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Vesicle Trafficking in Cancer pp 1–31Cite as

Clathrin-Mediated Endocytosis

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Abstract

Clathrin-mediated endocytosis is the main portal of entry into the cell for many soluble and membrane molecules. Clathrin-coated vesicles are formed from the plasma membrane in a sequence of coordinated protein-lipid and protein-protein interactions, starting with adaptor-mediated recruitment of clathrin to the membrane, proceeding to clathrin polymerization and assembly into deeply curved coated buds, and ending with the dynamin-dependent scission of a coated vesicle. Clathrin coats trap and concentrate endocytic cargo by using a multitude of adaptor proteins that recognize specific sequence motifs in the cytosolic domains of receptors and other transmembrane cargo molecules. Endocytic cargo that is concentrated in this manner, such as signaling receptors, may regulate the stability, size, and dynamics of individual clathrin coats and thereby influence endocytosis.

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References

  1. Howes MT, Mayor S, Parton RG (2010) Molecules, mechanisms, and cellular roles of clathrin-­independent endocytosis. Curr Opin Cell Biol 22(4):519–527

    Article  PubMed  CAS  Google Scholar 

  2. McMahon HT, Boucrot E (2011) Molecular mechanism and physiological functions of clathrin-­mediated endocytosis. Nat Rev Mol Cell Biol 12(8):517–533

    Article  PubMed  CAS  Google Scholar 

  3. Lund KA, Opresko LK, Strarbuck C, Walsh BJ, Wiley HS (1990) Quantitative analysis of the endocytic system involved in hormone-induced receptor internalization. J Biol Chem 265:15713–15723

    PubMed  CAS  Google Scholar 

  4. Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Annu Rev Biochem 78:857–902. doi:10.1146/annurev.biochem.78.081307.110540

    Article  PubMed  CAS  Google Scholar 

  5. Young A (2007) Structural insights into the clathrin coat. Semin Cell Dev Biol 18(4):448–458

    Article  PubMed  CAS  Google Scholar 

  6. Fotin A, Cheng Y, Sliz P, Grigorieff N, Harrison SC, Kirchhausen T, Walz T (2004) Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432(7017):573–579

    Article  PubMed  CAS  Google Scholar 

  7. Kirchhausen T, Harrison SC (1981) Protein organization in clathrin trimers. Cell 23(3):755–761

    Article  PubMed  CAS  Google Scholar 

  8. Undewickell E, Branton D (1981) Assembly units of clathrin coats. Nature 289:420–422

    Article  Google Scholar 

  9. Ybe JA, Brodsky FM, Hofmann K, Lin K, Liu SH, Chen L, Earnest TN, Fletterick RJ, Hwang PK (1999) Clathrin self-assembly is mediated by a tandemly repeated superhelix. Nature 399(6734):371–375

    Article  PubMed  CAS  Google Scholar 

  10. Kirchhausen T, Harrison SC (1984) Structural domains of clathrin heavy chains. J Cell Biol 718 99(5):1725–1734

    Article  PubMed  CAS  Google Scholar 

  11. Fotin A, Cheng Y, Grigorieff N, Walz T, Harrison SC, Kirchhausen T (2004) Structure of an auxilin-bound clathrin coat and its implications for the mechanism of uncoating. Nature 432(7017):649–653

    Article  PubMed  CAS  Google Scholar 

  12. ter Haar E, Musacchio A, Harrison SC, Kirchhausen T (1998) Atomic structure of clathrin: a β propeller terminal domain joins an α zigzag linker. Cell 95:563–575

    Article  PubMed  Google Scholar 

  13. Miele AE, Watson PJ, Evans PR, Traub LM, Owen DJ (2004) Two distinct interaction motifs in amphiphysin bind two independent sites on the clathrin terminal domain beta-propeller. Nat Struct Mol Biol 11(3):242–248

    Article  PubMed  CAS  Google Scholar 

  14. Chen CY, Reese ML, Hwang PK, Ota N, Agard D, Brodsky FM (2002) Clathrin light and heavy chain interface: alpha-helix binding superhelix loops via critical tryptophans. EMBO J 21(22):6072–6082

    Article  PubMed  CAS  Google Scholar 

  15. Nathke IS, Heuser J, Lupas A, Stock J, Turck CW, Brodsky FM (1992) Folding and trimerization of clathrin subunits at the triskelion hub. Cell 68(5):899–910

    Article  PubMed  CAS  Google Scholar 

  16. Ungewickell E (1983) Biochemical and immunological studies on clathrin light chains and their binding sites on clathrin triskelions. EMBO J 2(8):1401–1408

    PubMed  CAS  Google Scholar 

  17. Huang F, Khvorova A, Marshall W, Sorkin A (2004) Analysis of clathrin-mediated endocytosis of epidermal growth factor receptor by RNA interference. J Biol Chem 279(16):16657–16661

    Article  PubMed  CAS  Google Scholar 

  18. Pishvaee B, Munn A, Payne GS (1997) A novel structural model for regulation of clathrin function. EMBO J 16(9):2227–2239

    Article  PubMed  CAS  Google Scholar 

  19. Boulant S, Kural C, Zeeh J-C, Ubelmann F, Kirchhausen T (2011) Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat Cell Biol 13(9):1124–1131

    Article  PubMed  CAS  Google Scholar 

  20. Wilbur JD, Chen CY, Manalo V, Hwang PK, Fletterick RJ, Brodsky FM (2008) Actin binding by Hip1 (huntingtin-interacting protein 1) and Hip1R (hip1-related protein) is regulated by clathrin light chain. J Biol Chem 283(47):32870–32879

    Article  PubMed  CAS  Google Scholar 

  21. Chen H, De Camilli P (2005) The association of epsin with ubiquitinated cargo along the endocytic pathway is negatively regulated by its interaction with clathrin. Proc Natl Acad Sci U S A 102(8):2766–2771

    Article  PubMed  CAS  Google Scholar 

  22. Engqvist-Goldstein AE, Warren RA, Kessels MM, Keen JH, Heuser J, Drubin DG (2001) The actin-binding protein Hip1R associates with clathrin during early stages of endocytosis and promotes clathrin assembly in vitro. J Cell Biol 154(6):1209–1223

    Article  PubMed  CAS  Google Scholar 

  23. Ferreira F, Foley M, Cooke A, Cunningham M, Smith G, Woolley R, Henderson G, Kelly E, Mundell S, Smythe E (2012) Endocytosis of g protein-coupled receptors is regulated by clathrin light chain phosphorylation. Curr Biol 22(15):1361–1370

    Article  PubMed  CAS  Google Scholar 

  24. Keen JH, Willingham MC, Pastan I (1981) Clathrin and coated vesicle proteins immunological characterization. J Biol Chem 256(5):2538–2544

    PubMed  CAS  Google Scholar 

  25. Pearse BM, Robinson MS (1984) Purification and properties of 100-kd proteins from coated vesicles and their reconstitution with clathrin. EMBO J 3(9):1951–1957

    PubMed  CAS  Google Scholar 

  26. Collins BM, McCoy AJ, Kent HM, Evans PR, Owen DJ (2002) Molecular architecture and functional model of the endocytic AP2 complex. Cell 109(4):523–535

    Article  PubMed  CAS  Google Scholar 

  27. Heuser JE, Keen J (1988) Deep-etch visualization of proteins involved in clathrin assembly. J Cell Biol 107(3):877–886

    Article  PubMed  CAS  Google Scholar 

  28. Zaremba S, Keen JH (1983) Assembly polypeptides from coated vesicles mediate reassembly of unique clathrin coats. J Cell Biol 97(5 pt 1):1339–1347

    Article  PubMed  CAS  Google Scholar 

  29. Owen DJ, Collins BM, Evans PR (2004) Adaptors for clathrin coats: structure and function. Annu Rev Cell Dev Biol 20:153–191

    Article  PubMed  CAS  Google Scholar 

  30. Gaidarov I, Chen Q, Falck JR, Reddy KK, Keen JH (1996) A functional phosphatidylinositol 3,4,5-trisphosphate/phosphoinositide binding domain in the clathrin adaptor AP-2 alpha subunit. Implications for the endocytic pathway. J Biol Chem 271(34):20922–20929

    Article  PubMed  CAS  Google Scholar 

  31. Jackson LP, Kelly BT, McCoy AJ, Gaffry T, James LC, Collins BM, Höning S, Evans PR, Owen DJ (2010) A large-scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex. Cell 141(7):1220–1229

    Article  PubMed  CAS  Google Scholar 

  32. Kelly BT, McCoy AJ, Spate K, Miller SE, Evans PR, Honing S, Owen DJ (2008) A structural explanation for the binding of endocytic dileucine motifs by the AP2 complex. Nature 456(7224):976–979

    Article  PubMed  CAS  Google Scholar 

  33. Rohde G, Wenzel D, Haucke V (2002) A phosphatidylinositol (4,5)-bisphosphate binding site within mu2-adaptin regulates clathrin-mediated endocytosis. J Cell Biol 158(2):209–214

    Article  PubMed  CAS  Google Scholar 

  34. Ahle S, Ungewickell E (1986) Purification and properties of a new clathrin assembly protein. EMBO J 5(12):3143–3149

    PubMed  CAS  Google Scholar 

  35. Chen H, Fre S, Slepnev VI, Capua MR, Takei K, Butler MH, Di Fiore PP, De Camilli P (1998) Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis. Nature 394(6695):793–797

    Article  PubMed  CAS  Google Scholar 

  36. Ford MG, Pearse BM, Higgins MK, Vallis Y, Owen DJ, Gibson A, Hopkins CR, Evans PR, McMahon HT (2001) Simultaneous binding of Ptdins (4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291(5506):1051–1055

    Article  PubMed  CAS  Google Scholar 

  37. Tebar F, Bohlander S, Sorkin A (1999) Interactions of clathrin assembly lymphoid myeloid (CALM) protein with clathrin and its impact on endocytosis. Mol Biol Cell 10:2687–2702

    PubMed  CAS  Google Scholar 

  38. Dannhauser PN, Ungewickell EJ (2012) Reconstitution of clathrin-coated bud and vesicle formation with minimal components. Nat Cell Biol 14(6):634–639

    Article  PubMed  CAS  Google Scholar 

  39. Hinrichsen L, Meyerholz A, Groos S, Ungewickell EJ (2006) Bending a membrane: how clathrin affects budding. Proc Natl Acad Sci U S A 103(23):8715–8720

    Article  PubMed  CAS  Google Scholar 

  40. Cocucci E, Aguet F, Boulant S, Kirchhausen T (2012) The first five seconds in the life of a clathrin-coated pit. Cell 150(3):495–507

    Article  PubMed  CAS  Google Scholar 

  41. Henne WM, Boucrot E, Meinecke M, Evergren E, Vallis Y, Mittal R, McMahon HT (2010) FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 328(5983):1281–1284

    Article  PubMed  CAS  Google Scholar 

  42. Nunez D, Antonescu C, Mettlen M, Liu A, Schmid SL, Loerke D, Danuser G (2011) Hotspots organize clathrin-mediated endocytosis by efficient recruitment and retention of nucleating resources. Traffic 12(12):1868–1878

    Article  PubMed  CAS  Google Scholar 

  43. Umasankar PK, Sanker S, Thieman JR, Chakraborty S, Wendland B, Tsang M, Traub LM (2012) Distinct and separable activities of the endocytic clathrin-coat components fcho1/2 and AP-2 in developmental patterning. Nat Cell Biol 14(5):488–501

    Article  PubMed  CAS  Google Scholar 

  44. Mulkearns EE, Cooper JA (2012) FCH domain only-2 organizes clathrin-coated structures and interacts with disabled-2 for low-density lipoprotein receptor endocytosis. Mol Biol Cell 23(7):1330–1342

    Article  PubMed  CAS  Google Scholar 

  45. Teckchandani A, Mulkearns EE, Randolph TW, Toida N, Cooper JA (2012) The clathrin adaptor dab2 recruits EH domain scaffold proteins to regulate integrin beta1 endocytosis. Mol Biol Cell 23(15):2905–2916

    Article  PubMed  CAS  Google Scholar 

  46. Tebar F, Sorkina T, Sorkin A, Ericsson M, Kirchhausen T (1996) Eps15 is a component of clathrin-coated pits and vesicles and is located at the rim of coated pits. J Biol Chem 271(46):28727–28730

    Article  PubMed  CAS  Google Scholar 

  47. Traub LM (2009) Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat Rev Mol Cell Biol 10(9):583–596

    Article  PubMed  CAS  Google Scholar 

  48. Claing A, Laporte SA, Caron MG, Lefkowitz RJ (2002) Endocytosis of G protein-coupled receptors: roles of G protein-coupled receptor kinases and beta-arrestin proteins. Prog Neurobiol 66(2):61–79

    Article  PubMed  CAS  Google Scholar 

  49. Kim Y-M, Benovic JL (2002) Differential roles of arrestin-2 interaction with clathrin and adaptor protein 2 in G protein-coupled receptor trafficking. J Biol Chem 277(34):30760–30768

    Article  PubMed  CAS  Google Scholar 

  50. Ehrlich M, Boll W, Van Oijen A, Hariharan R, Chandran K, Nibert ML, Kirchhausen T (2004) Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118(5):591–605

    Article  PubMed  CAS  Google Scholar 

  51. Kazazic M, Bertelsen V, Pedersen KW, Vuong TT, Grandal MV, Rodland MS, Traub LM, Stang E, Madshus IH (2009) Epsin 1 is involved in recruitment of ubiquitinated EGF receptors into clathrin-coated pits. Traffic 10(2):235–245

    Article  PubMed  CAS  Google Scholar 

  52. Ford MG, Mills IG, Peter BJ, Vallis Y, Praefcke GJ, Evans PR, McMahon HT (2002) Curvature of clathrin-coated pits driven by epsin. Nature 419(6905):361–366

    Article  PubMed  CAS  Google Scholar 

  53. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, Evans PR, McMahon HT (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303(5657):495–499

    Article  PubMed  CAS  Google Scholar 

  54. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, Transidico P, Di Fiore PP, Polo S (2005) From the cover: clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci U S A 102(8):2760–2765

    Article  PubMed  CAS  Google Scholar 

  55. Ferguson SM, De Camilli P (2012) Dynamin, a membrane-remodelling gtpase. Nat Rev Mol Cell Biol 13(2):75–88

    PubMed  CAS  Google Scholar 

  56. Schmid SL, Frolov VA (2011) Dynamin: functional design of a membrane fission catalyst. Annu Rev Cell Dev Biol 27(3):1–27

    Google Scholar 

  57. Takei K, McPherson PS, Schmid SL, De Camilli P (1995) Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals [see comments]. Nature 374(6518):186–190

    Article  PubMed  CAS  Google Scholar 

  58. Bashkirov PV, Akimov SA, Evseev AI, Schmid SL, Zimmerberg J, Frolov VA (2008) GTPase cycle of dynamin is coupled to membrane squeeze and release, leading to spontaneous fission. Cell 135(7):1276–1286

    Article  PubMed  CAS  Google Scholar 

  59. Boucrot E, Pick A, Camdere G, Liska N, Evergren E, McMahon HT, Kozlov MM (2012) Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell 149(1):124–136

    Article  PubMed  CAS  Google Scholar 

  60. Shevchuk AI, Novak P, Taylor M, Diakonov IA, Ziyadeh-Isleem A, Bitoun M, Guicheney P et al (2012) An alternative mechanism of clathrin-coated pit closure revealed by ion conductance microscopy. J Cell Biol 197(4):499–508

    Article  PubMed  CAS  Google Scholar 

  61. Taylor MJ, Perrais D, Merrifield CJ (2011) A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol 9(3):e1000604

    Article  PubMed  CAS  Google Scholar 

  62. Taylor MJ, Lampe M, Merrifield CJ (2012) A feedback loop between dynamin and actin recruitment during clathrin-mediated endocytosis. PLoS Biol 10(4):e1001302

    Article  PubMed  CAS  Google Scholar 

  63. Schlossman DM, Schmid SL, Braell WA, Rothman JE (1984) An enzyme that removes clathrin coats: purification of an uncoating atpase. J Cell Biol 99(2):723–733

    Article  PubMed  CAS  Google Scholar 

  64. Ungewickell E, Ungewickell H, Holstein SE, Lindner R, Prasad K, Barouch W, Martin B, Greene LE, Eisenberg E (1995) Role of auxilin in uncoating clathrin-coated vesicles. Nature 378(6557):632–635

    Article  PubMed  CAS  Google Scholar 

  65. Scheele U, Kalthoff C, Ungewickell E (2001) Multiple interactions of auxilin 1 with clathrin and the AP-2 adaptor complex. J Biol Chem 276(39):36131–36138

    Article  PubMed  CAS  Google Scholar 

  66. Nakatsu F, Perera RM, Lucast L, Zoncu R, Domin J, Gertler FB, Toomre D, De Camilli P (2010) The inositol 5-phosphatase SHIP2 regulates endocytic clathrin-coated pit dynamics. J Cell Biol 190(3):307–315

    Article  PubMed  CAS  Google Scholar 

  67. Schuske KR, Richmond JE, Matthies DS, Davis WS, Runz S, Rube DA, van der Bliek AM, Jorgensen EM (2003) Endophilin is required for synaptic vesicle endocytosis by localizing synaptojanin. Neuron 40(4):749–762

    Article  PubMed  CAS  Google Scholar 

  68. McPherson PS, Garcia EP, Slepnev VI, David C, Zhang X, Grabs D, Sossin WS, Bauerfeind R, Nemoto Y, De Camilli P (1996) A presynaptic inositol-5-phosphatase. Nature 379(6563):353–357

    Article  PubMed  CAS  Google Scholar 

  69. Erdmann KS, Mao Y, McCrea HJ, Zoncu R, Lee S, Paradise S, Modregger J, Biemesderfer D, Toomre D, De Camilli P (2007) A role of the lowe syndrome protein OCRL in early steps of the endocytic pathway. Dev Cell 13(3):377–390

    Article  PubMed  CAS  Google Scholar 

  70. Sorkin A, von Zastrow M (2009) Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 10(9):609–622

    Article  PubMed  CAS  Google Scholar 

  71. Rao Y, Rückert C, Saenger W, Haucke V (2012) The early steps of endocytosis: from cargo selection to membrane deformation. Eur J Cell Biol 91(4):226–233

    Article  PubMed  CAS  Google Scholar 

  72. Ohno H, Stewart J, Fournier MC, Bosshart H, Rhee I, Miyatake S, Saito T, Gallusser A, Kirchhausen T, Bonifacino JS (1995) Interaction of tyrosine-based sorting signals with clathrin-­associated proteins. Science 269(5232):1872–1875

    Article  PubMed  CAS  Google Scholar 

  73. Owen DJ, Evans PR (1998) A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 282(5392):1327–1332

    Article  PubMed  CAS  Google Scholar 

  74. Kittler JT, Chen G, Kukhtina V, Vahedi-Faridi A, Zhenglin G, Tretter V, Smith KR et al (2008) Regulation of synaptic inhibition by phospho-dependent binding of the AP2 complex to a YECL motif in the GABAA receptor gamma2 subunit. Proc Natl Acad Sci U S A 105(9):3616–3621

    Article  PubMed  CAS  Google Scholar 

  75. Rollason R, Korolchuk V, Hamilton C, Schu P, Banting G (2007) Clathrin-mediated endocytosis of a lipid-raft-associated protein is mediated through a dual tyrosine motif. J Cell Sci 120(pt 21):3850–3858

    Article  PubMed  CAS  Google Scholar 

  76. Masuyama N, Kuronita T, Tanaka R, Muto T, Hirota Y, Takigawa A, Fujita H, Aso Y, Amano J, Tanaka Y (2009) HM1.24 is internalized from lipid rafts by clathrin-mediated endocytosis through interaction with alpha-adaptin. J Biol Chem 284(23):15927–15941

    Article  PubMed  CAS  Google Scholar 

  77. Höning S, Ricotta D, Krauss M, Späte K, Spolaore B, Motley A, Robinson M, Robinson C, Haucke V, Owen DJ (2005) Phosphatidylinositol- (4,5)-bisphosphate regulates sorting signal recognition by the clathrin-associated adaptor complex AP2. Mol Cell 18(5):519–531

    Article  PubMed  CAS  Google Scholar 

  78. Conner SD, Schmid SL (2002) Identification of an adaptor-associated kinase, AAK1, as a regulator of clathrin-mediated endocytosis. J Cell Biol 156(5):921–929

    Article  PubMed  CAS  Google Scholar 

  79. Conner SD, Schröter T, Schmid SL (2003) AAK1-mediated micro2 phosphorylation is stimulated by assembled clathrin. Traffic 4(12):885–890

    Article  PubMed  CAS  Google Scholar 

  80. Henderson DM, Conner SD (2007) A novel AAK1 splice variant functions at multiple steps of the endocytic pathway. Mol Biol Cell 18(7):2698–2706

    Article  PubMed  CAS  Google Scholar 

  81. Jackson AP, Flett A, Smythe C, Hufton L, Wettey FR, Smythe E (2003) Clathrin promotes incorporation of cargo into coated pits by activation of the AP2 adaptor micro2 kinase. J Cell Biol 163(2):231–236

    Article  PubMed  CAS  Google Scholar 

  82. Olusanya O, Andrews PD, Swedlow JR, Smythe E (2001) Phosphorylation of threonine 156 of the mu2 subunit of the AP2 complex is essential for endocytosis in vitro and in vivo. Curr Biol 11(11):896–900

    Article  PubMed  CAS  Google Scholar 

  83. Ricotta D, Conner SD, Schmid SL, von Figura K, Honing S (2002) Phosphorylation of the AP2 mu subunit by AAK1 mediates high affinity binding to membrane protein sorting signals. J Cell Biol 156(5):791–795

    Article  PubMed  CAS  Google Scholar 

  84. Shiratori T, Miyatake S, Ohno H, Nakaseko C, Isono K, Bonifacino JS, Saito T (1997) Tyrosine phosphorylation controls internalization of CTLA-4 by regulating its interaction with clathrin-associated adaptor complex AP-2. Immunity 6(5):583–589

    Article  PubMed  CAS  Google Scholar 

  85. Jurd R, Tretter V, Walker J, Brandon NJ, Moss SJ (2010) Fyn kinase contributes to tyrosine phosphorylation of the GABA (A) receptor gamma2 subunit. Mol Cell Neurosci 44(2):129–134, http://www.sciencedirect.com/science/article/pii/S1044743110000461

    Google Scholar 

  86. Goh LK, Huang F, Kim W, Gygi S, Sorkin A (2010) Multiple mechanisms collectively regulate clathrin-mediated endocytosis of the epidermal growth factor receptor. J Cell Biol 189(5):871–883

    Article  PubMed  CAS  Google Scholar 

  87. Huang F, Jiang X, Sorkin A (2003) Tyrosine phosphorylation of the beta2 subunit of clathrin adaptor complex AP-2 reveals the role of a di-leucine motif in the epidermal growth factor receptor trafficking. J Biol Chem 278(44):43411–43417

    Article  PubMed  CAS  Google Scholar 

  88. Sorkin A, Mazzotti M, Sorkina T, Scotto L, Beguinot L (1996) Epidermal growth factor receptor interaction with clathrin adaptors is mediated by the tyr974-containing internalization motif. J Biol Chem 271(23):13377–13384

    Article  PubMed  CAS  Google Scholar 

  89. Haucke V, De Camilli P (1999) AP-2 recruitment to synaptotagmin stimulated by tyrosine-­based endocytic motifs. Science 285(5431):1268–1271

    Article  PubMed  CAS  Google Scholar 

  90. Lee I, Doray B, Govero J, Kornfeld S (2008) Binding of cargo sorting signals to AP-1 enhances its association with ADP ribosylation factor 1-GTP. J Cell Biol 180(3):467–472

    Article  PubMed  CAS  Google Scholar 

  91. Ishiyama N, Lee S-H, Liu S, Li G-Y, Smith MJ, Reichardt LF, Ikura M (2010) Dynamic and static interactions between p120 catenin and e-cadherin regulate the stability of cell-cell adhesion. Cell 141(1):117–128

    Article  PubMed  CAS  Google Scholar 

  92. Davis MA, Ireton RC, Reynolds AB (2003) A core function for p120-catenin in cadherin turnover. J Cell Biol 163(3):525–534

    Article  PubMed  CAS  Google Scholar 

  93. Miyashita Y, Ozawa M (2007) Increased internalization of p120-uncoupled e-cadherin and a requirement for a dileucine motif in the cytoplasmic domain for endocytosis of the protein. J Biol Chem 282(15):11540–11548

    Article  PubMed  CAS  Google Scholar 

  94. Sato K, Watanabe T, Wang S, Kakeno M, Matsuzawa K, Matsui T, Yokoi K et al (2011) Numb controls e-cadherin endocytosis through p120 catenin with apkc. Mol Biol Cell 22(17):3103–3119

    Article  PubMed  CAS  Google Scholar 

  95. Chen WJ, Goldstein JL, Brown MS (1990) NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J Biol Chem 265(6):3116–3123

    PubMed  CAS  Google Scholar 

  96. Davis CG, Lehrman MA, Russell DW, Anderson RG, Brown MS, Goldstein JL (1986) The J.D. Mutation in familial hypercholesterolemia: amino acid substitution in cytoplasmic domain impedes internalization of LDL receptors. Cell 45(1):15–24

    Article  PubMed  CAS  Google Scholar 

  97. Hinrichsen L, Harborth J, Andrees L, Weber K, Ungewickell EJ (2003) Effect of clathrin heavy chain- and alpha-adaptin-specific small inhibitory RNAs on endocytic accessory proteins and receptor trafficking in HeLa cells. J Biol Chem 278(46):45160–45170

    Article  PubMed  CAS  Google Scholar 

  98. Motley A, Bright NA, Seaman MNJ, Robinson MS (2003) Clathrin-mediated endocytosis in ap-2-depleted cells. J Cell Biol 162(5):909–918

    Article  PubMed  CAS  Google Scholar 

  99. Garcia CK, Wilund K, Arca M, Zuliani G, Fellin R, Maioli M, Calandra S et al (2001) Autosomal recessive hypercholesterolemia caused by mutations in a putative LDL receptor adaptor protein. Science 292(5520):1394–1398

    Article  PubMed  CAS  Google Scholar 

  100. Mishra SK, Keyel PA, Hawryluk MJ, Agostinelli NR, Watkins SC, Traub LM (2002) Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor. EMBO J 21(18):4915–4926

    Article  PubMed  CAS  Google Scholar 

  101. Morris SM, Cooper JA (2001) Disabled-2 colocalizes with the LDLR in clathrin-coated pits and interacts with AP-2. Traffic 2(2):111–123

    Article  PubMed  CAS  Google Scholar 

  102. Santolini E, Puri C, Salcini AE, Gagliani MC, Pelicci PG, Tacchetti C, Di Fiore PP (2000) Numb is an endocytic protein. J Cell Biol 151(6):1345–1352

    Article  PubMed  CAS  Google Scholar 

  103. Chetrit D, Ziv N, Ehrlich M (2009) Dab2 regulates clathrin assembly and cell spreading. Biochem J 418(3):701–715

    Article  PubMed  CAS  Google Scholar 

  104. Eden ER, Sun X-M, Patel DD, Soutar AK (2007) Adaptor protein disabled-2 modulates low density lipoprotein receptor synthesis in fibroblasts from patients with autosomal recessive hypercholesterolaemia. Hum Mol Genet 16(22):2751–2759

    Article  PubMed  CAS  Google Scholar 

  105. Keyel PA, Mishra SK, Roth R, Heuser JE, Watkins SC, Traub LM (2006) A single common portal for clathrin-mediated endocytosis of distinct cargo governed by cargo-selective adaptors. Mol Biol Cell 17(10):4300

    Article  PubMed  CAS  Google Scholar 

  106. Maurer ME, Cooper JA (2006) The adaptor protein dab2 sorts LDL receptors into coated pits independently of AP-2 and ARH. J Cell Sci 119(pt 20):4235–4246

    Article  PubMed  CAS  Google Scholar 

  107. Uhlik MT, Temple B, Bencharit S, Kimple AJ, Siderovski DP, Johnson GL (2005) Structural and evolutionary division of phosphotyrosine binding (PTB) domains. J Mol Biol 345(1):1–20

    Article  PubMed  CAS  Google Scholar 

  108. Stolt PC, Bock HH (2006) Modulation of lipoprotein receptor functions by intracellular adaptor proteins. Cell Signal 18(10):1560–1571

    Article  PubMed  CAS  Google Scholar 

  109. Howell BW, Lanier LM, Frank R, Gertler FB, Cooper JA (1999) The disabled 1 phosphotyrosine-­binding domain binds to the internalization signals of transmembrane glycoproteins and to phospholipids. Mol Cell Biol 19(7):5179–5188

    PubMed  CAS  Google Scholar 

  110. Dvir H, Shah M, Girardi E, Guo L, Farquhar MG, Zajonc DM (2012) Atomic structure of the autosomal recessive hypercholesterolemia phosphotyrosine-binding domain in complex with the LDL-receptor tail. Proc Natl Acad Sci U S A 109(18):6916–6921

    Article  PubMed  CAS  Google Scholar 

  111. Edeling MA, Mishra SK, Keyel PA, Steinhauser AL, Collins BM, Roth R, Heuser JE, Owen DJ, Traub LM (2006) Molecular switches involving the AP-2 beta2 appendage regulate endocytic cargo selection and clathrin coat assembly. Dev Cell 10(3):329–342

    Article  PubMed  CAS  Google Scholar 

  112. Berdnik D, Török T, González-Gaitán M, Knoblich JA (2002) The endocytic protein alpha-­adaptin is required for numb-mediated asymmetric cell division in drosophila. Dev Cell 3(2):221–231

    Article  PubMed  CAS  Google Scholar 

  113. Kyriazis GA, Wei Z, Vandermey M, Jo D-G, Xin O, Mattson MP, Chan SL (2008) Numb endocytic adapter proteins regulate the transport and processing of the amyloid precursor protein in an isoform-dependent manner: implications for Alzheimer disease pathogenesis. J Biol Chem 283(37):25492–25502

    Article  PubMed  CAS  Google Scholar 

  114. Sorensen EB, Conner SD (2008) AAK1 regulates numb function at an early step in clathrin-­mediated endocytosis. Traffic 9(10):1791–1800

    Article  PubMed  CAS  Google Scholar 

  115. Nishimura T, Kaibuchi K (2007) Numb controls integrin endocytosis for directional cell migration with apkc and PAR-3. Dev Cell 13(1):15–28

    Article  PubMed  CAS  Google Scholar 

  116. Tokumitsu H, Hatano N, Yokokura S, Sueyoshi Y, Nozaki N, Kobayashi R (2006) Phosphorylation of numb regulates its interaction with the clathrin-associated adaptor AP-2. FEBS Lett 580(24):5797–5801

    Article  PubMed  CAS  Google Scholar 

  117. Schmid EM, Ford MG, Burtey A, Praefcke GJ, Peak-Chew SY, Mills IG, Benmerah A, McMahon HT (2006) Role of the AP2 beta-appendage hub in recruiting partners for ­clathrin-­coated vesicle assembly. PLoS Biol 4(9):e262, http://dx.doi.org/10.1371%2Fjournal.pbio.0040262

    Article  PubMed  CAS  Google Scholar 

  118. Südhof TC, Rothman JE (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323(5913):474–477

    Article  PubMed  CAS  Google Scholar 

  119. Koo SJ, Markovic S, Puchkov D, Mahrenholz CC, Beceren-Braun F, Maritzen T, Dernedde J, Volkmer R, Oschkinat H, Haucke V (2011) SNARE motif-mediated sorting of synaptobrevin by the endocytic adaptors clathrin assembly lymphoid myeloid leukemia (CALM) and AP180 at synapses. Proc Natl Acad Sci U S A 108(33):13540–13545

    Article  PubMed  CAS  Google Scholar 

  120. Miller SE, Sahlender DA, Graham SC, Honing S, Robinson MS, Peden AA, Owen DJ (2011) The molecular basis for the endocytosis of small r-snares by the clathrin adaptor CALM. Cell 147(5):1118–1131

    Article  PubMed  CAS  Google Scholar 

  121. Miller SE, Collins BM, McCoy AJ, Robinson MS, Owen DJ (2007) A snare-adaptor interaction is a new mode of cargo recognition in clathrin-coated vesicles. Nature 450(7169):570–574

    Article  PubMed  CAS  Google Scholar 

  122. Pryor PR, Jackson L, Gray SR, Edeling MA, Thompson A, Sanderson CM, Evans PR, Owen DJ, Paul Luzio J (2008) Molecular basis for the sorting of the SNARE VAMP7 into endocytic clathrin-coated vesicles by the arfgap hrb. Cell 134(5):817–827

    Article  PubMed  CAS  Google Scholar 

  123. Diril MK, Wienisch M, Jung N, Klingauf J, Haucke V (2006) Stonin 2 is an AP-2-dependent endocytic sorting adaptor for synaptotagmin internalization and recycling. Dev Cell 10(2):233–244

    Article  PubMed  CAS  Google Scholar 

  124. Martina JA, Bonangelino CJ, Aguilar RC, Bonifacino JS (2001) Stonin 2: an adaptor-like protein that interacts with components of the endocytic machinery. J Cell Biol 153(5):1111–1120

    Article  PubMed  CAS  Google Scholar 

  125. Voglmaier SM, Kam K, Yang H, Fortin DL, Hua Z, Nicoll RA, Edwards RH (2006) Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron 51(1):71–84

    Article  PubMed  CAS  Google Scholar 

  126. Magalhaes AC, Dunn H, Ferguson SSG (2012) Regulation of GPCR activity, trafficking and localization by gpcr-interacting proteins. Br J Pharmacol 165(6):1717–1736

    Article  PubMed  CAS  Google Scholar 

  127. Benovic JL, Strasser RH, Caron MG, Lefkowitz RJ (1986) Beta-adrenergic receptor kinase: identification of a novel protein kinase that phosphorylates the agonist-occupied form of the receptor. Proc Natl Acad Sci U S A 83(9):2797–2801

    Article  PubMed  CAS  Google Scholar 

  128. Fredericks ZL, Pitcher JA, Lefkowitz RJ (1996) Identification of the G protein-coupled receptor kinase phosphorylation sites in the human beta2-adrenergic receptor. J Biol Chem 271(23):13796–13803

    Article  PubMed  CAS  Google Scholar 

  129. Ferguson SS, Downey WE III, Colapietro AM, Barak LS, Ménard L, Caron MG (1996) Role of beta-arrestin in mediating agonist-promoted G protein-coupled receptor internalization. Science 271(5247):363–366

    Article  PubMed  CAS  Google Scholar 

  130. Goodman OB Jr, Krupnick JG, Santini F, Gurevich VV, Penn RB, Gagnon AW, Keen JH, Benovic JL (1996) Beta-arrestin acts as a clathrin adaptor in endocytosis of the beta2-­adrenergic receptor. Nature 383(6599):447–450

    Article  PubMed  CAS  Google Scholar 

  131. Kang DS, Kern RC, Puthenveedu MA, von Zastrow M, Williams JC, Benovic JL (2009) Structure of an arrestin2-clathrin complex reveals a novel clathrin binding domain that modulates receptor trafficking. J Biol Chem 284(43):29860–29872

    Article  PubMed  CAS  Google Scholar 

  132. Krupnick JG, Goodman OB Jr, Keen JH, Benovic JL (1997) Arrestin/clathrin interaction. Localization of the clathrin binding domain of nonvisual arrestins to the carboxy terminus. J Biol Chem 272(23):15011–15016

    Article  PubMed  CAS  Google Scholar 

  133. Milano SK, Pace HC, Kim Y-M, Brenner C, Benovic JL (2002) Scaffolding functions of arrestin-2 revealed by crystal structure and mutagenesis. Biochemistry 41(10):3321–3328

    Article  PubMed  CAS  Google Scholar 

  134. Laporte SA, Oakley RH, Holt JA, Barak LS, Caron MG (2000) The interaction of beta-­arrestin with the AP-2 adaptor is required for the clustering of beta 2-adrenergic receptor into clathrin-coated pits. J Biol Chem 275(30):23120–23126

    Article  PubMed  CAS  Google Scholar 

  135. Laporte SA, Oakley RH, Zhang J, Holt JA, Ferguson SS, Caron MG, Barak LS (1999) The beta2-adrenergic receptor/betaarrestin complex recruits the clathrin adaptor AP-2 during endocytosis. Proc Natl Acad Sci U S A 96(7):3712–3717

    Article  PubMed  CAS  Google Scholar 

  136. Hirsch JA, Schubert C, Gurevich VV, Sigler PB (1999) The 2.8 A crystal structure of visual arrestin: a model for arrestin’s regulation. Cell 97(2):257–269

    Article  PubMed  CAS  Google Scholar 

  137. Gurevich VV, Gurevich EV (2004) The molecular acrobatics of arrestin activation. Trends Pharmacol Sci 25(2):105–111

    Article  PubMed  CAS  Google Scholar 

  138. Gaidarov I, Krupnick JG, Falck JR, Benovic JL, Keen JH (1999) Arrestin function in G protein-­coupled receptor endocytosis requires phosphoinositide binding. EMBO J 18(4):871–881

    Article  PubMed  CAS  Google Scholar 

  139. Lin FT, Krueger KM, Kendall HE, Daaka Y, Fredericks ZL, Pitcher JA, Lefkowitz RJ (1997) Clathrin-mediated endocytosis of the beta-adrenergic receptor is regulated by phosphorylation/dephosphorylation of beta-arrestin1. J Biol Chem 272(49):31051–31057

    Article  PubMed  CAS  Google Scholar 

  140. Ahmed MR, Zhan X, Song X, Kook S, Gurevich VV, Gurevich EV (2011) Ubiquitin ligase parkin promotes Mdm2-arrestin interaction but inhibits arrestin ubiquitination. Biochemistry 50(18):3749–3763

    Article  PubMed  CAS  Google Scholar 

  141. Shenoy SK, McDonald PH, Kohout TA, Lefkowitz RJ (2001) Regulation of receptor fate by ubiquitination of activated beta 2- adrenergic receptor and beta-arrestin. Science 294(5545):1307–1313

    Article  PubMed  CAS  Google Scholar 

  142. Chen W, Kirkbride KC, How T, Nelson CD, Mo J, Frederick JP, Wang XF, Lefkowitz RJ, Blobe GC (2003) Beta-arrestin 2 mediates endocytosis of type III TGF-beta receptor and down-regulation of its signaling. Science 301(5638):1394–1397

    Article  PubMed  CAS  Google Scholar 

  143. Lin CH, MacGurn JA, Chu T, Stefan CJ, Emr SD (2008) Arrestin-related ubiquitin-ligase adaptors regulate endocytosis and protein turnover at the cell surface—supplemental info. Cell 135(4):714–725

    Article  PubMed  CAS  Google Scholar 

  144. Yu A, Rual J-F, Tamai K, Harada Y, Vidal M, He X, Kirchhausen T (2007) Association of dishevelled with the clathrin AP-2 adaptor is required for frizzled endocytosis and planar cell polarity signaling. Dev Cell 12(1):129–141

    Article  PubMed  CAS  Google Scholar 

  145. Canals M, Scholten DJ, de Munnik S, Han MK, Smit MJ, Leurs R (2012) Ubiquitination of CXCR7 controls receptor trafficking. PLoS One 7(3):e34192

    Article  PubMed  CAS  Google Scholar 

  146. Wolfe BL, Marchese A, Trejo JA (2007) Ubiquitination differentially regulates clathrin-­dependent internalization of protease-activated receptor-1. J Cell Biol 177(5):905–916

    Article  PubMed  CAS  Google Scholar 

  147. Miranda M, Sorkin A (2007) Regulation of receptors and transporters by ubiquitination: new insights into surprisingly similar mechanisms. Mol Interv 7(3):157–167

    Article  PubMed  CAS  Google Scholar 

  148. Komander D, Rape M (2012) The ubiquitin code. Annu Rev Biochem 81:203–229

    Article  PubMed  CAS  Google Scholar 

  149. Polo S, Sigismund S, Faretta M, Guidi M, Capua MR, Bossi G, Chen H, De Camilli P, Di Fiore PP (2002) A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416(6879):451–455

    Article  PubMed  CAS  Google Scholar 

  150. Sato Y, Yoshikawa A, Mimura H, Yamashita M, Yamagata A, Fukai S (2009) Structural basis for specific recognition of lys 63-linked polyubiquitin chains by tandem UIMs of RAP80. EMBO J 28(16):2461–2468

    Article  PubMed  CAS  Google Scholar 

  151. Sims JJ, Cohen RE (2009) Linkage-specific avidity defines the lysine 63-linked polyubiquitin-­binding preference of rap80. Mol Cell 33(6):775–783

    Article  PubMed  CAS  Google Scholar 

  152. Drake MT, Downs MA, Traub LM (2000) Epsin binds to clathrin by associating directly with the clathrin-terminal domain. Evidence for cooperative binding through two discrete sites. J Biol Chem 275(9):6479–6489

    Article  PubMed  CAS  Google Scholar 

  153. Yarden Y, Pines G (2012) The ERBB network: at last, cancer therapy meets systems biology. Nat Rev Cancer 12(8):553–563

    Article  PubMed  CAS  Google Scholar 

  154. Ferguson KM, Berger MB, Mendrola JM, Cho HS, Leahy DJ, Lemmon MA (2003) EGF activates its receptor by removing interactions that autoinhibit ectodomain dimerization. Mol Cell 11(2):507–517

    Article  PubMed  CAS  Google Scholar 

  155. Lemmon MA, Schlessinger J (2010) Cell signaling by receptor tyrosine kinases. Cell 141(7):1117–1134

    Article  PubMed  CAS  Google Scholar 

  156. Jiang X, Huang F, Marusyk A, Sorkin A (2003) Grb2 regulates internalization of EGF receptors through clathrin-coated pits. Mol Biol Cell 14(3):858–870

    Article  PubMed  CAS  Google Scholar 

  157. Jiang X, Sorkin A (2003) Epidermal growth factor receptor internalization through clathrin-­coated pits requires cbl RING finger and proline-rich domains but not receptor polyubiquitylation. Traffic 4(8):529–543

    Article  PubMed  CAS  Google Scholar 

  158. Levkowitz G, Waterman H, Zamir E, Kam Z, Oved S, Langdon WY, Beguinot L, Geiger B, Yarden Y (1998) C-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev 12(23):3663–3674

    Article  PubMed  CAS  Google Scholar 

  159. Waterman H, Katz M, Rubin C, Shtiegman K, Lavi S, Elson A, Jovin T, Yarden Y (2002) A mutant EGF-receptor defective in ubiquitylation and endocytosis unveils a role for Grb2 in negative signaling. EMBO J 21(3):303–313

    Article  PubMed  CAS  Google Scholar 

  160. Huang F, Kirkpatrick D, Jiang X, Gygi S, Sorkin A (2006) Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol Cell 21(6):737–748

    Article  PubMed  CAS  Google Scholar 

  161. Umebayashi K, Stenmark H, Yoshimori T (2008) Ubc4/5 and C-cbl continue to ubiquitinate EGF receptor after internalization to facilitate polyubiquitination and degradation. Mol Biol Cell 19(8):3454–3462

    Article  PubMed  CAS  Google Scholar 

  162. Huang F, Goh LK, Sorkin A (2007) EGF receptor ubiquitination is not necessary for its internalization. Proc Natl Acad Sci U S A 104(43):16904–16909

    Article  PubMed  CAS  Google Scholar 

  163. Haglund K, Sigismund S, Polo S, Szymkiewicz I, Di Fiore PP, Dikic I (2003) Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat Cell Biol 5(5):461–466

    Article  PubMed  CAS  Google Scholar 

  164. Frosi Y, Anastasi S, Ballarò C, Varsano G, Castellani L, Maspero E, Polo S, Alemà S, Segatto O (2010) A two-tiered mechanism of EGFR inhibition by RALT/MIG6 via kinase suppression and receptor degradation. J Cell Biol 189(3):557–571

    Article  PubMed  CAS  Google Scholar 

  165. Liu NS, Loo LS, Loh E, Seet L-F, Hong W (2009) Participation of Tom1L1 in EGF-stimulated endocytosis of EGF receptor. EMBO J 28(22):3485–3499

    Article  PubMed  CAS  Google Scholar 

  166. Madshus IH, Stang E (2009) Internalization and intracellular sorting of the EGF receptor: a model for understanding the mechanisms of receptor trafficking. J Cell Sci 122(pt 19):3433–3439

    Article  PubMed  CAS  Google Scholar 

  167. Sorkin A, Goh LK (2009) Endocytosis and intracellular trafficking of erbbs. Exp Cell Res 315(4):683–696

    Article  PubMed  CAS  Google Scholar 

  168. Duval M, Bédard-Goulet S, Delisle C, Gratton J-P (2003) Vascular endothelial growth factor-­dependent down-regulation of flk-1/KDR involves cbl-mediated ubiquitination. Consequences on nitric oxide production from endothelial cells. J Biol Chem 278(22):20091–20097

    Article  PubMed  CAS  Google Scholar 

  169. Fasen K, Cerretti DP, Huynh-Do U (2008) Ligand binding induces Cbl-dependent EphB1 receptor degradation through the lysosomal pathway. Traffic 9(2):251–266

    Article  PubMed  CAS  Google Scholar 

  170. Levkowitz G, Waterman H, Ettenberg SA, Katz M, Tsygankov AY, Alroy I, Lavi S et al (1999) Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol Cell 4(6):1029–1040

    Article  PubMed  CAS  Google Scholar 

  171. Marmor MD, Yarden Y (2004) Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene 23(11):2057–2070

    Article  PubMed  CAS  Google Scholar 

  172. Miyake S, Mullane-Robinson KP, Lill NL, Douillard P, Band H (1999) Cbl-mediated negative regulation of platelet-derived growth factor receptor-dependent cell proliferation. A critical role for cbl tyrosine kinase-binding domain. J Biol Chem 274(23):16619–16628

    Article  PubMed  CAS  Google Scholar 

  173. Penengo L, Rubin C, Yarden Y, Gaudino G (2003) C-Cbl is a critical modulator of the Ron tyrosine kinase receptor. Oncogene 22(24):3669–3679

    Article  PubMed  CAS  Google Scholar 

  174. Wilhelmsen K, Burkhalter S, van der Geer P (2002) C-Cbl binds the CSF-1 receptor at tyrosine 973, a novel phosphorylation site in the receptor’s carboxy-terminus. Oncogene 21(7):1079–1089

    Article  PubMed  CAS  Google Scholar 

  175. Arévalo JC, Waite J, Rajagopal R, Beyna M, Chen Z-Y, Lee FS, Chao MV (2006) Cell survival through trk neurotrophin receptors is differentially regulated by ubiquitination. Neuron 50(4):549–559

    Article  PubMed  CAS  Google Scholar 

  176. Monami G, Emiliozzi V, Morrione A (2008) Grb10/Nedd4-mediated multiubiquitination of the insulin-like growth factor receptor regulates receptor internalization. J Cell Physiol 216(2):426–437

    Article  PubMed  CAS  Google Scholar 

  177. Persaud A, Alberts P, Hayes M, Guettler S, Clarke I, Sicheri F, Dirks P, Ciruna B, Rotin D (2011) Nedd4-1 binds and ubiquitylates activated FGFR1 to control its endocytosis and function. EMBO J 30(16):3259–3273

    Article  PubMed  CAS  Google Scholar 

  178. Sundvall M, Korhonen A, Paatero I, Gaudio E, Melino G, Croce CM, Aqeilan RI, Elenius K (2008) Isoform-specific monoubiquitination, endocytosis, and degradation of alternatively spliced ErbB4 isoforms. Proc Natl Acad Sci U S A 105(11):4162–4167

    Article  PubMed  CAS  Google Scholar 

  179. Vecchione A, Marchese A, Henry P, Rotin D, Morrione A (2003) The Grb10/Nedd4 complex regulates ligand-induced ubiquitination and stability of the insulin-like growth factor I receptor. Mol Cell Biol 23(9):3363–3372

    Article  PubMed  CAS  Google Scholar 

  180. Rotin D, Staub O (2012) Nedd4-2 and the regulation of epithelial sodium transport. Front Physiol 3:212

    Article  PubMed  Google Scholar 

  181. Butterworth MB (2010) Regulation of the epithelial sodium channel (ENaC) by membrane trafficking. Biochim Biophys Acta 1802(12):1166–1177

    Article  PubMed  CAS  Google Scholar 

  182. Staub O, Gautschi I, Ishikawa T, Breitschopf K, Ciechanover A, Schild L, Rotin D (1997) Regulation of stability and function of the epithelial Na+ channel (ENaC) by ubiquitination. EMBO J 16(21):6325–6336

    Article  PubMed  CAS  Google Scholar 

  183. Miranda M, Wu CC, Sorkina T, Korstjens DR, Sorkin A (2005) Enhanced ubiquitylation and accelerated degradation of the dopamine transporter mediated by protein kinase C. J Biol Chem 280(42):35617–35624

    Article  PubMed  CAS  Google Scholar 

  184. García-Tardón N, González-González IM, Martínez-Villarreal J, Fernández-Sánchez E, Giménez C, Zafra F (2012) Protein kinase C (PKC)-promoted endocytosis of glutamate transporter GLT-1 requires ubiquitin ligase nedd4-2-dependent ubiquitination but not phosphorylation. J Biol Chem 287(23):19177–19187

    Article  PubMed  CAS  Google Scholar 

  185. Fernández-Sánchez E, Martínez-Villarreal J, Giménez C, Zafra F (2009) Constitutive and regulated endocytosis of the glycine transporter GLYT1b is controlled by ubiquitination. J Biol Chem 284(29):19482–19492

    Article  PubMed  CAS  Google Scholar 

  186. de Juan-Sanz J, Zafra F, López-Corcuera B, Aragón C (2011) Endocytosis of the neuronal glycine transporter GLYT2: role of membrane rafts and protein kinase c-dependent ubiquitination. Traffic 12(12):1850–1867

    Article  PubMed  CAS  Google Scholar 

  187. Vina-Vilaseca A, Bender-Sigel J, Sorkina T, Closs EI, Sorkin A (2011) Protein kinase c-dependent ubiquitination and clathrin-mediated endocytosis of the cationic amino acid transporter CAT-1. J Biol Chem 286(10):8697–8706

    Article  PubMed  CAS  Google Scholar 

  188. Loerke D, Mettlen M, Yarar D, Jaqaman K, Jaqaman H, Danuser G, Schmid SL (2009) Cargo and dynamin regulate clathrin-coated pit maturation. PLoS Biol 7(3):e57

    Article  PubMed  CAS  Google Scholar 

  189. Mettlen M, Loerke D, Yarar D, Danuser G, Schmid SL (2010) Cargo- and adaptor-specific mechanisms regulate clathrin-mediated endocytosis. J Cell Biol 188(6):919–933

    Article  PubMed  CAS  Google Scholar 

  190. Johannessen LE, Pedersen NM, Pedersen KW, Madshus IH, Stang E (2006) Activation of the epidermal growth factor (EGF) receptor induces formation of EGF receptor- and grb2-­containing clathrin-coated pits. Mol Cell Biol 26(2):389–401

    Article  PubMed  CAS  Google Scholar 

  191. Puri C, Tosoni D, Comai R, Rabellino A, Segat D, Caneva F, Luzzi P, Di Fiore PP, Tacchetti C (2005) Relationships between EGFR signaling-competent and endocytosis-competent membrane microdomains. Mol Biol Cell 16(6):2704–2718

    Article  PubMed  CAS  Google Scholar 

  192. Rappoport JZ, Simon SM (2009) Endocytic trafficking of activated EGFR is AP-2 dependent and occurs through preformed clathrin spots. J Cell Sci 122(pt 9):1301–1305

    Article  PubMed  CAS  Google Scholar 

  193. Santini F, Gaidarov I, Keen JH (2002) G protein-coupled receptor/arrestin3 modulation of the endocytic machinery. J Cell Biol 156(4):665–676

    Article  PubMed  CAS  Google Scholar 

  194. Cureton DK, Massol RH, Saffarian S, Kirchhausen TL, Whelan SP (2009) Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog 5(4):e1000394

    Article  PubMed  CAS  Google Scholar 

  195. Liu AP, Aguet F, Danuser G, Schmid SL (2010) Local clustering of transferrin receptors promotes clathrin-coated pit initiation. J Cell Biol 191(7):1381–1393

    Article  PubMed  CAS  Google Scholar 

  196. Meyerholz A, Hinrichsen L, Groos S, Esk PC, Brandes G, Ungewickell EJ (2005) Effect of clathrin assembly lymphoid myeloid leukemia protein depletion on clathrin coat formation. Traffic 6(12):1225–1234

    Article  PubMed  CAS  Google Scholar 

  197. Morgan JR, Zhao X, Womack M, Prasad K, Augustine GJ, Lafer EM (1999) A role for the clathrin assembly domain of AP180 in synaptic vesicle endocytosis. J Neurosci 19(23):10201–10212

    PubMed  CAS  Google Scholar 

  198. Nonet ML, Holgado AM, Brewer F, Serpe CJ, Norbeck BA, Holleran J, Wei L, Hartwieg E, Jorgensen EM, Alfonso A (1999) UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles. Mol Biol Cell 10(7): 2343–2360

    PubMed  CAS  Google Scholar 

  199. Heuser J, Kirchhausen T (1985) Deep-etch views of clathrin assemblies. J Ultrastruct Res 92(1–2):1–27

    Article  PubMed  CAS  Google Scholar 

  200. Saffarian S, Cocucci E, Kirchhausen T (2009) Distinct dynamics of endocytic clathrin-coated pits and coated plaques. PLoS Biol 7(9):e1000191

    Article  PubMed  CAS  Google Scholar 

  201. Puthenveedu MA, von Zastrow M (2006) Cargo regulates clathrin-coated pit dynamics. Cell 127(1):113–124

    Article  PubMed  CAS  Google Scholar 

  202. Ritter SL, Hall RA (2009) Fine-tuning of GPCR activity by receptor-interacting proteins. Nat Rev Mol Cell Biol 10(12):819–830

    Article  PubMed  CAS  Google Scholar 

  203. Tosoni D, Puri C, Confalonieri S, Salcini AE, De Camilli P, Tacchetti C, Di Fiore PP (2005) TTP specifically regulates the internalization of the transferrin receptor. Cell 123(5):875–888

    Article  PubMed  CAS  Google Scholar 

  204. Warren RA, Green FA, Enns CA (1997) Saturation of the endocytic pathway for the transferrin receptor does not affect the endocytosis of the epidermal growth factor receptor. J Biol Chem 272(4):2116–2121

    Article  PubMed  CAS  Google Scholar 

  205. Warren RA, Green FA, Stenberg PE, Enns CA (1998) Distinct saturable pathways for the endocytosis of different tyrosine motifs. J Biol Chem 273(27):17056–17063

    Article  PubMed  CAS  Google Scholar 

  206. Marks MS, Woodruff L, Ohno H, Bonifacino JS (1996) Protein targeting by tyrosine- and di-leucine-based signals: evidence for distinct saturable components. J Cell Biol 135(2):341–354

    Article  PubMed  CAS  Google Scholar 

  207. Cao TT, Mays RW, von Zastrow M (1998) Regulated endocytosis of G protein-coupled receptors by a biochemically and functionally distinct subpopulation of clathrin-coated pits. J Biol Chem 273(38):24592–24602

    Article  PubMed  CAS  Google Scholar 

  208. Mundell SJ, Luo J, Benovic JL, Conley PB, Poole AW (2006) Distinct clathrin-coated pits sort different G protein-coupled receptor cargo. Traffic 7(10):1420–1431

    Article  PubMed  CAS  Google Scholar 

  209. Lakadamyali M, Rust MJ, Zhuang X (2006) Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 124(5):997–1009

    Article  PubMed  CAS  Google Scholar 

  210. Leonard D, Hayakawa A, Lawe D, Lambright D, Bellve KD, Standley C, Lifshitz LM, Fogarty KE, Corvera S (2008) Sorting of EGF and transferrin at the plasma membrane and by cargo-specific signaling to eea1-enriched endosomes. J Cell Sci 121(pt 20):3445–3458

    Article  PubMed  CAS  Google Scholar 

  211. Doyon JB, Zeitler B, Cheng J, Cheng AT, Cherone JM, Santiago Y, Lee AH et al (2011) Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells. Nat Cell Biol 13(3):331–337

    Article  PubMed  CAS  Google Scholar 

  212. Eliceiri KW, Berthold MR, Goldberg IG, Ibáñez L, Manjunath BS, Martone ME, Murphy RF et al (2012) Biological imaging software tools. Nat Methods 9(7):697–710

    Article  PubMed  CAS  Google Scholar 

  213. Jaqaman K, Loerke D, Mettlen M, Kuwata H, Grinstein S, Schmid SL, Danuser G (2008) Robust single-particle tracking in live-cell time-lapse sequences. Nat Methods 5(8): 695–702

    Article  PubMed  CAS  Google Scholar 

  214. Liang L, Shen H, De Camilli P, Duncan JS (2010) Tracking clathrin coated pits with a multiple hypothesis based method. Med Image Comput Comput Assist Interv 13(pt 2):315–322

    PubMed  Google Scholar 

  215. Meijering E, Dzyubachyk O, Smal I (2012) Methods for cell and particle tracking. Methods Enzymol 504:183–200

    Article  PubMed  Google Scholar 

  216. Weigert R, Sramkova M, Parente L, Amornphimoltham P, Masedunskas A (2010) Intravital microscopy: a novel tool to study cell biology in living animals. Histochem Cell Biol 133(5):481–491

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

Supported by NIH grants CA089151 (AS), DA014204 (AS) and DA024698 (MAP).

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Authors and Affiliations

  1. Department of Cell Biology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA

    Alexander Sorkin

  2. Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, PA, USA

    Manojkumar A. Puthenveedu

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  2. Manojkumar A. Puthenveedu
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Correspondence to Alexander Sorkin or Manojkumar A. Puthenveedu .

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  1. Department of Biological Regulation, Candiotty Bldg, Hertzel St 1, Rehovot, 76100, Israel

    Yosef Yarden

  2. , Department of Biological Regulation, Weizmann Institute of Science, Hertzl Street 1, Rehovot, 76100, Israel

    Gabi Tarcic

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Sorkin, A., Puthenveedu, M.A. (2013). Clathrin-Mediated Endocytosis. In: Yarden, Y., Tarcic, G. (eds) Vesicle Trafficking in Cancer. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-6528-7_1

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