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Regulated portals of entry into the cell

Abstract

The plasma membrane is the interface between cells and their harsh environment. Uptake of nutrients and all communication among cells and between cells and their environment occurs through this interface. ‘Endocytosis’ encompasses several diverse mechanisms by which cells internalize macromolecules and particles into transport vesicles derived from the plasma membrane. It controls entry into the cell and has a crucial role in development, the immune response, neurotransmission, intercellular communication, signal transduction, and cellular and organismal homeostasis. As the complexity of molecular interactions governing endocytosis are revealed, it has become increasingly clear that it is tightly coordinated and coupled with overall cell physiology and thus, must be viewed in a broader context than simple vesicular trafficking.

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Figure 1: Multiple portals of entry into the mammalian cell.
Figure 2: Cargo-stimulated signalling pathways induce uptake by phagocytosis and caveolae.
Figure 3: Core components of the machinery driving clathrin-mediated endocytosis.
Figure 4: Clathrin-mediated endocytosis is accompanied by the temporally and spatially regulated interactions of multiple factors.

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References

  1. De Duve, C. Blueprint for a Cell: The Nature and Origin of Life (Patterson, Burlington, North Carolina, 1991)

    Google Scholar 

  2. Aderem, A. & Underhill, D. M. Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol. 17, 593–623 (1999)

    Article  CAS  PubMed  Google Scholar 

  3. Hall, A. & Nobes, C. D. Rho GTPases: Molecular switches that control the organization and dynamics of the actin cytoskeleton. Phil. Trans. R. Soc. Lond. B 355, 965–970 (2000)

    Article  CAS  Google Scholar 

  4. Fadok, V. A. & Chimini, G. The phagocytosis of apoptotic cells. Semin. Immunol. 13, 365–372 (2001)

    Article  CAS  PubMed  Google Scholar 

  5. Gold, E. S. et al. Dynamin 2 is required for phagocytosis in macrophages. J. Exp. Med. 190, 1849–1856 (1999)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Steele-Mortimer, O., Knodler, L. A. & Finlay, B. B. Poisons, ruffles and rockets: Bacterial pathogens and the host cell cytoskeleton. Traffic 1, 107–118 (2000)

    Article  CAS  PubMed  Google Scholar 

  7. Chimini, G. & Chavrier, P. Function of Rho family proteins in actin dynamics during phagocytosis and engulfment. Nature Cell Biol. 2, E191–E196 (2000)

    Article  CAS  PubMed  Google Scholar 

  8. Ridley, A. J. Rho proteins: Linking signaling with membrane trafficking. Traffic 2, 303–310 (2001)

    Article  CAS  PubMed  Google Scholar 

  9. Mellman, I. & Steinman, R. M. Dendritic cells: Specialized and regulated antigen processing machines. Cell 106, 255–258 (2001)

    Article  CAS  PubMed  Google Scholar 

  10. Anderson, R. G. The caveolae membrane system. Annu. Rev. Biochem. 67, 199–225 (1998)

    Article  CAS  PubMed  Google Scholar 

  11. Drab, M. et al. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293, 2449–2452 (2001)

    Article  ADS  CAS  PubMed  Google Scholar 

  12. 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 

  13. Pelkmans, L., Puntener, D. & Helenius, A. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 296, 535–539 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  14. Thomsen, P., Roepstorff, K., Stahlhut, M. & van Deurs, B. Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. Mol. Biol. Cell 13, 238–250 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Pelkmans, L. & Helenius, A. Endocytosis via caveolae. Traffic 3, 311–320 (2002)

    Article  CAS  PubMed  Google Scholar 

  16. Parton, R. G., Joggerst, B. & Simons, K. Regulated internalization of caveolae. J. Cell Biol. 127, 1199–1215 (1994)

    Article  CAS  PubMed  Google Scholar 

  17. Minshall, R. D. et al. Endothelial cell-surface gp60 activates vesicle formation and trafficking via Gi-coupled Src kinase signaling pathway. J. Cell Biol. 150, 1057–1070 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. 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 

  19. Edidin, M. Shrinking patches and slippery rafts: Scales of domains in the plasma membrane. Trends Cell Biol. 11, 492–496 (2001)

    Article  CAS  PubMed  Google Scholar 

  20. 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  ADS  CAS  PubMed  Google Scholar 

  21. Sandvig, K., Olsnes, S., Brown, J. E., Petersen, O. W. & van Deurs, B. Endocytosis from coated pits of Shiga toxin: A glycolipid-binding protein from Shigella dysenteriae 1. J. Cell Biol. 108, 1331–1343 (1989)

    Article  CAS  PubMed  Google Scholar 

  22. 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 

  23. Nichols, B. J. & Lippincott-Schwartz, J. Endocytosis without clathrin coats. Trends Cell Biol. 11, 406–412 (2001)

    Article  CAS  PubMed  Google Scholar 

  24. Artalejo, C. R., Elhamdani, A. & Palfrey, H. C. Sustained stimulation shifts the mechanism of endocytosis from dynamin-1-dependent rapid endocytosis to clathrin- and dynamin-2-mediated slow endocytosis in chromaffin cells. Proc. Natl Acad. Sci. USA 99, 6358–6363 (2002)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  25. Damke, H., Baba, T., van der Bliek, A. M. & Schmid, S. L. Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J. Cell Biol. 131, 69–80 (1995)

    Article  CAS  PubMed  Google Scholar 

  26. Schmid, S. L. Clathrin-coated vesicle formation and protein sorting: An integrated process. Annu. Rev. Biochem. 66, 511–548 (1997)

    Article  CAS  PubMed  Google Scholar 

  27. Brodsky, F. M., Chen, C.-Y., Kneuhl, C., Towler, M. C. & Wakeham, D. E. Biological basket weaving: Formation and function of clathrin-coated vesicles. Annu. Rev. Cell Dev. Biol. 17, 517–568 (2001)

    Article  CAS  PubMed  Google Scholar 

  28. Di Fiore, P. P. & De Camilli, P. Endocytosis and signaling: An inseparable partnership. Cell 106, 1–4 (2001)

    Article  CAS  PubMed  Google Scholar 

  29. Seto, E. S., Bellen, H. J. & Lloyd, T. E. When cell biology meets development: Endocytic regulation of signaling pathways. Genes Dev. 16, 1314–1336 (2002)

    Article  CAS  PubMed  Google Scholar 

  30. Beattie, E. C. et al. Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nature Neurosci. 3, 1291–1300 (2000)

    Article  CAS  PubMed  Google Scholar 

  31. De Camilli, P. & Takei, K. Molecular mechanisms in synaptic vesicle endocytosis and recycling. Neuron 16, 481–486 (1996)

    Article  CAS  PubMed  Google Scholar 

  32. Kirchhausen, T. Clathrin. Annu. Rev. Biochem. 69, 699–727 (2000)

    Article  CAS  PubMed  Google Scholar 

  33. Kirchhausen, T. Adaptors for clathrin-mediated traffic. Annu. Rev. Cell Dev. Biol. 15, 705–732 (1999)

    Article  CAS  PubMed  Google Scholar 

  34. Robinson, M. S. & Bonifacino, J. S. Adaptor-related proteins. Curr. Opin. Cell Biol. 13, 444–453 (2001)

    Article  CAS  PubMed  Google Scholar 

  35. Collins, B. M., McCoy, A. J., Kent, H. M., Evans, P. R. & Owen, D. J. Molecular architecture and functional model of the endocytic AP2 complex. Cell 109, 523–535 (2002)

    Article  CAS  PubMed  Google Scholar 

  36. Marsh, M. & McMahon, H. T. The structural era of endocytosis. Science 285, 215–220 (1999)

    Article  CAS  PubMed  Google Scholar 

  37. Lindner, R. & Ungewickell, E. Clathrin-associated proteins of bovine brain coated vesicles. J. Biol. Chem. 267, 16567–16573 (1992)

    CAS  PubMed  Google Scholar 

  38. McMahon, H. T. Endocytosis: An assembly protein for clathrin cages. Curr. Biol. 9, R332–R335 (1999)

    Article  CAS  PubMed  Google Scholar 

  39. Wendland, B. & Emr, S. D. Pan1p, yeast eps15, functions as a multivalent adaptor that coordinates protein-protein interactions essential for endocytosis. J. Cell Biol. 141, 71–84 (1998)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Tebar, F., Bohlander, S. K. & Sorkin, A. Clathrin assembly lymphoid myeloid leukemia (CALM) protein: Localization in endocytic-coated pits, interactions with clathrin, and the impact of overexpression on clathrin-mediated traffic. Mol. Biol. Cell 10, 2687–2702 (1999)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Springer, S., Spang, A. & Schekman, R. A primer on vesicle budding. Cell 97, 145–148 (1999)

    Article  CAS  PubMed  Google Scholar 

  42. Rothman, J. E. The machinery and principles of vesicle transport in the cell. Nature Med. 8, 1059–1062 (2002)

    Article  CAS  PubMed  Google Scholar 

  43. Lin, H. C., Moore, M. S., Sanan, D. A. & Anderson, R. G. W. Reconstitution of clathrin-coated pit budding from plasma membranes. J. Cell Biol. 114, 881–891 (1991)

    Article  CAS  PubMed  Google Scholar 

  44. Smythe, E., Carter, L. L. & Schmid, S. L. Cytosol- and clathrin-dependent stimulation of endocytosis in vitro by purified adaptors. J. Cell Biol. 119, 1163–1171 (1992)

    Article  CAS  PubMed  Google Scholar 

  45. Gilbert, A., Paccaud, J. P. & Carpentier, J. L. Direct measurement of clathrin-coated vesicle formation using a cell-free assay. J. Cell Sci. 110, 3105–3115 (1997)

    CAS  PubMed  Google Scholar 

  46. Hinshaw, J. E. Dynamin and its role in membrane fission. Annu. Rev. Cell Dev. Biol. 16, 483–519 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Sever, S., Damke, H. & Schmid, S. L. Garrotes, springs, ratchets and whips: Putting dynamin models to the test. Traffic 1, 385–392 (2000)

    Article  CAS  PubMed  Google Scholar 

  48. Hinshaw, J. E. & Schmid, S. L. Dynamin self assembles into rings suggesting a mechanism for coated vesicle budding. Nature 374, 190–192 (1995)

    Article  ADS  CAS  PubMed  Google Scholar 

  49. Sweitzer, S. & Hinshaw, J. Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93, 1021–1029 (1998)

    Article  CAS  PubMed  Google Scholar 

  50. Stowell, M. H. B., Marks, B., Wigge, P. & McMahon, H. T. Nucleotide-dependent conformational changes in dynamin: Evidence for a mechanochemical molecular spring. Nature Cell Biol. 1, 27–32 (1999)

    Article  CAS  PubMed  Google Scholar 

  51. Sever, S., Muhlberg, A. B. & Schmid, S. L. Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature 398, 481–486 (1999)

    Article  ADS  CAS  PubMed  Google Scholar 

  52. Song, B. D. & Schmid, S. L. A Molecular motor or a regulator? Dynamin's in a class of its own. Biochemistry 42, 1369–1376 (2003)

    Article  CAS  PubMed  Google Scholar 

  53. Damke, H., Baba, T., Warnock, D. E. & Schmid, S. L. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915–934 (1994)

    Article  CAS  PubMed  Google Scholar 

  54. Damke, H., Binns, D. D., Ueda, H., Schmid, S. L. & Baba, T. Dynamin GTPase domain mutants block endocytic vesicle formation at morphologically distinct stages. Mol. Biol. Cell 12, 2578–2589 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Marks, B. et al. GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410, 231–235 (2001)

    Article  ADS  CAS  PubMed  Google Scholar 

  56. Sever, S., Damke, H. & Schmid, S. L. Dynamin:GTP controls the formation of constricted coated pits, the rate limiting step in clathrin-mediated endocytosis. J. Cell Biol. 150, 1137–1148 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Rothman, J. E. Mechanisms of intracellular protein transport. Nature 372, 55–63 (1994)

    Article  ADS  CAS  PubMed  Google Scholar 

  58. Slepnev, V. I. & De Camilli, P. Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nature Rev. Neurosci. 1, 161–172 (2000)

    Article  CAS  Google Scholar 

  59. Farsad, K. et al. Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J. Cell Biol. 155, 193–200 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Takei, K. et al. Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes. Cell 94, 131–141 (1998)

    Article  CAS  PubMed  Google Scholar 

  61. Ford, M. G. et al. Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291, 1051–1055 (2001)

    Article  ADS  CAS  PubMed  Google Scholar 

  62. Gaidarov, I., Santini, F., Warren, R. A. & Keen, J. H. Spatial control of coated pit dynamics in living cells. Nature Cell Biol. 1, 1–7 (1999)

    Article  CAS  PubMed  Google Scholar 

  63. Roos, J. & Kelly, R. B. The endocytic machinery in nerve terminals surrounds sites of exocytosis. Curr. Biol. 9, 1411–1414 (1999)

    Article  CAS  PubMed  Google Scholar 

  64. Wigge, P. & McMahon, H. T. The amphiphysin family of proteins and their role in endocytosis at the synapse. Trends Neurosci. 21, 339–344 (1998)

    Article  CAS  PubMed  Google Scholar 

  65. Zhang, B. & Zelhof, A. C. Amphiphysins: Raising the BAR for synaptic vesicle recycling and membrane dynamics. Traffic 3, 452–460 (2002)

    Article  CAS  PubMed  Google Scholar 

  66. Benmerah, A., Bayrou, M., Cerf-Bensussan, N. & Dautry-Varsat, A. Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J. Cell Sci. 112, 1303–1311 (1999)

    CAS  PubMed  Google Scholar 

  67. 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 

  68. Ford, M. G. et al. Curvature of clathrin-coated pits driven by epsin. Nature 419, 361–366 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  69. Hyman, J., Chen, H., Di Fiore, P. P., De Camilli, P. & Brunger, A. T. Epsin 1 undergoes nucleocytosolic shuttling and its eps15 interactor NH2-terminal homology (ENTH) domain, structurally similar to Armadillo and HEAT repeats, interacts with the transcription factor promyelocytic leukemia Zn2+ finger protein (PLZF). J. Cell Biol. 149, 537–546 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Doria, M. et al. The eps15 homology (EH) domain-based interaction between eps15 and hrb connects the molecular machinery of endocytosis to that of nucleocytosolic transport. J. Cell Biol. 147, 1379–1384 (1999)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Yamabhai, M. et al. Intersectin, a novel adaptor protein with two Eps15 homology and five Src homology 3 domains. J. Biol. Chem. 273, 31401–31407 (1998)

    Article  CAS  PubMed  Google Scholar 

  72. McPherson, P. S., Kay, B. K. & Hussain, N. K. Signaling on the endocytic pathway. Traffic 2, 375–384 (2001)

    Article  CAS  PubMed  Google Scholar 

  73. Cremona, O. & De Camilli, P. Phosphoinositides in membrane traffic at the synapse. J. Cell Sci. 114, 1041–1052 (2001)

    CAS  PubMed  Google Scholar 

  74. Takei, K., Slepnev, V. I., Haucke, V. & De Camilli, P. Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nature Cell Biol. 1, 33–39 (1999)

    Article  CAS  PubMed  Google Scholar 

  75. Burger, K. N., Demel, R. A., Schmid, S. L. & de Kruijff, B. Dynamin is membrane-active: Lipid insertion is induced by phosphoinositides and phosphatidic acid. Biochemistry 39, 12485–12493 (2000)

    Article  CAS  PubMed  Google Scholar 

  76. Schmidt, A. et al. Endophilin I mediates synaptic vesicle formation by transfer of arachidonate to lysophosphatidic acid. Nature 401, 133–141 (1999)

    Article  ADS  CAS  PubMed  Google Scholar 

  77. Ayscough, K. R. Endocytosis and the development of cell polarity in yeast require a dynamic F-actin cytoskeleton. Curr. Biol. 10, 1587–1590 (2000)

    Article  CAS  PubMed  Google Scholar 

  78. Fujimoto, L. M., Roth, R., Heuser, J. E. & Schmid, S. L. Actin assembly plays a variable, but not obligatory role in receptor-mediated endocytosis in mammalian cells. Traffic 1, 161–171 (2000)

    Article  CAS  PubMed  Google Scholar 

  79. Qualmann, B., Kessels, M. M. & Kelly, R. B. Molecular links between endocytosis and the actin cytoskeleton. J. Cell Biol. 150, F111–F116 (2000)

    Article  CAS  PubMed  Google Scholar 

  80. Merrifield, C. J. et al. Endocytic vesicles move at the tips of actin tails in cultured mast cells. Nature Cell Biol. 1, 72–74 (1999)

    Article  CAS  PubMed  Google Scholar 

  81. Merrifield, C., Feldman, M. E., Wan, L. & Almers, W. Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nature Cell Biol. 4, 691–698 (2002)

    Article  CAS  PubMed  Google Scholar 

  82. Lee, E. & De Camilli, P. Dynamin at actin tails. Proc. Natl Acad. Sci. USA 99, 161–166 (2002)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  83. Orth, J. D., Krueger, E. W., Cao, H. & McNiven, M. A. The large GTPase dynamin regulates actin comet formation and movement in living cells. Proc. Natl Acad. Sci. USA 99, 167–172 (2002)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  84. Cousin, M. A. & Robinson, P. J. The dephosphins: Dephosphorylation by calcineurin triggers synaptic vesicle endocytosis. Trends Neurosci. 24, 659–665 (2001)

    Article  CAS  PubMed  Google Scholar 

  85. Wilde, A. & Brodsky, F. M. In vivo phosphorylation of adaptors regulates their interaction with clathrin. J. Cell Biol. 135, 635–646 (1996)

    Article  CAS  PubMed  Google Scholar 

  86. Fingerhut, A., von Figura, K. & Honing, S. Binding of AP2 to sorting signals is modulated by AP2 phosphorylation. J. Biol. Chem. 276, 5476–5482 (2001)

    Article  CAS  PubMed  Google Scholar 

  87. Olusanya, O., Andrews, P. D., Swedlow, J. R. & Smythe, E. Phosphorylation of threonine 156 of the µ2 subunit of the AP2 complex is essential for endocytosis in vitro and in vivo. Curr. Biol. 11, 896–900 (2001)

    Article  CAS  PubMed  Google Scholar 

  88. Greener, T., Zhao, X., Nojima, H., Eisenberg, E. & Greene, L. E. Role of cyclin G-associated kinase in uncoating clathrin-coated vesicles from non-neuronal cells. J. Biol. Chem. 275, 1365–1370 (2000)

    Article  CAS  PubMed  Google Scholar 

  89. Korolchuk, V. I. & Banting, G. CK2 and GAK/auxilin2 are major protein kinases in clathrin-coated vesicles. Traffic 3, 428–439 (2002)

    Article  CAS  PubMed  Google Scholar 

  90. Conner, S. D. & Schmid, S. L. Identification of an adaptor-associated kinase, AAK1, as a regulator of clathrin-mediated endocytosis. J. Cell Biol. 156, 921–929 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Ricotta, D., Conner, S. D., Schmid, S. L., von Figura, K. & Honing, S. Phosphorylation of the AP2 µ subunit by AAK1 mediates high affinity binding to membrane protein sorting signals. J. Cell Biol. 156, 791–795 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Warren, R. A., Green, F. A., Stenberg, P. E. & Enns, C. A. Distinct saturable pathways for the endocytosis of different tyrosine motifs. J. Biol. Chem. 273, 17056–17063 (1998)

    Article  CAS  PubMed  Google Scholar 

  93. Morris, S. M. & Cooper, J. A. Disabled-2 colocalizes with the LDLR in clathrin-coated pits and interacts with AP-2. Traffic 2, 111–123 (2001)

    Article  CAS  PubMed  Google Scholar 

  94. Mishra, S. K. et al. Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor. EMBO J. 21, 4915–4926 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Miller, W. E. & Lefkowitz, R. J. Expanding roles for β-arrestins as scaffolds and adapters in GPCR signaling and trafficking. Curr. Opin. Cell Biol. 13, 139–145 (2001)

    Article  CAS  PubMed  Google Scholar 

  96. Hicke, L. A new ticket for entry into budding vesicles—ubiquitin. Cell 106, 527–530 (2001)

    Article  CAS  PubMed  Google Scholar 

  97. 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 

  98. Ahn, S. et al. Src-dependent tyrosine phosphorylation regulates dynamin self-assembly and ligand-induced endocytosis of the epidermal growth factor receptor. J. Biol. Chem. 277, 26642–26651 (2002)

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank R. Milligan, M. G. Finn and C. Waterman-Storer for critically reading the manuscript, and acknowledge the many researchers whose important contributions to the primary literature can be found in the reviews that were cited owing to space limitations.

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Conner, S., Schmid, S. Regulated portals of entry into the cell. Nature 422, 37–44 (2003). https://doi.org/10.1038/nature01451

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