Endocytosis and signalling: Intertwining molecular networks

Nature Reviews Molecular Cell Biology

Volumn 10, Issue 9, 2009, Pages 609-622

  Sorkin, Alexander ^a   Von Zastrow, Mark ^b  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; BETA ARRESTIN; CELL PROTEIN; DISHEVELLED PROTEIN; EPSIN; G PROTEIN COUPLED RECEPTOR; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; INTERSECTIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1 PARTNER 1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; NOTCH RECEPTOR; PHOSPHOTYROSINE INTERACTION ADAPTOR PROTEIN 1; PHOSPHOTYROSINE INTERACTION ADAPTOR PROTEIN 2; PROTEIN P14; PROTEIN P18; PROTEIN TYROSINE KINASE; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

CELL MEMBRANE; CELL SURFACE; ENDOCYTOSIS; ENDOSOME; HUMAN; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION;

ANIMALS; CELL MEMBRANE; ENDOCYTOSIS; HUMANS; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 69249137477     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm2748     Document Type: Review

References (151)

1. Polo, s. & Di Fiore, P. P. Endocytosis conducts the cell signaling orchestra. Cell 124, 897-900 (2006).
2. von Zastrow, M. & sorkin, A. signaling on the endocytic pathway. Curr. Opin. Cell Biol. (2007).
3. Conner, s. D. & schmid, s. L. Regulated portals of entry into the cell. Nature 422, 37-44 (2003).
4. sorkin, A. Cargo recognition during clathrin-mediated endocytosis: a team effort. Curr. Opin. Cell Biol. 16, 392-399 (2004).
5. Doherty, G. J. & McMahon, H. T. Mechanisms of endocytosis. Annu. Rev. Biochem. 78, 857-902 (2009).
6. Yao, D., Ehrlich, M., Henis, Y. I. & Leof, E. B. Transforming growth factor-β receptors interact with AP2 by direct binding to β2 subunit. Mol. Biol. Cell 13, 4001-4012 (2002).
7. Kumar, K. G. et al. site-specific ubiquitination exposes a linear motif to promote interferon-α receptor endocytosis. J. Cell Biol. 179, 935-950 (2007).
8. Brett, T. J. & Traub, L. M. Molecular structures of coat and coat-associated proteins: function follows form. Curr. Opin. Cell Biol. 18, 395-406 (2006).
9. Yu, A. et al. Association of dishevelled with the clathrin ap-2 adaptor is required for frizzled endocytosis and planar cell polarity signaling. Dev. Cell 12, 129-141 (2007).
10. Gurevich, V. V. et al. Arrestin interactions with G protein-coupled receptors. Direct binding studies of wild type and mutant arrestins with rhodopsin, β2-adrenergic, and m2 muscarinic cholinergic receptors. J. Biol. Chem. 270, 720-731 (1995).
11. Moore, C. A., Milano, s. K. & Benovic, J. L. Regulation of receptor trafficking by GRKs and arrestins. Annu. Rev. Physiol. 69, 451-482 (2007).
12. Edeling, M. A. et al. Molecular switches involving the AP-2 β2 appendage regulate endocytic cargo selection and clathrin coat assembly. Dev. Cell 10, 329-342 (2006).
13. Gaidarov, I., Krupnick, J. G., Falck, J. R., Benovic, J. L. & Keen, J. H. Arrestin function in G protein-coupled receptor endocytosis requires phosphoinositide binding. EMBO J. 18, 871-881 (1999).
14. shenoy, s. K., McDonald, P. H., Kohout, T. A. & Lefkowitz, R. J. Regulation of receptor fate by ubiquitination of activated β2-adrenergic receptor and β-arrestin. Science 294, 1307-1313 (2001).
15. Hicke, L. & Riezman, H. Ubiquitination of a yeast plasma membrane receptor signals its ligandstimulated endocytosis. Cell 84, 277-287 (1996).
16. Gupta-Rossi, N. et al. Monoubiquitination and endocytosis direct γ-secretase cleavage of activated Notch receptor. J. Cell Biol. 166, 73-83 (2004).
17. Kazazic, M. et al. Epsin 1 is involved in recruitment of ubiquitinated EGF receptors into clathrin-coated pits. Traffic 10, 235-245 (2009).
18. Arevalo, J. C. et al. Cell survival through Trk neurotrophin receptors is differentially regulated by ubiquitination. Neuron 50, 549-559 (2006).
19. Peschard, P. et al. Mutation of the c-Cbl TKB domain binding site on the Met receptor tyrosine kinase converts it into a transforming protein. Mol. Cell 8, 995-1004 (2001).
20. Jiang, X., Huang, F., Marusyk, A. & sorkin, A. Grb2 regulates internalization of EGF receptors through clathrin-coated pits. Mol. Biol. Cell 14, 858-870 (2003).
21. Traub, L. M. & Lukacs, G. L. Decoding ubiquitin sorting signals for clathrin-dependent endocytosis by CLAsPs. J. Cell Sci. 120, 543-553 (2007).
22. Wolfe, B. L., Marchese, A. & Trejo, J. Ubiquitination differentially regulates clathrin-dependent internalization of protease-activated receptor-1. J. Cell Biol. 177, 905-916 (2007).
23. Hanyaloglu, A. C. & von Zastrow, M. Regulation of GPCRs by endocytic membrane trafficking and its potential implications. Annu. Rev. Pharmacol. Toxicol. 48, 537-568 (2008).
24. Nickerson, D. P., Russell, M. R. & Odorizzi, G. A concentric circle model of multivesicular body cargo sorting. EMBO Rep. 8, 644-650 (2007).
25. Raiborg, C. & stenmark, H. The EsCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445-452 (2009).
26. Jekely, G., sung, H. H., Luque, C. M. & Rorth, P. Regulators of endocytosis maintain localized receptor tyrosine kinase signaling in guided migration. Dev. Cell 9, 197-207 (2005).
27. McLaughlin, s. & Murray, D. Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438, 605-611 (2005).
28. Haugh, J. M. & Meyer, T. Active EGF receptors have limited access to PtdIns(4, 5)P(2) in endosomes: implications for phospholipase C and PI 3-kinase signaling. J. Cell Sci. 115, 303-310 (2002).
29. sasaki, T., sasaki, J., sakai, T., Takasuga, s. & suzuki, A. The physiology of phosphoinositides. Biol. Pharm. Bull. 30, 1599-1604 (2007).
30. sorkin, A. & Von Zastrow, M. signal transduction and endocytosis: close encounters of many kinds. Nature Rev. Mol. Cell Biol. 3, 600-614 (2002).
31. Vieira, A. V., Lamaze, C. & schmid, s. L. Control of EGF receptor signaling by clathrin-mediated endocytosis. Science 274, 2086-2089 (1996). The requirement of clathrin-dependent endocytosis for the full activation of ERK1 and ERK2 by EGFR is shown for the first time.
32. Kermorgant, s. & Parker, P. J. Receptor trafficking controls weak signal delivery: a strategy used by c-Met for sTAT3 nuclear accumulation. J. Cell Biol. 182, 855-863 (2008).
33. Lampugnani, M. G., Orsenigo, F., Gagliani, M. C., Tacchetti, C. & Dejana, E. Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments. J. Cell Biol. 174, 593-604 (2006).
34. sigismund, s. et al. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev. Cell 15, 209-219 (2008).
35. Galperin, E. & sorkin, A. Endosomal targeting of MEK2 requires RAF, MEK kinase activity and clathrindependent endocytosis. Traffic 9, 1776-1790 (2008).
36. Johannessen, L. E., Ringerike, T., Molnes, J. & Madshus, I. H. Epidermal growth factor receptor efficiently activates mitogen-activated protein kinase in HeLa cells and hep2 cells conditionally defective in clathrin-dependent endocytosis. Exp. Cell Res. 260, 136-145 (2000).
37. DeGraff, J. L., Gagnon, A. W., Benovic, J. L. & Orsini, M. J. Role of arrestins in endocytosis and signaling of α2-adrenergic receptor subtypes. J. Biol. Chem. 274, 11253-11259 (1999).
38. Teis, D., Wunderlich, W. & Huber, L. A. Localization of the MP1-MAPK scaffold complex to endosomes is mediated by p14 and required for signal transduction. Dev. Cell 3, 803-814 (2002).
39. Nada, s. et al. The novel lipid raft adaptor p18 controls endosome dynamics by anchoring the MEK-ERK pathway to late endosomes. EMBO J. 28, 477-489 (2009).
40. Teis, D. et al. p14-MP1-MEK1 signaling regulates endosomal traffic and cellular proliferation during tissue homeostasis. J. Cell Biol. 175, 861-868 (2006). The first demonstration of the assembly of a MAPK signalling complex in late endosomes and of the importance of this complex for the activation of ERK1 and ERK2 by EGFR.
41. Pullikuth, A., McKinnon, E., schaeffer, H. J. & Catling, A. D. The MEK1 scaffolding protein MP1 regulates cell spreading by integrating PAK1 and Rho signals. Mol. Cell. Biol. 25, 5119-5133 (2005).
42. Daaka, Y. et al. Essential role for G protein-coupled receptor endocytosis in the activation of mitogenactivated protein kinase. J. Biol. Chem. 273, 685-688 (1998). Early evidence supporting the hypothesis of endosomal signalling by GPCRs.
43. Oakley, R. H., Laporte, s. A., Holt, J. A., Barak, L. s. & Caron, M. G. Association of β-arrestin with G proteincoupled receptors during clathrin-mediated endocytosis dictates the profile of receptor resensitization. J. Biol. Chem. 274, 32248-32257 (1999).
44. DeFea, K. A. et al. β-arrestin-dependent endocytosis of proteinase-activated receptor 2 is required for intracellular targeting of activated ERK1/2. J. Cell Biol. 148, 1267-1281 (2000). This study provides evidence that β-arrestins control the selectivity of GPCR signalling from the endocytic pathway by physically restricting the localization of a GPCR-activated MAPK.
45. DeWire, s. M., Ahn, s., Lefkowitz, R. J. & shenoy, s. K. β-arrestins and cell signaling. Annu. Rev. Physiol. 69, 483-510 (2007).
46. Terrillon, s. & Bouvier, M. Receptor activityindependent recruitment of βarrestin2 reveals specific signalling modes. EMBO J. 23, 3950-3961 (2004).
47. Garcia-Regalado, A. et al. G protein-coupled receptorpromoted trafficking of Gβ1γ2 leads to AKT activation at endosomes via a mechanism mediated by Gβ1γ2- Rab11a interaction. Mol. Biol. Cell 19, 4188-4200 (2008).
48. Watson, F. L. et al. Rapid nuclear responses to targetderived neurotrophins require retrograde transport of ligand-receptor complex. J. Neurosci. 19, 7889-7900 (1999).
49. Cui, B. et al. One at a time, live tracking of NGF axonal transport using quantum dots. Proc. Natl Acad. Sci. USA 104, 13666-13671 (2007).
50. Grimes, M. L. et al. Endocytosis of activated TrkA: evidence that nerve growth factor induces formation of signaling endosomes. J. Neuroscience 16, 7950-7964 (1996). Biochemical evidence for the assembly of specific NTRK1 signalling complexes on endosomes that are involved in retrograde signalling in neurons.
51. Howe, C. L., Valletta, J. s., Rusnak, A. s. & Mobley, W. C. NGF signaling from clathrin-coated vesicles: evidence that signaling endosomes serve as a platform for the Ras-MAPK pathway. Neuron 32, 801-814 (2001).
52. Wu, C., Lai, C. F. & Mobley, W. C. Nerve growth factor activates persistent Rap1 signaling in endosomes. J. Neurosci. 21, 5406-5416 (2001).
53. Wu, C., Cui, B., He, L., Chen, L. & Mobley, W. C. The coming of age of axonal neurotrophin signaling endosomes. J. Proteomics 72, 46-55 (2009).
54. Wu, C. et al. A functional dynein-microtubule network is required for NGF signaling through the Rap1/MAPK pathway. Traffic 8, 1503-1520 (2007).
55. Watson, F. L. et al. Neurotrophins use the Erk5 pathway to mediate a retrograde survival response. Nature Neurosci. 4, 981-988 (2001). This study identifies ERK5 as being specifically involved in retrograde signalling by neurotrophins. It also shows the importance of clathrin-mediated endocytosis in the axonal termini and of retrograde endosomal transport for ERK5 activation in the neuronal soma.
56. Zheng, J. et al. Clathrin-dependent endocytosis is required for TrkB-dependent Akt-mediated neuronal protection and dendritic growth. J. Biol. Chem. 283, 13280-13288 (2008).
57. Delcroix, J. D. et al. NGF signaling in sensory neurons: evidence that early endosomes carry NGF retrograde signals. Neuron 39, 69-84 (2003).
58. Deinhardt, K. et al. Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron 52, 293-305 (2006).
59. Valdez, G. et al. Pincher-mediated macroendocytosis underlies retrograde signaling by neurotrophin receptors. J. Neurosci. 25, 5236-5247 (2005).
60. Valdez, G. et al. Trk-signaling endosomes are generated by Rac-dependent macroendocytosis. Proc. Natl Acad. Sci. USA 104, 12270-12275 (2007).
61. Mok, s. A. & Campenot, R. B. A nerve growth factorinduced retrograde survival signal mediated by mechanisms downstream of TrkA. Neuropharmacology 52, 270-278 (2007).
62. Cox, L. J., Hengst, U., Gurskaya, N. G., Lukyanov, K. A. & Jaffrey, s. R. Intra-axonal translation and retrograde trafficking of CREB promotes neuronal survival. Nature Cell Biol. 10, 149-159 (2008).
63. Tsukazaki, T., Chiang, T. A., Davison, A. F., Attisano, L. & Wrana, J. L. sARA, a FYVE domain protein that recruits smad2 to the TGFβ receptor. Cell 95, 779-791 (1998). The first demonstration of the role of a FYVE domain protein (SARA) and endosomes in TGFβ signalling.
64. Hayes, s., Chawla, A. & Corvera, s. TGF β receptor internalization into EEA1-enriched early endosomes: role in signaling to smad2. J. Cell Biol. 158, 1239-1249 (2002).
65. Chen, Y. G., Wang, Z., Ma, J., Zhang, L. & Lu, Z. Endofin, a FYVE domain protein, interacts with smad4 and facilitates TGF-β signaling. J. Biol. Chem. 282, 9688-9695 (2007).
66. Hartung, A. et al. Different routes of bone morphogenic protein (BMP) receptor endocytosis influence BMP signaling. Mol. Cell. Biol. 26, 7791-7805 (2006).
67. Lu, Z. et al. Transforming growth factor β activates smad2 in the absence of receptor endocytosis. J. Biol. Chem. 277, 29363-29368 (2002).
68. slessareva, J. E., Routt, s. M., Temple, B., Bankaitis, V. A. & Dohlman, H. G. Activation of the phosphatidylinositol 3-kinase Vps34 by a G protein α subunit at the endosome. Cell 126, 191-203 (2006). This study provides direct evidence linking trimeric G proteins to signalling from endosomes.
69. Mullershausen, F. et al. Persistent signaling induced by FTY720-phosphate is mediated by internalized s1P1 receptors. Nature Chem. Biol. 5, 428-434 (2009).
70. Calebiro, D. et al. Persistent cAMP-signals triggered by internalized G-protein-coupled receptors. PLoS Biol. 18 Aug 2009 (doi:10.1371/journal. pbio.1000172).
71. Miaczynska, M. et al. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 116, 445-456 (2004).
72. Lin, D. C. et al. APPL1 associates with TrkA and GIPC1 and is required for nerve growth factor-mediated signal transduction. Mol. Cell. Biol. 26, 8928-8941 (2006).
73. Zoncu, R. et al. A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 136, 1110-1121 (2009).
74. Schenck, A. et al. The endosomal protein Appl1 mediates Akt substrate specificity and cell survival in vertebrate development. Cell 133, 486-497 (2008). The first in vivo evidence for the role of APPL proteins and endosomes in a specific Akt signalling pathway.
75. Varsano, T. et al. GIPC is recruited by APPL to peripheral TrkA endosomes and regulates TrkA trafficking and signaling. Mol. Cell. Biol. 26, 8942-8952 (2006).
76. Vaccari, T., Lu, H., Kanwar, R., Fortini, M. E. & Bilder, D. Endosomal entry regulates Notch receptor activation in Drosophila melanogaster. J. Cell Biol. 180, 755-762 (2008). This study provides evidence for the ubiquitylationdependent internalization of activated Notch, and shows the importance of this internalization for the γ-secretase-mediated cleavage of Notch.
77. Wilkin, M. et al. Drosophila HOPs and AP-3 complex genes are required for a Deltex-regulated activation of notch in the endosomal trafficking pathway. Dev. Cell 15, 762-772 (2008).
78. Pasternak, s. H. et al. Presenilin-1, nicastrin, amyloid precursor protein, and γ-secretase activity are co-localized in the lysosomal membrane. J. Biol. Chem. 278, 26687-26694 (2003).
79. schneider-Brachert, W. et al. Compartmentalization of TNF receptor 1 signaling: internalized TNF receptosomes as death signaling vesicles. Immunity 21, 415-428 (2004).
80. Liao, W. et al. CARP-2 is an endosome-associated ubiquitin ligase for RIP and regulates TNF-induced NF-κB activation. Curr. Biol. 18, 641-649 (2008).
81. Kagan, J. C. et al. TRAM couples endocytosis of Tolllike receptor 4 to the induction of interferon-β. Nature Immunol. 9, 361-368 (2008). The demonstration of the recruitment of specific signalling complexes to the activated Toll-like receptor, based on the change of the lipid composition of the membrane during endocytosis.
82. Honda, K. et al. spatiotemporal regulation of MyD88-IRF-7 signalling for robust type-I interferon induction. Nature 434, 1035-1040 (2005).
83. sorkin, A. & Goh, L. K. Endocytosis and intracellular trafficking of ErbBs. Exp. Cell Res. 315, 683-696 (2009).
84. Marchese, A., Paing, M. M., Temple, B. R. & Trejo, J. G protein-coupled receptor sorting to endosomes and lysosomes. Annu. Rev. Pharmacol. Toxicol. 48, 601-629 (2008).
85. Weber, U., Eroglu, C. & Mlodzik, M. Phospholipid membrane composition affects EGF receptor and Notch signaling through effects on endocytosis during Drosophila development. Dev. Cell 5, 559-570 (2003).
86. Huang, F., Kirkpatrick, D., Jiang, X., Gygi, s. & sorkin, A. Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol. Cell 21, 737-748 (2006).
87. Niendorf, s. et al. Essential role of ubiquitin-specific protease 8 for receptor tyrosine kinase stability and endocytic trafficking in vivo. Mol. Cell. Biol. 27, 5029-5039 (2007).
88. Row, P. E., Prior, I. A., McCullough, J., Clague, M. J. & Urbe, s. The ubiquitin isopeptidase UBPY regulates endosomal ubiquitin dynamics and is essential for receptor down-regulation. J. Biol. Chem. 281, 12618-12624 (2006).
89. Malerod, L., stuffers, s., Brech, A. & stenmark, H. Vps22/EAP30 in EsCRT-II mediates endosomal sorting of growth factor and chemokine receptors destined for lysosomal degradation. Traffic 8, 1617-1629 (2007).
90. Lloyd, T. E. et al. Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108, 261-269 (2002). This study shows in vivo that HRS and lysosomal sorting of RTKs have a role in the intensity of RTK signalling
91. Hammond, D. E. et al. Endosomal dynamics of Met determine signaling output. Mol. Biol. Cell 14, 1346-1354 (2003).
92. Wurdinger, T. et al. miR-296 regulates growth factor receptor overexpression in angiogenic endothelial cells. Cancer Cell 14, 382-393 (2008).
93. Bache, K. G. et al. The EsCRT-III subunit hVps24 is required for degradation but not silencing of the epidermal growth factor receptor. Mol. Biol. Cell 17, 2513-2523 (2006).
94. Pitcher, J. A., Payne, E. s., Csortos, C., DePaoli-Roach, A. A. & Lefkowitz, R. J. The G-protein-coupled receptor phosphatase: a protein phosphatase type 2A with a distinct subcellular distribution and substrate specificity. Proc. Natl Acad. Sci. USA 92, 8343-8347 (1995).
95. seachrist, J. L., Anborgh, P. H. & Ferguson, s. s. β2-adrenergic receptor internalization, endosomal sorting, and plasma membrane recycling are regulated by rab GTPases. J. Biol. Chem. 275, 27221-27228 (2000).
96. Filipeanu, C. M. et al. Enhancement of the recycling and activation of β-adrenergic receptor by Rab4 GTPase in cardiac myocytes. J. Biol. Chem. 281, 11097-11103 (2006).
97. Odley, A. et al. Regulation of cardiac contractility by Rab4-modulated β2-adrenergic receptor recycling. Proc. Natl Acad. Sci. USA 101, 7082-7087 (2004). This study provides evidence that RAB4-dependent recycling promotes GPCR signalling in vivo.
98. Padilla, B. E. et al. Endothelin-converting enzyme-1 regulates endosomal sorting of calcitonin receptor-like receptor and β-arrestins. J. Cell Biol. 179, 981-997 (2007).
99. Cattaruzza, F., Cottrell, G. s., Vaksman, N. & Bunnett, N. W. Endothelin-converting enzyme 1 promotes re-sensitization of neurokinin 1 receptordependent neurogenic inflammation. Br. J. Pharmacol. 156, 730-739 (2009).
100. Wang, Y., Lauffer, B., Von Zastrow, M., Kobilka, B. K. & Xiang, Y. N-ethylmaleimide-sensitive factor regulates β2 adrenoceptor trafficking and signaling in cardiomyocytes. Mol. Pharmacol. 72, 429-439 (2007).
101. French, A. R., Tadaki, D. K., Niyogi, s. K., & Lauffenburger, D. A. Intracellular trafficking of epidermal growth factor family ligands is directly influenced by the pH sensitivity of the receptor/ligand interaction. J. Biol. Chem. 270, 4334-4340 (1995).
102. Di Guglielmo, G. M., Le Roy., C., Goodfellow, A. F. & Wrana, J. L. Distinct endocytic pathways regulate TGF-β receptor signalling and turnover. Nature Cell Biol. 5, 410-421 (2003).
103. Connolly, J. L., Green, s. A. & Greene, L. A. Comparison of rapid changes in surface morphology and coated pit formation of PC12 cells in response to nerve growth factor, epidermal growth factor, and dibutyryl cyclic AMP. J. Cell Biol. 98, 457-465 (1984).
104. Wilde, A. et al. EGF receptor signaling stimulates sRC kinase phosphorylation of clathrin, influencing clathrin redistribution and EGF uptake. Cell 96, 1-20 (1999).
105. Beattie, E. C., Howe, C. L., Wilde, A., Brodsky, F. M. & Mobley, W. C. NGF signals through TrkA to increase clathrin at the plasma membrane and enhance clathrin-mediated membrane trafficking. J. Neurosci. 20, 7325-7333 (2000).
106. Johannessen, L. E., Pedersen, N. M., Pedersen, K. W., Madshus, I. H. & stang, E. Activation of the epidermal growth factor (EGF) receptor induces formation of EGF receptor- and grb2-containing clathrin-coated pits. Mol. Cell. Biol. 26, 389-401 (2006).
107. Hanover, J. A., Beguinot, L., Willingham, M. C. & Pastan, I. H. Transit of receptors for epidermal growth factor and transferrin through clathrin-coated pits. Analysis of the kinetics of receptor entry. J. Biol. Chem.260, 15938-15945 (1985).
108. Carpentier, J.-L. et al. Co-localization of 125I-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. 95, 73-77 (1982).
109. Keyel, P. A. et al. A single common portal for clathrinmediated endocytosis of distinct cargo governed by cargo-selective adaptors. Mol. Biol. Cell 17, 4300-4317 (2006).
110. Rappoport, J. Z. & simon, s. M. Endocytic trafficking of activated EGFR is AP-2 dependent and occurs through preformed clathrin spots. J. Cell Sci. 122, 1301-1305 (2009).
111. santini, F., Gaidarov, I. & Keen, J. H. G protein-coupled receptor/arrestin3 modulation of the endocytic machinery. J. Cell Biol. 156, 665-676 (2002). This study provides early evidence that activated GPCRs can change the properties of the clathrin-coated pits through which they are endocytosed.
112. Puthenveedu, M. A. & von Zastrow, M. Cargo regulates clathrin-coated pit dynamics. Cell 127, 113-124 (2006).
113. Bauerfeind, R., Takei, K. & De Camilli, P. Amphiphysin I is associated with coated endocytic intermediates and undergoes stimulation-dependent dephosphorylation in nerve terminals. J. Biol. Chem. 272, 30984-30992 (1997).
114. Marks, B. & McMahon, H. T. Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals. Curr. Biol. 8, 740-749 (1998).
115. Irie, F., Okuno, M., Pasquale, E. B. & Yamaguchi, Y. EphrinB-EphB signalling regulates clathrin-mediated endocytosis through tyrosine phosphorylation of synaptojanin 1. Nature Cell Biol. 7, 501-509 (2005).
116. Rink, J., Ghigo, E., Kalaidzidis, Y. & Zerial, M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 122, 735-749 (2005).
117. White, I. J., Bailey, L. M., Aghakhani, M. R., Moss, s. E. & Futter, C. E. EGF stimulates annexin 1-dependent inward vesiculation in a multivesicular endosome subpopulation. EMBO J. 25, 1-12 (2006).
118. Cavalli, V. et al. The stress-induced MAP kinase p38 regulates endocytic trafficking via the GDI:Rab5 complex. Mol. Cell 7, 421-432 (2001).
119. Zwang, Y. & Yarden, Y. p38 MAP kinase mediates stress-induced internalization of EGFR: implications for cancer chemotherapy. EMBO J. 25, 4195-4206 (2006).
120. Nekhoroshkova, E., Albert, s., Becker, M. & Rapp, U. R. A-RAF kinase functions in ARF6 regulated endocytic membrane traffic. PLoS ONE 4, e4647 (2009).
121. Yudowski, G. A., Puthenveedu, M. A., Henry, A. G. & von Zastrow, M. Cargo-mediated regulation of a rapid Rab4-dependent recycling pathway. Mol. Biol. Cell 20, 2774-2784 (2009).
122. Zweifel, L. s., Kuruvilla, R. & Ginty, D. D. Functions and mechanisms of retrograde neurotrophin signalling. Nature Rev. Neurosci. 6, 615-625 (2005).
123. Kessels, H. W. & Malinow, R. synaptic AMPA receptor plasticity and behavior. Neuron 61, 340-350 (2009).
124. Kim, J. A. et al. Morphine-induced receptor endocytosis in a novel knockin mouse reduces tolerance and dependence. Curr. Biol. 18, 129-135 (2008).
125. Mosesson, Y., Mills, G. B. & Yarden, Y. Derailed endocytosis: an emerging feature of cancer. Nature Rev. Cancer 8, 835-850 (2008).
126. Hershko, A. & Ciechanover, A. The ubiquitin system for protein degradation. Annu. Rev. Biochem. 61, 761-807 (1992).
127. Pickart, C. M. & Fushman, D. Polyubiquitin chains: polymeric protein signals. Curr. Opin. Chem. Biol. 8, 610-616 (2004).
128. staub, O. & Rotin, D. Role of ubiquitylation in cellular membrane transport. Physiol. Rev. 86, 669-707 (2006).
129. Hurley, J. H., Lee, s. & Prag, G. Ubiquitin-binding domains. Biochem. J. 399, 361-372 (2006).
130. Millard, s. M. & Wood, s. A. Riding the DUBway: regulation of protein trafficking by deubiquitylating enzymes. J. Cell Biol. 173, 463-468 (2006).
131. Carey, R. M., Balcz, B. A., Lopez-Coviella, I. & slack, B. E. Inhibition of dynamin-dependent endocytosis increases shedding of the amyloid precursor protein ectodomain and reduces generation of amyloid β protein. BMC Cell Biol. 6, 30 (2005).
132. Chyung, J. H., Raper, D. M. & selkoe, D. J. γ-secretase exists on the plasma membrane as an intact complex that accepts substrates and effects intramembrane cleavage. J. Biol. Chem. 280, 4383-4392 (2005).
133. Urra, M. s. et al. TrkA receptor activation by NGF induces shedding of the p75 neurotrophin receptor followed by endosomal γ-secretase-mediated release of the p75 intracellular domain. J. Biol. Chem. 282, 7606-7615 (2007).
134. Nichols, J. T., Miyamoto, A. & Weinmaster, G. Notch signaling - constantly on the move. Traffic 8, 959-969 (2007).
135. Pavlopoulos, E. et al. Neuralized encodes a peripheral membrane protein involved in delta signaling and endocytosis. Dev. Cell 1, 807-816 (2001).
136. Itoh, M. et al. Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev. Cell 4, 67-82 (2003).
137. Koo, B. K. et al. An obligatory role of mind bomb-1 in notch signaling of mammalian development. PLoS ONE 2, e1221 (2007).
138. Fehon, R. G. et al. Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila. Cell 61, 523-534 (1990).
139. Jekely, G. & Rorth, P. Hrs mediates downregulation of multiple signalling receptors in Drosophila. EMBO Rep. 4, 1163-1168 (2003).
140. Wilkin, M. B. et al. Regulation of notch endosomal sorting and signaling by Drosophila Nedd4 family proteins. Curr. Biol. 14, 2237-2244 (2004).
141. Chastagner, P., Israel, A. & Brou, C. AIP4/Itch regulates Notch receptor degradation in the absence of ligand. PLoS ONE 3, e2735 (2008).
142. Lefkowitz, R. J., Pitcher, J., Krueger, K. & Daaka, Y. Mechanisms of β-adrenergic receptor desensitization and resensitization. Adv. Pharmacol. 42, 416-420 (1998).
143. Waterman, H. et al. A mutant EGF-receptor defective in ubiquitylation and endocytosis unveils a role for Grb2 in negative signaling. EMBO J. 21, 303-313 (2002).
144. Rozakis-Adcock, M., Fernley, R., Wade, J., Pawson, T. & Bowtell, D. The sH2 and sH3 domains of mammalian Grb2 couple the EGF receptor to the Ras activator msos1. Nature 363, 83-85 (1993).
145. Loesch, M. & Chen, G. The p38 MAPK stress pathway as a tumor suppressor or more? Front. Biosci. 13, 3581-3593 (2008).
146. shih, s. C. et al. Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nature Cell Biol. 4, 389-393 (2002).
147. Aguilar, R. C. et al. Epsin N-terminal homology domains perform an essential function regulating Cdc42 through binding Cdc42 GTPase-activating proteins. Proc. Natl Acad. Sci. USA 103, 4116-4121 (2006).
148. Martin, N. P. et al. Intersectin regulates epidermal growth factor receptor endocytosis, ubiquitylation, and signaling. Mol. Pharmacol. 70, 1643-1653 (2006).
149. simpson, F. et al. sH3-domain-containing proteins function at distinct steps in clathrin-coated vesicle formation. Nature Cell Biol. 1, 119-124 (1999).
150. Hussain, N. K. et al. Endocytic protein intersectin-l regulates actin assembly via Cdc42 and N-WAsP. Nature Cell Biol. 3, 927-932 (2001).
151. schulte, G. & Bryja, V. The Frizzled family of unconventional G-protein-coupled receptors. Trends Pharmacol. Sci. 28, 518-525 (2007).