Clathrin Adaptor Proteins in Cargo Endocytosis
Abstract
Eukaryotic cells continuously remodel the protein and lipid composition of the plasma membrane in response to the extracellular milieu. Membrane retrieval typically involves inward budding of small bilayer-encapsulated vesicles that shuttle protein and lipid from the surface to internal endosomal elements. Clathrin-mediated endocytosis is a dominant pathway for internalization in many cell types, and a range of dedicated signals are used to ensure selective sorting in this pathway. Evidence suggests that the clathrin coat utilizes a diverse collection of clathrin-associated sorting proteins (CLASPs) to ensure the efficient and noncompetitive concentration of a wide variety of sorting signals within transport vesicles forming at the cell surface.
Keywords
Coated Vesicle Sorting Signal Clathrin Coat Sensory Organ Precursor Autosomal Recessive HypercholesterolemiaPreview
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References
- 1.Le Roy C, Wrana JL. Clathrin-and nonclathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 2005; 6:112–126.PubMedCrossRefGoogle Scholar
- 2.Cadavid AL, Ginzel A, Fischer JA. The function of the Drosophila fat facets deubiquitinating enzyme in limiting photoreceptor cell number is intimately associated with endocytosis. Development 2000; 127:1727–1736.PubMedGoogle Scholar
- 3.Berdnik D, Torok T, Gonzalez-Gaitan M et al. The endocytic protein α-Adaptin is required for Numb-mediated asymmetric cell division in Drosophila. Dev Cell 2002; 3:221–231.PubMedCrossRefGoogle Scholar
- 4.Resh MD. Membrane targeting of lipid modified signal transduction proteins. Subcell Biochem 2004; 37:217–232.PubMedGoogle Scholar
- 5.Roper K, Corbeil D, Huttner WB. Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat Cell Biol 2000; 2:582–592.PubMedCrossRefGoogle Scholar
- 6.Brone B, Eggermont J. PDZ proteins retain and regulate membrane transporters in polarized epithelial cell membranes. Am J Physiol Cell Physiol 2005; 288:C20–C29.PubMedGoogle Scholar
- 7.Bonifacino JS, Traub LM. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 2003; 72:395–447.PubMedCrossRefGoogle Scholar
- 8.Sanan DA, Van der Westhuyzen DR, Gevers W et al. The surface distribution of low density lipoprotein receptors on cultured fibroblasts and endothelial cells. Ultrastructural evidence for dispersed receptors. Histochemistry 1987; 86:517–523.PubMedCrossRefGoogle Scholar
- 9.Lobel P, Fujimoto K, Ye RD et al. Mutations in the cytoplasmic domain of the 275 kd mannose 6-phosphate receptor differentially alter lysosomal enzyme sorting and endocytosis. Cell 1989; 57:787–796.PubMedCrossRefGoogle Scholar
- 10.Nabi IR, Le PU. Caveolae/raft-dependent endocytosis. J Cell Biol 2003; 161:673–677.PubMedCrossRefGoogle Scholar
- 11.Brodsky FM, Chen CY, Knuehl C et al. Biological basket weaving: Formation and function of clathrin-coated vesicles. Annu Rev Cell Dev Biol 2001; 17:517–568.PubMedCrossRefGoogle Scholar
- 12.Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature 2003; 422:37–44.PubMedCrossRefGoogle Scholar
- 13.Damm EM, Pelkmans L, Kartenbeck J et al. Clathrin-and caveolin-1-independent endocytosis: Entry of simian virus 40 into cells devoid of caveolae. J Cell Biol 2005; 168:477–488.PubMedCrossRefGoogle Scholar
- 14.Kirkham M, Fujita A, Chadda R et al. Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J Cell Biol 2005; 168:465–476.PubMedCrossRefGoogle Scholar
- 15.Roth TF, Porter KR. Yolk protein uptake in the oocyte of the mosquito Aedes aegypti. L J Cell Biol 1964; 20:313–332.CrossRefGoogle Scholar
- 16.Fotin A, Cheng Y, Sliz P et al. Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 2004; 432:573–579.PubMedCrossRefGoogle Scholar
- 17.ter Haar E, Musacchio A, Harrison SC et al. Atomic structure of clathrin: A β propeller terminal domain joins an α zigzag linker. Cell 1998; 95:563–573.PubMedCrossRefGoogle Scholar
- 18.Blondeau F, Ritter B, Allaire PD et al. Tandem MS analysis of brain clathrin-coated vesicles reveals their critical involvement in synaptic vesicle recycling. Proc Natl Acad Sci USA 2004; 101:3833–3838.PubMedCrossRefGoogle Scholar
- 19.Owen DJ, Collins BM, Evans PR. Adaptors for clathrin coats: Structure and function. Annu Rev Cell Dev Biol 2004; 20:153–191.PubMedCrossRefGoogle Scholar
- 20.Heuser JE, Keen J. Deep-etch visualization of proteins involved in clathrin assembly. J Cell Biol 1988; 107:877–886.PubMedCrossRefGoogle Scholar
- 21.Collins BM, McCoy AJ, Kent HM et al. Molecular architecture and functional model of the endocytic AP2 complex. Cell 2002; 109:523–535.PubMedCrossRefGoogle Scholar
- 22.Owen DJ, Vallis Y, Noble ME et al. A structural explanation for the binding of multiple ligands by the α-adaptin appendage domain. Cell 1999; 97:805–815.PubMedCrossRefGoogle Scholar
- 23.Traub LM, Downs MA, Westrich JL et al. Crystal structure of the α appendage of AP-2 reveals a recruitment platform for clathrin-coat assembly. Proc Natl Acad Sci USA 1999; 96:8907–8912.PubMedCrossRefGoogle Scholar
- 24.Owen DJ, Vallis Y, Pearse BM et al. The structure and function of the P2-adaptin appendage domain. EMBO J 2000; 19:4216–4227.PubMedCrossRefGoogle Scholar
- 25.Galluser A, Kirchhausen T. The β1 and the β2 subunits of the AP complexes are the clathrin coat assembly components. EMBO J 1993; 12:5237–5244.Google Scholar
- 26.ter Haar E, Harrison SC, Kirchhausen T. Peptide-in-groove interactions link target proteins to the beta-propeller of clathrin. Proc Natl Acad Sci USA 2000; 97:1096–1100.PubMedCrossRefGoogle Scholar
- 27.Gaidarov I, Keen JH. Phosphoinositide-AP-2 interactions required for targeting to plasma membrane clathrin-coated pits. J Cell Biol 1999; 146:755–764.PubMedCrossRefGoogle Scholar
- 28.Padron D, Wang YJ, Yamamoto M et al. Phosphatidylinositol phosphate 5-kinase Iβ recruits AP-2 to the plasma membrane and regulates rates of constitutive endocytosis. J Cell Biol 2003; 162:693–701.PubMedCrossRefGoogle Scholar
- 29.Lundmark R, Carlsson SR. Regulated membrane recruitment of dynamin-2 mediated by sorting nexin 9. J Biol Chem 2004.Google Scholar
- 30.Praefcke GJ, McMahon HT. The dynamin superfamily: Universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 2004; 5:133–147.PubMedCrossRefGoogle Scholar
- 31.Soulet F, Yarar D, Leonard M et al. SNX9 regulates dynamin assembly and is required for efficient clathrin-mediated endocytosis. Mol Biol Cell 2005; 16, (in press).Google Scholar
- 32.Olusanya O, Andrews PD, Swedlow JR et al. Phosphorylation of threonine 156 of the μ2 subunit of the AP2 complex is essential for endocytosis in vitro and in vivo. Curr Biol 2001; 11:896–900.PubMedCrossRefGoogle Scholar
- 33.Ricotta D, Conner SD, Schmid SL et al. Phosphorylation of the AP2 μ subunit by AAK1 mediates high affinity binding to membrane protein sorting signals. J Cell Biol 2002; 156:791–795.PubMedCrossRefGoogle Scholar
- 34.Rohde G, Wenzel D, Haucke V. A phosphatidylinositol (4,5)-bisphosphate binding site within μ2-adaptin regulates clathrin-mediated endocytosis. J Cell Biol 2002; 158:209–214.PubMedCrossRefGoogle Scholar
- 35.Jackson AP, Flett A, Smythe C et al. Clathrin promotes incorporation of cargo into coated pits by activation of the AP2 adaptor μ2 kinase. J Cell Biol 2003; 163:231–236.PubMedCrossRefGoogle Scholar
- 36.Conner SD, Schroter T, Schmid SL. AAK1 mediated μ2 phosphorylation is stimulated by assembled clathrin. Traffic 2003; 4:885–890.PubMedCrossRefGoogle Scholar
- 37.Nesterov A, Carter RE, Sorkina T et al. 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 1999; 18:2489–2499.PubMedCrossRefGoogle Scholar
- 38.Ehrlich M, Boll W, Van Oijen A et al. Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 2004; 118:591–605.PubMedCrossRefGoogle Scholar
- 39.Gonzalez-Gaitan M, Jackie H. Role of Drosophila α-adaptin in presynaptic vesicle recycling. Cell 1997; 88:767–776.PubMedCrossRefGoogle Scholar
- 40.Shim J, Lee J. Molecular genetic analysis of apm-2 and aps-2, genes encoding the medium and small chains of the AP-2 clathrin-associated protein complex in the nematode Caenorhabditis elegans. Mol Cells 2000; 10:309–316.PubMedGoogle Scholar
- 41.Huang KM, D’Hondt K, Riezman H et al. Clathrin functions in the absence of heterotetrameric adaptors and AP180-related proteins in yeast. EMBO J 1999; 18:3897–3908.PubMedCrossRefGoogle Scholar
- 42.Yeung BG, Phan HL, Payne GS. Adaptor complex-independent clathrin function in yeast. Mol Biol Cell 1999; 10:3643–3659.PubMedGoogle Scholar
- 43.Hinrichsen L, Harborth J, Andrees L et al. Effect of clathrin heavy chain-and α-adaptin specific small interfering RNAs on endocytic accessory proteins and receptor trafficking in HeLa cells. J Biol Chem 2003; 278:45160–45170.PubMedCrossRefGoogle Scholar
- 44.Motley A, Bright NA, Seaman MN et al. Clathrin-mediated endocytosis in AP-2-depleted cells. J Cell Biol 2003; 162:909–918.PubMedCrossRefGoogle Scholar
- 45.Huang F, Khvorova A, Marshall W et al. Analysis of clathrin-mediated endocytosis of epidermal growth factor receptor by RNA interference. J Biol Chem 2004; 279:16657–16661.PubMedCrossRefGoogle Scholar
- 46.Robinson MS. Adaptable adaptors for coated vesicles. Trends Cell Biol 2004; 14:167–174.PubMedCrossRefGoogle Scholar
- 47.Janvier K, Kato Y, Boehm M et al. Recognition of dileucine-based sorting signals from HIV-1 Nef and LIMP-II by the AP-1 γ-σ1 and AP-3 δ-σ3 hemicomplexes. J Cell Biol 2003; 163:1281–1290.PubMedCrossRefGoogle Scholar
- 48.Marks MS, LW, Ohno H, Bonifacino JS. Protein targeting by tyrosine-and di-leucine-based signals: Evidence for distinct saturable components. J Cell Biol 1996; 135:341–354.PubMedCrossRefGoogle Scholar
- 49.Carpentier JL, Gorden P, Anderson RG et al. Colocalization of125 I-epidermal growth factor and ferritin-low density lipoprotein in coated pits: A quantitative electron microscopic study in normal and mutant human fibroblasts. J Cell Biol 1982; 95:73–77.PubMedCrossRefGoogle Scholar
- 50.Morris SM, Cooper JA. Disabled-2 colocalizes with the LDLR in clathrin-coated pits and interacts with AP-2. Traffic 2001; 2:111–123.PubMedCrossRefGoogle Scholar
- 51.Mishra SK, Keyel PA, Hawryluk MJ et al. Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor. EMBO J 2002; 21:4915–4926.PubMedCrossRefGoogle Scholar
- 52.Stang E, Blystad FD, Kazazic M et al. Cbl-dependent ubiquitination is required for progression of EGF receptors into clathrin-coated pits. Mol Biol Cell 2004; 15:3591–3604.PubMedCrossRefGoogle Scholar
- 53.Sorkin A, McKinsey T, Shih W et al. Stoichiometric interaction of the epidermal growth factor receptor with the clathrin-associated protein complex AP-2. J Biol Chem 1995; 270:619–625.PubMedCrossRefGoogle Scholar
- 54.Nesterov A, Wiley HS, Gill GN. Ligand-induced endocytosis of epidermal growth factor receptors that are defective in binding adaptor proteins. Proc Natl Acad Sci USA 1995; 92:8719–8723.PubMedCrossRefGoogle Scholar
- 55.Warren RA, Green FA, Enns CA. Saturation of the endocytic pathway for the transferrin receptor does not affect the endocytosis of the epidermal growth factor receptor. J Biol Chem 1997; 272:2116–2121.PubMedCrossRefGoogle Scholar
- 56.Warren RA, Green FA, Stenberg PE et al. Distinct saturable pathways for the endocytosis of different tyrosine motifs. J Biol Chem 1998; 273:17056–17063.PubMedCrossRefGoogle Scholar
- 57.Maxfield FR, Schlessinger J, Shechter Y et al. Collection of insulin, EGF and (X2-macroglobulin in the same patches on the surface of cultured fibroblasts and common internalization. Cell 1978; 14:805–810.PubMedCrossRefGoogle Scholar
- 58.Ajioka RS, Kaplan J. Characterization of endocytic compartments using the horseradish peroxidase-diaminobenzidine density shift technique. J Cell Biol 1987; 104:77–85.PubMedCrossRefGoogle Scholar
- 59.Sorkin A, Von Zastrow M. Signal transduction and endocytosis: Close encounters of many kinds. Nat Rev Mol Cell Biol 2002; 3:600–614.PubMedCrossRefGoogle Scholar
- 60.Marchese A, Chen C, Kim YM et al. The ins and outs of G protein-coupled receptor trafficking. Trends Biochem Sci 2003; 28:369–376.PubMedCrossRefGoogle Scholar
- 61.Lefkowitz RJ, Whalen EJ. β-arrestins: Traffic cops of cell signaling. Curr Opin Cell Biol 2004; 16:162–168.PubMedCrossRefGoogle Scholar
- 62.Gaidarov I, Krupnick JG, Falck JR et al. Arrestin function in G protein-coupled receptor endocytosis requires phosphoinositide binding. EMBO J 1999; 18:871–881.PubMedCrossRefGoogle Scholar
- 63.Laporte SA, Oakley RH, Holt JA et al. The interaction of β-arrestin with the AP-2 adaptor is required for the clustering of p2-adrenergic receptor into clathrin-coated pits. J Biol Chem 2000; 275:23120–23126.PubMedCrossRefGoogle Scholar
- 64.Milano SK, Pace HC, Kim YM et al. Scaffolding functions of arrestin-2 revealed by crystal structure and mutagenesis. Biochemistry 2002; 41:3321–3328.PubMedCrossRefGoogle Scholar
- 65.Goodman Jr OB, Krupnick JG, Santini F et al. β-arrestin acts as a clathrin adaptor in endocytosis of the β2-adrenergic receptor. Nature 1996; 383:447–450.PubMedCrossRefGoogle Scholar
- 66.Krupnick JG, Goodman Jr OB, Keen Jr JH. Arrestin/clathrin interaction. Localization of the clathrin binding domain of nonvisual arrestins to the carboxy terminus. J Biol Chem 1997; 272:15011–15016.PubMedCrossRefGoogle Scholar
- 67.Santini F, Penn RB, Gagnon AW et al. Selective recruitment of arrestin-3 to clathrin coated pits upon stimulation of G protein-coupled receptors. J Cell Sci 2000; 113 (Pt 13):2463–2470.PubMedGoogle Scholar
- 68.Chen W, Ren XR, Nelson CD et al. Activity-dependent internalization of smoothened mediated by β-arrestin 2 and GRK2. Science 2004; 306:2257–2260.PubMedCrossRefGoogle Scholar
- 69.Chen W, ten Berge D, Brown J et al. Dishevelled 2 recruits β-arrestin 2 to mediate Wnt5A-stimulated endocytosis of Frizzled 4. Science 2003; 301:1391–1394.PubMedCrossRefGoogle Scholar
- 70.Chen W, Kirkbride KC, How T et al. β-arrestin 2 mediates endocytosis of type III TGF-β receptor and down-regulation of its signaling. Science 2003; 301:1394–1397.PubMedCrossRefGoogle Scholar
- 71.Wu JH, Peppel K, Nelson CD et al. The adaptor protein β-arrestin2 enhances endocytosis of the low-density lipoprotein receptor. J Biol Chem 2003.Google Scholar
- 72.Slepnev VI, De Camilli P. Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nat Rev Neurosci 2000; 1:161–172.PubMedCrossRefGoogle Scholar
- 73.McMahon HT, Mills IG. COP and clathrin-coated vesicle budding: Different pathways, common approaches. Curr Opin Cell Biol 2004; 16:379–391.PubMedCrossRefGoogle Scholar
- 74.Sorkin A. Cargo recognition during clathrin-mediated endocytosis: A team effort. Curr Opin Cell Biol 2004; 16:392–399.PubMedCrossRefGoogle Scholar
- 75.Blaikie P, Immanuel D, Wu J et al. A region in Shc distinct from the SH2 domain can bind tyrosine-phosphorylated growth factor receptors. J Biol Chem 1994; 269:32031–32034.PubMedGoogle Scholar
- 76.Yan KS, Kuti M, Zhou MM. PTB or not PTB — that is the question. FEBS Lett 2002; 513:67–70.PubMedCrossRefGoogle Scholar
- 77.Davis CG, Lehrman MA, Russell DW et al. The J.D. mutation in familial hypercholesterolemia: Amino acid substitution in cytoplasmic domain impedes internalization of LDL receptors. Cell 1986; 45:15–24.PubMedCrossRefGoogle Scholar
- 78.Garcia CK, Wilund K, Arca M et al. Autosomal recessive hypercholesterolemia caused by mutations in a putative LDL receptor adaptor protein. Science 2001; 292:1394–1398.PubMedCrossRefGoogle Scholar
- 79.Morris SM, Tallquist MD, Rock CO et al. Dual roles for the Dab2 adaptor protein in embryonic development and kidney transport. EMBO J 2002; 21:1555–1564.PubMedCrossRefGoogle Scholar
- 80.Jones C, Hammer RE, Li WP et al. Normal sorting, but defective endocytosis of the LDL receptor in mice with autosomal recessive hypercholesterolemia. J Biol Chem 2003; 278:29024–29030.PubMedCrossRefGoogle Scholar
- 81.Tietge UJ, Genschel J, Schmidt HH. A Q136Stop mutation in the ARH gene causing autosomal recessive hypercholesterolaemia with severely delayed LDL catabolism. J Intern Med 2003; 253:582–583.PubMedCrossRefGoogle Scholar
- 82.Eden ER, Patel DD, Sun X et al. Restoration of LDL-receptor function in cells from patients with autosomal recessive hypercholesterolemia by retroviral expression of ARH1. J Clin Invest 2002; 110:1695–1702.PubMedGoogle Scholar
- 83.Al-Kateb H, Bahring S, Hoffmann K et al. Mutation in the ARH gene and a chromosome 13q locus influence cholesterol levels in a new form of digenic-recessive familial hypercholesterolemia. Circ Res 2002; 90:951–958.PubMedCrossRefGoogle Scholar
- 84.Canizales-Quinteros S, Aguilar-Salinas CA, Huertas-Vazquez A et al. A novel ARH splice site mutation in a Mexican kindred with autosomal recessive hypercholesterolemia. Hum Genet 2005; 116:114–120.PubMedCrossRefGoogle Scholar
- 85.Harada-Shiba M, Takagi A, Miyamoto Y et al. Clinical features and genetic analysis of autosomal recessive hypercholesterolemia. J Clin Endocrinol Metab 2003; 88:2541–2547.PubMedCrossRefGoogle Scholar
- 86.Barbagallo CM, Emmanuele G, Cefalu AB et al. Autosomal recessive hypercholesterolemia in a Sicilian kindred harboring the 432insA mutation of the ARH gene. Atherosclerosis 2003; 166:395–400.PubMedCrossRefGoogle Scholar
- 87.Osono Y, Woollett LA, Herz J et al. Role of the low density lipoprotein receptor in the flux of cholesterol through the plasma and across the tissues of the mouse. J Clin Invest 1995; 95:1124–1132.PubMedCrossRefGoogle Scholar
- 88.Nagai J, Christensen EI, Morris SM et al. Mutually-dependent localization of megalin and Dab2 in the renal proximal tubule. Am J Physiol Renal Physiol 2005: (in press).Google Scholar
- 89.Nykjaer A, Dragun D, Walther D et al. An endocytic pathway essential for renal uptake and activation of the steroid 25-(OH) vitamin D3. Cell 1999; 96:507–515.PubMedCrossRefGoogle Scholar
- 90.Mishra SK, Watkins SC, Traub LM. The autosomal recessive hypercholesterolemia (ARH) protein interfaces directly with the clathrin-coat machinery. Proc Natl Acad Sci USA 2002; 99:16099–16104.PubMedCrossRefGoogle Scholar
- 91.Stolt PC, Jeon H, Song HK et al. Origins of peptide selectivity and phosphoinositide binding revealed by structures of Disabled-1 PTB domain complexes. Structure (Camb) 2003; 11:569–579.PubMedCrossRefGoogle Scholar
- 92.Yun M, Keshvara L, Park CG et al. Crystal structures of the dab homology domains of mouse disabled 1 and 2. J Biol Chem 2003; 278:36572–36581.PubMedCrossRefGoogle Scholar
- 93.Morris AJ, Frohman MA, Engebrecht J. Measurement of phospholipase D activity. Anal Biochem 1997; 252:1–9.PubMedCrossRefGoogle Scholar
- 94.He G, Gupta S, Yi M et al. ARH is a modular adaptor protein that interacts with the LDL receptor, clathrin and AP-2. J Biol Chem 2002; 277:44044–44049.PubMedCrossRefGoogle Scholar
- 95.Brett TJ, Traub LM, Fremont DH. Accessory protein recruitment motifs in clathrin-mediated endocytosis. Structure (Camb) 2002; 10:797–809.PubMedCrossRefGoogle Scholar
- 96.Miele AE, Watson PJ, Evans PR et al. Two distinct interaction motifs in amphiphysin bind two independent sites on the clathrin terminal domain β-propeller. Nat Struct Mol Biol 2004; 11:242–248.PubMedCrossRefGoogle Scholar
- 97.Praefcke GJ, Ford MG, Schmid EM et al. Evolving nature of the AP2 α-appendage hub during clathrin-coated vesicle endocytosis. EMBO J 2004; 23:4371–4383.PubMedCrossRefGoogle Scholar
- 98.Owen DJ. Linking endocytic cargo to clathrin: Structural and functional insights into coated vesicle formation. Biochem Soc Trans 2004; 32:1–14.PubMedCrossRefGoogle Scholar
- 99.Shen Q, Temple S. Creating asymmetric cell divisions by skewing endocytosis. Sci STKE 2002; 2002:PE52.PubMedCrossRefGoogle Scholar
- 100.Rhyu MS, Jan LY, Jan YN. Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell 1994; 76:477–491.PubMedCrossRefGoogle Scholar
- 101.O’Connor-Giles KM, Skeath JB. Numb inhibits membrane localization of Sanpodo, a four-pass transmembrane protein, to promote asymmetric divisions in Drosophila. Dev Cell 2003; 5:231–243.PubMedCrossRefGoogle Scholar
- 102.Wendland B. Epsins: Adaptors in endocytosis? Nat Rev Mol Cell Biol 2002; 3:971–977.PubMedCrossRefGoogle Scholar
- 103.Hicke L, Dunn R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cel Dev Biol 2003; 19:141–172.CrossRefGoogle Scholar
- 104.Ford MG, Mills IG, Peter BJ et al. Curvature of clathrin-coated pits driven by epsin. Nature 2002; 419:361–366.PubMedCrossRefGoogle Scholar
- 105.Hofmann K, Falquet L. A ubiquitin-interacting motif conserved in components of the proteasomal and lysosomal protein degradation systems. Trends Biochem Sci 2001; 26:347–350.PubMedCrossRefGoogle Scholar
- 106.Chen H, Fre S, Slepnev VI et al. Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis. Nature 1998; 394:793–797.PubMedCrossRefGoogle Scholar
- 107.Drake MT, Downs MA, Traub LM. Epsin binds to clathrin by associating directly with the clathrin-terminal domain: Evidence for cooperative binding through two discrete sites. J Biol Chem 2000; 275:6479–6489.PubMedCrossRefGoogle Scholar
- 108.Rosenthal JA, Chen H, Slepnev VI et al. The epsins define a family of proteins that interact with components of the clathrin coat and contain a new protein module. J Biol Chem 1999; 274:33959–33965.PubMedCrossRefGoogle Scholar
- 109.Tian X, Hansen D, Schedl T et al. Epsin potentiates Notch pathway activity in Drosophila and C. elegans. Development 2004; 131:5807–5815.PubMedCrossRefGoogle Scholar
- 110.Overstreet E, Fitch E, Fischer JA. Fat facets and Liquid facets promote Delta endocytosis and Delta signaling in the signaling cells. Development 2004; 131:5355–5366.PubMedCrossRefGoogle Scholar
- 111.Lai EC, Roegiers F, Qin X et al. The ubiquitin ligase Drosophila Mind bomb promotes Notch signaling by regulating the localization and activity of Serrate and Delta. Development 2005; 132:2319–2332.PubMedCrossRefGoogle Scholar
- 112.Wang W, Struhl G. Drosophila Epsin mediates a select endocytic pathway that DSL ligands must enter to activate Notch. Development 2004; 131:5367–5380.PubMedCrossRefGoogle Scholar
- 113.Le Borgne R, Bardin A, Schweisguth F. The roles of receptor and ligand endocytosis in regulating Notch signaling. Development 2005; 132:1751–1762.PubMedCrossRefGoogle Scholar
- 114.Chen X, Zhang B, Fischer JA. A specific protein substrate for a deubiquitinating enzyme: Liquid facets is the substrate of Fat facets. Genes Dev 2002; 16:289–294.PubMedCrossRefGoogle Scholar
- 115.Metzler M, Li B, Gan L et al. Disruption of the endocytic protein HIP1 results in neurological deficits and decreased AMPA receptor trafficking. EMBO J 2003; 22:3254–3266.PubMedCrossRefGoogle Scholar
- 116.Nonet ML, Holgado AM, Brewer F et al. UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles. Mol Biol Cell 1999; 10:2343–2360.PubMedGoogle Scholar
- 117.Mossessova E, Bickford LC, Goldberg J. SNARE selectivity of the COPII coat. Cell 2003; 114:483–495.PubMedCrossRefGoogle Scholar
- 118.Traub LM. Common principles in clathrin-mediated sorting at the Golgi and the plasma membrane. Biochim Biophys Acta 2005; in press.Google Scholar
- 119.Merrifield CJ. Seeing is believing: Imaging actin dynamics at single sites of endocytosis. Trends Cell Biol 2004; 14:352–358.PubMedCrossRefGoogle Scholar
- 120.Blagoev B, Ong SE, Kratchmarova I et al. Temporal analysis of phosphotyrosine-dependent signaling networks by quantitative proteomics. Nat Biotechnol 2004; 22:1139–1145.PubMedCrossRefGoogle Scholar
- 121.Barabasi AL, Oltvai ZN. Network biology: Understanding the cell’s functional organization. Nat Rev Genet 2004; 5:101–113.PubMedCrossRefGoogle Scholar