J. F. Ras proteins: different signals from different locations. Nature Rev. Mol. Cell Biol. 4, 373–384 (2003).
  Article CAS Google Scholar
• Parton, R. G. & Hancock, J. F. Lipid rafts and plasma membrane microorganization: insights from Ras. Trends Cell Biol. 14, 141–147 (2004).
  Article CAS PubMed Google Scholar
• Kusumi, A., Koyama-Honda, I. & Suzuki, K. Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic 5, 213–230 (2004).
  Article CAS PubMed Google Scholar
• Drevot, P. et al. TCR signal initiation machinery is pre-assembled and activated in a subset of membrane rafts. EMBO J. 21, 1899–1908 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Pierce, S. K. Lipid rafts and B-cell activation. Nature Rev. Immunol. 2, 96–105 (2002).
  Article CAS Google Scholar
• Saltiel, A. R. & Pessin, J. E. Insulin signaling in microdomains of the plasma membrane. Traffic 4, 711–716 (2003).
  Article CAS PubMed Google Scholar
• Tansey, M. G., Baloh, R. H., Milbrandt, J. & Johnson, E. M. Jr. GFRα-mediated localization of RET to lipid rafts is required for effective downstream signaling, differentiation, and neuronal survival. Neuron 25, 611–623 (2000).
  Article CAS PubMed Google Scholar
• Paratcha, G., Ledda, F. & Ibanez, C. F. The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell 113, 867–879 (2003).
  Article CAS PubMed Google Scholar
• Legler, D. F., Micheau, O., Doucey, M. A., Tschopp, J. & Bron, C. Recruitment of TNF receptor 1 to lipid rafts is essential for TNFα-mediated NF-κB activation. Immunity 18, 655–664 (2003).
  Article CAS PubMed Google Scholar
• Wang, D. et al. CD3/CD28 costimulation-induced NF-κB activation is mediated by recruitment of protein kinase C-θ, Bcl10, and IκB kinase β to the immunological synapse through CARMA1. Mol. Cell. Biol. 24, 164–171 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Sehgal, P. B., Guo, G. G., Shah, M., Kumar, V. & Patel, K. Cytokine signaling: STATS in plasma membrane rafts. J. Biol. Chem. 277, 12067–12074 (2002).
  Article CAS PubMed Google Scholar
• Marmor, M. D. & Yarden, Y. Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene 23, 2057–2070 (2004).
  Article CAS PubMed Google Scholar
• Nesterov, A., Carter, R. E., Sorkina, T., Gill, G. N. & Sorkin, A. Inhibition of the receptor-binding function of clathrin adaptor protein AP-2 by dominant-negative mutant μ2 subunit and its effects on endocytosis. EMBO J. 18, 2489–2499 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Polo, S. et al. A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416, 451–455 (2002). Shows that UIM-containing proteins, which bind ubiquitin, recruit ubiquitin ligases and are themselves monoubiquitylated.
  Article CAS PubMed Google Scholar
• Hicke, L. & Riezman, H. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84, 277–287 (1996).
  Article CAS PubMed Google Scholar
• Haglund, K. et al. Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nature Cell Biol. 5, 461–466 (2003).
  Article CAS PubMed Google Scholar
• Legendre-Guillemin, V., Wasiak, S., Hussain, N. K., Angers, A. & McPherson, P. S. ENTH/ANTH proteins and clathrin-mediated membrane budding. J. Cell Sci. 117, 9–18 (2004).
  Article CAS PubMed Google Scholar
• French, A. R., Tadaki, D. K., Niyogi, S. K. & Lauffenburger, D. A. Intracellular trafficking of epidermal growth factor family ligands is directly influenced by the pH sensitivity of the receptor/ligand interaction. J. Biol. Chem. 270, 4334–4340 (1995).
  Article CAS PubMed Google Scholar
• Bao, J. et al. Threonine phosphorylation diverts internalized epidermal growth factor receptors from a degradative pathway to the recycling endosome. J. Biol. Chem. 275, 26178–26186 (2000).
  Article CAS PubMed Google Scholar
• Katzmann, D. J., Babst, M. & Emr, S. D. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106, 145–155 (2001).
  Article CAS PubMed Google Scholar
• Bache, K. G., Raiborg, C., Mehlum, A. & Stenmark, H. STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J. Biol. Chem. 278, 12513–12521 (2003).
  Article CAS PubMed Google Scholar
• Raiborg, C., Bache, K. G., Mehlum, A., Stang, E. & Stenmark, H. Hrs recruits clathrin to early endosomes. EMBO J. 20, 5008–5021 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Katzmann, D. J., Stefan, C. J., Babst, M. & Emr, S. D. Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J. Cell Biol. 162, 413–423 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Bache, K. G., Brech, A., Mehlum, A. & Stenmark, H. Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J. Cell Biol. 162, 435–442 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Gruenberg, J. & Stenmark, H. The biogenesis of multivesicular endosomes. Nature Rev. Mol. Cell Biol. 5, 317–323 (2004).
  Article CAS Google Scholar
• Parton, R. G. & Richards, A. A. Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 4, 724–738 (2003).
  Article CAS PubMed Google Scholar
• Nichols, B. J. GM1-containing lipid rafts are depleted within clathrin-coated pits. Curr. Biol. 13, 686–690 (2003).
  Article CAS PubMed Google Scholar
• Nichols, B. Caveosomes and endocytosis of lipid rafts. J. Cell Sci. 116, 4707–4714 (2003).
  Article CAS PubMed Google Scholar
• Sato, S. B. et al. Distribution and transport of cholesterol-rich membrane domains monitored by a membrane-impermeant fluorescent polyethylene glycol-derivatized cholesterol. J. Biol. Chem. 279, 23790–23796 (2004).
  Article CAS PubMed Google Scholar
• Sharma, D. K. et al. Selective stimulation of caveolar endocytosis by glycosphingolipids and cholesterol. Mol. Biol. Cell 15, 3114–3122 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Nabi, I. R. & Le, P. U. Caveolae/raft-dependent endocytosis. J. Cell Biol. 161, 673–677 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Parton, R. G., Joggerst, B. & Simons, K. Regulated internalization of caveolae. J. Cell Biol. 127, 1199–1215 (1994).
  Article CAS PubMed Google Scholar
• Pelkmans, L., Puntener, D. & Helenius, A. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 296, 535–539 (2002).
  Article CAS PubMed Google Scholar
• Mundy, D. I., Machleidt, T., Ying, Y. S., Anderson, R. G. & Bloom, G. S. Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton. J. Cell Sci. 115, 4327–4339 (2002).
  Article CAS PubMed Google Scholar
• Pelkmans, L., Burli, T., Zerial, M. & Helenius, A. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 118, 767–780 (2004).
  Article CAS PubMed Google Scholar
• Le, P. U. & Nabi, I. R. Distinct caveolae-mediated endocytic pathways target the Golgi apparatus and the endoplasmic reticulum. J. Cell Sci. 116, 1059–1071 (2003).
  Article CAS PubMed Google Scholar
• Lu, Z., Ghosh, S., Wang, Z. & Hunter, T. Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of β-catenin, and enhanced tumor cell invasion. Cancer Cell 4, 499–515 (2003).
  Article CAS PubMed Google Scholar
• Parton, R. G. Caveolae — from ultrastructure to molecular mechanisms. Nature Rev. Mol. Cell Biol. 4, 162–167 (2003).
  Article CAS Google Scholar
• Lamaze, C. et al. Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol. Cell 7, 661–671 (2001).
  Article CAS PubMed Google Scholar
• Sabharanjak, S., Sharma, P., Parton, R. G. & Mayor, S. GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev. Cell 2, 411–423 (2002). Shows that GPI-anchored proteins can be internalized through a caveolae-negative, lipid-raft pathway, can reach tubular–vesicular endosomes and can traffic back to the plasma membrane through the recycling endosome compartment. Provides the first direct evidence for crosstalk between the lipid-raft internalization pathway and the classic endosomal system.
  Article CAS PubMed Google Scholar
• Kirchhausen, T. Clathrin adaptors really adapt. Cell 109, 413–416 (2002).
  Article CAS PubMed Google Scholar
• Schlessinger, J. Ligand-induced, receptor-mediated dimerization and activation of EGF receptor. Cell 110, 669–672 (2002).
  Article CAS PubMed Google Scholar
• Mineo, C., Gill, G. N. & Anderson, R. G. Regulated migration of epidermal growth factor receptor from caveolae. J. Biol. Chem. 274, 30636–30643 (1999).
  Article CAS PubMed Google Scholar
• Roepstorff, K., Thomsen, P., Sandvig, K. & van Deurs, B. Sequestration of epidermal growth factor receptors in non-caveolar lipid rafts inhibits ligand binding. J. Biol. Chem. 277, 18954–18960 (2002).
  Article CAS PubMed Google Scholar
• Pike, L. J. & Casey, L. Localization and turnover of phosphatidylinositol 4,5-bisphosphate in caveolin-enriched membrane domains. J. Biol. Chem. 271, 26453–26456 (1996).
  Article CAS PubMed Google Scholar
• Yamabhai, M. & Anderson, R. G. Second cysteine-rich region of epidermal growth factor receptor contains targeting information for caveolae/rafts. J. Biol. Chem. 277, 24843–24846 (2002).
  Article CAS PubMed Google Scholar
• Anderson, R. G. The caveolae membrane system. Annu. Rev. Biochem. 67, 199–225 (1998).
  Article CAS PubMed Google Scholar
• de Melker, A. A., van der Horst, G., Calafat, J., Jansen, H. & Borst, J. c-Cbl ubiquitinates the EGF receptor at the plasma membrane and remains receptor associated throughout the endocytic route. J. Cell Sci. 114, 2167–2178 (2001).
  Article CAS PubMed Google Scholar
• Peter, B. J. et al. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495–499 (2004).
  Article CAS PubMed Google Scholar
• Soubeyran, P., Kowanetz, K., Szymkiewicz, I., Langdon, W. Y. & Dikic, I. Cbl–CIN85–endophilin complex mediates ligand-induced downregulation of EGF receptors. Nature 416, 183–187 (2002).
  Article CAS PubMed Google Scholar
• Wilde, A. et al. EGF receptor signaling stimulates SRC kinase phosphorylation of clathrin, influencing clathrin redistribution and EGF uptake. Cell 96, 677–687 (1999).
  Article CAS PubMed Google Scholar
• Confalonieri, S., Salcini, A. E., Puri, C., Tacchetti, C. & Di Fiore, P. P. Tyrosine phosphorylation of Eps15 is required for ligand-regulated, but not constitutive, endocytosis. J. Cell Biol. 150, 905–912 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Salcini, A. E., Chen, H., Iannolo, G., De Camilli, P. & Di Fiore, P. P. Epidermal growth factor pathway substrate 15, Eps15. Int. J. Biochem. Cell Biol. 31, 805–809 (1999).
  Article CAS PubMed Google Scholar
• Katzmann, D. J., Odorizzi, G. & Emr, S. D. Receptor downregulation and multivesicular-body sorting. Nature Rev. Mol. Cell Biol. 3, 893–905 (2002).
  Article CAS Google Scholar
• Bache, K. G., Raiborg, C., Mehlum, A., Madshus, I. H. & Stenmark, H. Phosphorylation of Hrs downstream of the epidermal growth factor receptor. Eur. J. Biochem. 269, 3881–3887 (2002).
  Article CAS PubMed Google Scholar
• McPherson, P. S., Kay, B. K. & Hussain, N. K. Signaling on the endocytic pathway. Traffic 2, 375–384 (2001).
  Article CAS PubMed Google Scholar
• Yarden, Y. & Sliwkowski, M. X. Untangling the ErbB signalling network. Nature Rev. Mol. Cell Biol. 2, 127–137 (2001).
  Article CAS Google Scholar
• Wells, A. et al. Ligand-induced transformation by a noninternalizing epidermal growth factor receptor. Science 247, 962–964 (1990).
  Article CAS PubMed Google Scholar
• Di Fiore, P. P. & Gill, G. N. Endocytosis and mitogenic signaling. Curr. Opin. Cell Biol. 11, 483–488 (1999).
  Article CAS PubMed Google Scholar
• Vieira, A. V., Lamaze, C. & Schmid, S. L. Control of EGF receptor signaling by clathrin-mediated endocytosis. Science 274, 2086–2089 (1996).
  Article CAS PubMed Google Scholar
• Di Guglielmo, G. M., Baass, P. C., Ou, W. J., Posner, B. I. & Bergeron, J. J. Compartmentalization of SHC, GRB2 and mSOS, and hyperphosphorylation of Raf-1 by EGF but not insulin in liver parenchyma. EMBO J. 13, 4269–4277 (1994). Together, references 66 and 67 were the first to show that signalling occurs during EGFR endocytosis.
  Article CAS PubMed PubMed Central Google Scholar
• Haugh, J. M., Huang, A. C., Wiley, H. S., Wells, A. & Lauffenburger, D. A. Internalized epidermal growth factor receptors participate in the activation of p21(ras) in fibroblasts. J. Biol. Chem. 274, 34350–34360 (1999).
  Article CAS PubMed Google Scholar
• Kranenburg, O., Verlaan, I. & Moolenaar, W. H. Dynamin is required for the activation of mitogen-activated protein (MAP) kinase by MAP kinase kinase. J. Biol. Chem. 274, 35301–35304 (1999).
  Article CAS PubMed Google Scholar
• Wang, Y., Pennock, S., Chen, X. & Wang, Z. Endosomal signaling of epidermal growth factor receptor stimulates signal transduction pathways leading to cell survival. Mol. Cell. Biol. 22, 7279–7290 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Howe, C. L., Valletta, J. S., Rusnak, A. S. & Mobley, W. C. NGF signaling from clathrin-coated vesicles: evidence that signaling endosomes serve as a platform for the Ras–MAPK pathway. Neuron 32, 801–814 (2001).
  Article CAS PubMed Google Scholar
• Teis, D., Wunderlich, W. & Huber, L. A. Localization of the MP1–MAPK scaffold complex to endosomes is mediated by p14 and required for signal transduction. Dev. Cell 3, 803–814 (2002).
  Article CAS PubMed Google Scholar
• Ohba, Y., Kurokawa, K. & Matsuda, M. Mechanism of the spatio-temporal regulation of Ras and Rap1. EMBO J. 22, 859–869 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Roy, S., Wyse, B. & Hancock, J. F. H-Ras signaling and K-Ras signaling are differentially dependent on endocytosis. Mol. Cell. Biol. 22, 5128–5140 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Carpenter, G. The EGF receptor: a nexus for trafficking and signaling. Bioessays 22, 697–707 (2000).
  Article CAS PubMed Google Scholar
• Mineo, C., James, G. L., Smart, E. J. & Anderson, R. G. Localization of epidermal growth factor-stimulated Ras/Raf-1 interaction to caveolae membrane. J. Biol. Chem. 271, 11930–11935 (1996).
  Article CAS PubMed Google Scholar
• Furuchi, T. & Anderson, R. G. Cholesterol depletion of caveolae causes hyperactivation of extracellular signal-related kinase (ERK). J. Biol. Chem. 273, 21099–21104 (1998).
  Article CAS PubMed Google Scholar
• Vaudry, D., Stork, P. J., Lazarovici, P. & Eiden, L. E. Signaling pathways for PC12 cell differentiation: making the right connections. Science 296, 1648–1649 (2002).
  Article CAS PubMed Google Scholar
• Pennock, S. & Wang, Z. Stimulation of cell proliferation by endosomal epidermal growth factor receptor as revealed through two distinct phases of signaling. Mol. Cell. Biol. 23, 5803–5815 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Levkowitz, G. et al. c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev. 12, 3663–3674 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Klapper, L. N., Waterman, H., Sela, M. & Yarden, Y. Tumor-inhibitory antibodies to HER-2/ErbB-2 may act by recruiting c-Cbl and enhancing ubiquitination of HER-2. Cancer Res. 60, 3384–3388 (2000).
  CAS PubMed Google Scholar
• Slamon, D. J. et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N. Engl. J. Med. 344, 783–792 (2001).
  Article CAS PubMed Google Scholar
• Mohney, R. P. et al. Intersectin activates Ras but stimulates transcription through an independent pathway involving JNK. J. Biol. Chem. 278, 47038–47045 (2003).
  Article CAS PubMed Google Scholar
• Miaczynska, M. et al. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 116, 445–456 (2004).
  Article CAS PubMed Google Scholar
• Derynck, R. & Zhang, Y. E. Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature 425, 577–584 (2003).
  Article CAS PubMed Google Scholar
• Wrana, J. L., Attisano, L., Wieser, R., Ventura, F. & Massague, J. Mechanism of activation of the TGF-β receptor. Nature 370, 341–347 (1994).
  Article CAS PubMed Google Scholar
• Tsukazaki, T., Chiang, T. A., Davison, A. F., Attisano, L. & Wrana, J. L. SARA, a FYVE domain protein that recruits Smad2 to the TGFβ receptor. Cell 95, 779–791 (1998).
  Article CAS PubMed Google Scholar
• Kavsak, P. et al. Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGFβ receptor for degradation. Mol. Cell 6, 1365–1375 (2000).
  CAS PubMed Google Scholar
• Ebisawa, T. et al. Smurf1 interacts with transforming growth factor-β type I receptor through Smad7 and induces receptor degradation. J. Biol. Chem. 276, 12477–12480 (2001).
  Article CAS PubMed Google Scholar
• Zwaagstra, J. C., Kassam, Z. & O'Connor-McCourt, M. D. Down-regulation of transforming growth factor-β receptors: cooperativity between the types I, II, and III receptors and modulation at the cell surface. Exp. Cell Res. 252, 352–362 (1999).
  Article CAS PubMed Google Scholar
• Garamszegi, N. et al. Transforming growth factor β receptor signaling and endocytosis are linked through a COOH terminal activation motif in the type I receptor. Mol. Biol. Cell 12, 2881–2893 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Anders, R. A., Dore, J. J. Jr, Arline, S. L., Garamszegi, N. & Leof, E. B. Differential requirement for type I and type II transforming growth factor β receptor kinase activity in ligand-mediated receptor endocytosis. J. Biol. Chem. 273, 23118–23125 (1998).
  Article CAS PubMed Google Scholar
• Ehrlich, M., Shmuely, A. & Henis, Y. I. A single internalization signal from the di-leucine family is critical for constitutive endocytosis of the type II TGF-β receptor. J. Cell Sci. 114, 1777–1786 (2001).
  Article CAS PubMed Google Scholar
• Di Guglielmo, G. M., Le Roy, C., Goodfellow, A. F. & Wrana, J. L. Distinct endocytic pathways regulate TGF-β receptor signalling and turnover. Nature Cell Biol. 5, 410–421 (2003). Shows that cell-surface TGFβRs are subjected to a dynamic compartmentalization between raft and non-raft membranes, and can traffic through distinct clathrin-dependent and clathrin-independent endocytic routes that regulate signalling and degradation, respectively.
  Article CAS PubMed Google Scholar
• Yao, D., Ehrlich, M., Henis, Y. I. & Leof, E. B. Transforming growth factor-β receptors interact with AP2 by direct binding to β2 subunit. Mol. Biol. Cell 13, 4001–4012 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Chen, W. et al. β-arrestin 2 mediates endocytosis of type III TGF-β receptor and down-regulation of its signaling. Science 301, 1394–1397 (2003).
  Article CAS PubMed Google Scholar
• Hayes, S., Chawla, A. & Corvera, S. TGFβ receptor internalization into EEA1-enriched early endosomes: role in signaling to Smad2. J. Cell Biol. 158, 1239–1249 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Mitchell, H., Choudhury, A., Pagano, R. E. & Leof, E. B. Ligand-dependent and-independent TGF-β receptor recycling regulated by clathrin-mediated endocytosis and Rab11. Mol. Biol. Cell 15, 4166–4178 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Itoh, F. et al. The FYVE domain in Smad anchor for receptor activation (SARA) is sufficient for localization of SARA in early endosomes and regulates TGF-β/Smad signalling. Genes Cells 7, 321–331 (2002).
  Article CAS PubMed Google Scholar
• Panopoulou, E. et al. Early endosomal regulation of Smad-dependent signaling in endothelial cells. J. Biol. Chem. 277, 18046–18052 (2002).
  Article CAS PubMed Google Scholar
• Lin, H. K., Bergmann, S. & Pandolfi, P. P. Cytoplasmic PML function in TGF-β signalling. Nature 431, 205–211 (2004).
  Article CAS PubMed Google Scholar
• Miura, S. et al. Hgs (Hrs), a FYVE domain protein, is involved in Smad signaling through cooperation with SARA. Mol. Cell. Biol. 20, 9346–9355 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Razani, B. et al. Caveolin-1 regulates transforming growth factor (TGF)-β/SMAD signaling through an interaction with the TGF-β type I receptor. J. Biol. Chem. 276, 6727–6738 (2001).
  Article CAS PubMed Google Scholar
• Lu, Z. et al. Transforming growth factor β activates Smad2 in the absence of receptor endocytosis. J. Biol. Chem. 277, 29363–29368 (2002).
  Article CAS PubMed Google Scholar
• Razani, B., Woodman, S. E. & Lisanti, M. P. Caveolae: from cell biology to animal physiology. Pharmacol. Rev. 54, 431–467 (2002).
  Article CAS PubMed Google Scholar
• Dyson, S. & Gurdon, J. B. The interpretation of position in a morphogen gradient as revealed by occupancy of activin receptors. Cell 93, 557–568 (1998).
  Article CAS PubMed Google Scholar
• Hemar, A. et al. Endocytosis of interleukin 2 receptors in human T lymphocytes: distinct intracellular localization and fate of the receptor α, β, and γ chains. J. Cell Biol. 129, 55–64 (1995).
  Article CAS PubMed Google Scholar
• Benlimame, N., Le, P. U. & Nabi, I. R. Localization of autocrine motility factor receptor to caveolae and clathrin-independent internalization of its ligand to smooth endoplasmic reticulum. Mol. Biol. Cell 9, 1773–1786 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Le, P. U., Guay, G., Altschuler, Y. & Nabi, I. R. Caveolin-1 is a negative regulator of caveolae-mediated endocytosis to the endoplasmic reticulum. J. Biol. Chem. 277, 3371–3379 (2002).
  Article CAS PubMed Google Scholar
• Pelkmans, L., Kartenbeck, J. & Helenius, A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nature Cell Biol. 3, 473–483 (2001). This is an elegant study of a viral internalization route through a caveolar/lipid-raft endocytic pathway.
  Article CAS PubMed Google Scholar
• Nichols, B. J. A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex. Nature Cell Biol. 4, 374–378 (2002).
  Article CAS PubMed Google Scholar
• Nichols, B. J. et al. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J. Cell Biol. 153, 529–541 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Denef, N., Neubuser, D., Perez, L. & Cohen, S. M. Hedgehog induces opposite changes in turnover and subcellular localization of patched and smoothened. Cell 102, 521–531 (2000).
  Article CAS PubMed Google Scholar
• Incardona, J. P. et al. Receptor-mediated endocytosis of soluble and membrane-tethered Sonic hedgehog by Patched-1. Proc. Natl Acad. Sci. USA 97, 12044–12049 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Zhu, A. J., Zheng, L., Suyama, K. & Scott, M. P. Altered localization of Drosophila Smoothened protein activates Hedgehog signal transduction. Genes Dev. 17, 1240–1252 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Incardona, J. P., Gruenberg, J. & Roelink, H. Sonic hedgehog induces the segregation of patched and smoothened in endosomes. Curr. Biol. 12, 983–995 (2002). In this study, the authors propose a model in which the trafficking of Ptc–Shh towards lysosomes regulates Smo signalling activity.
  Article CAS PubMed Google Scholar
• Karpen, H. E. et al. The sonic hedgehog receptor patched associates with caveolin-1 in cholesterol-rich microdomains of the plasma membrane. J. Biol. Chem. 276, 19503–19511 (2001).
  Article CAS PubMed Google Scholar
• Rietveld, A., Neutz, S., Simons, K. & Eaton, S. Association of sterol- and glycosylphosphatidylinositol-linked proteins with Drosophila raft lipid microdomains. J. Biol. Chem. 274, 12049–12054 (1999).
  Article CAS PubMed Google Scholar
• Dubois, L., Lecourtois, M., Alexandre, C., Hirst, E. & Vincent, J. P. Regulated endocytic routing modulates wingless signaling in Drosophila embryos. Cell 105, 613–624 (2001). This study links the distribution of Wg, its signalling and its trafficking. It shows that the range of Wg signalling is controlled by its lysosomal degradation, and is regulated by EGF.
  Article CAS PubMed Google Scholar
• Chen, W. et al. Dishevelled 2 recruits β-arrestin 2 to mediate Wnt5A-stimulated endocytosis of Frizzled 4. Science 301, 1391–1394 (2003).
  Article CAS PubMed Google Scholar
• Mao, B. et al. Kremen proteins are Dickkopf receptors that regulate Wnt/β-catenin signalling. Nature 417, 664–667 (2002).
  Article CAS PubMed Google Scholar
• Willert, K. et al. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423, 448–452 (2003).
  Article CAS PubMed Google Scholar
• Zacharias, D. A., Violin, J. D., Newton, A. C. & Tsien, R. Y. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296, 913–916 (2002).
  Article CAS PubMed Google Scholar
• Hurley, J. H. & Meyer, T. Subcellular targeting by membrane lipids. Curr. Opin. Cell Biol. 13, 146–152 (2001).
  Article CAS PubMed Google Scholar
• Varma, R. & Mayor, S. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394, 798–801 (1998).
  Article CAS PubMed Google Scholar
• Friedrichson, T. & Kurzchalia, T. V. Microdomains of GPI-anchored proteins in living cells revealed by crosslinking. Nature 394, 802–805 (1998).
  Article CAS PubMed Google Scholar
• Harder, T., Scheiffele, P., Verkade, P. & Simons, K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141, 929–942 (1998). Shows that proteins can be segregated between lipid-raft microdomains and non-lipid-raft membranes.
  Article CAS PubMed PubMed Central Google Scholar
• Schuck, S., Honsho, M., Ekroos, K., Shevchenko, A. & Simons, K. Resistance of cell membranes to different detergents. Proc. Natl Acad. Sci. USA 100, 5795–5800 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Anderson, R. G. & Jacobson, K. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296, 1821–1825 (2002).
  Article CAS PubMed Google Scholar
• Pike, L. J. Lipid rafts: heterogeneity on the high seas. Biochem. J. 378, 281–292 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• McCabe, J. B. & Berthiaume, L. G. N-terminal protein acylation confers localization to cholesterol, sphingolipid-enriched membranes but not to lipid rafts/caveolae. Mol. Biol. Cell 12, 3601–3617 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Kimura, A., Baumann, C. A., Chiang, S. H. & Saltiel, A. R. The sorbin homology domain: a motif for the targeting of proteins to lipid rafts. Proc. Natl Acad. Sci. USA 98, 9098–9103 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Plant, P. J. et al. Apical membrane targeting of Nedd4 is mediated by an association of its C2 domain with annexin XIIIb. J. Cell Biol. 149, 1473–1484 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Kirchhausen, T. Clathrin . Annu. Rev. Biochem. 69, 699–727 (2000).
  Article CAS PubMed Google Scholar
• Bonifacino, J. S. & Lippincott-Schwartz, J. Coat proteins: shaping membrane transport. Nature Rev. Mol. Cell Biol. 4, 409–414 (2003).
  Article CAS Google Scholar
• Murphy, R. F. Maturation models for endosome and lysosome biogenesis. Trends Cell Biol. 1, 77–82 (1991).
  Article CAS PubMed Google Scholar
• Griffiths, G. & Gruenberg, J. The arguments for pre-existing early and late endosomes. Trends Cell Biol. 1, 5–9 (1991).
  Article CAS PubMed Google Scholar
• Bishop, N. E. Dynamics of endosomal sorting. Int. Rev. Cytol. 232, 1–57 (2003).
  Article CAS PubMed Google Scholar
• Rothberg, K. G. et al. Caveolin, a protein component of caveolae membrane coats. Cell 68, 673–682 (1992).
  Article CAS PubMed Google Scholar
• Drab, M. et al. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293, 2449–2452 (2001).
  Article CAS PubMed Google Scholar
• Fra, A. M., Williamson, E., Simons, K. & Parton, R. G. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc. Natl Acad. Sci. USA 92, 8655–8659 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• Kurzchalia, T. V. & Parton, R. G. Membrane microdomains and caveolae. Curr. Opin. Cell Biol. 11, 424–431 (1999).
  Article CAS PubMed Google Scholar