Advertisement

Interplay of Endocytosis and Growth Factor Receptor Signalling

  • Rachel Moore
  • Marta Giralt Pujol
  • Zhou Zhu
  • Elizabeth Smythe
Chapter
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 57)

Abstract

Growth factor receptors play a variety of roles during embryonic development and in adult homeostasis. These receptors are activated repeatedly in different cellular contexts and with different cellular outcomes. This begs the question as to how cells in a particular developmental, spatial and temporal context, or in adult tissue, interpret signalling by growth factor receptors in order to deliver qualitatively different signalling outputs. One mechanism by which this could occur is via endocytic regulation. The original paradigm for the role of endocytosis in growth factor receptor signalling was that receptor uptake has a quantitative role in signalling by reducing the number of cell surface receptors available for activation and targeting activated receptors for degradation. However, a range of studies over the last several years, in many different experimental systems, has demonstrated an additional qualitative role for endocytic trafficking in receptor signalling, with specific outcomes depending on the location of the signalling complex. Confinement of receptors within endosomes can spatially regulate signalling, facilitating specific protein interactions or post-translational modifications that alter throughout the trafficking process. Therefore, endocytosis does not simply regulate cell surface expression, but tightly controls protein interactions and function to produce distinct outcomes.

References

  1. Aguet F, Upadhyayula S, Gaudin R, Chou YY, Cocucci E, He K, Chen BC, Mosaliganti K, Pasham M, Skillern W, Legant WR, Liu TL, Findlay G, Marino E, Danuser G, Megason S, Betzig E, Kirchhausen T (2016) Membrane dynamics of dividing cells imaged by lattice light-sheet microscopy. Mol Biol Cell 27:3418–3435CrossRefPubMedPubMedCentralGoogle Scholar
  2. Antonny B, Burd C, De Camilli P, Chen E, Daumke O, Faelber K, Ford M, Frolov VA, Frost A, Hinshaw JE, Kirchhausen T, Kozlov MM, Lenz M, Low HH, Mcmahon H, Merrifield C, Pollard TD, Robinson PJ, Roux A, Schmid S (2016) Membrane fission by dynamin: what we know and what we need to know. EMBO J 35:2270–2284CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bahouth SW, Nooh MM (2017) Barcoding of GPCR trafficking and signaling through the various trafficking roadmaps by compartmentalized signaling networks. Cell Signal 36:42–55CrossRefPubMedPubMedCentralGoogle Scholar
  4. Balaji K, Colicelli J (2013) RIN1 regulates cell migration through Rab5 GTPases and ABL tyrosine kinases. Commun Integr Biol 6:e25421CrossRefPubMedPubMedCentralGoogle Scholar
  5. Basagiannis D, Zografou S, Murphy C, Fotsis T, Morbidelli L, Ziche M, Bleck C, Mercer J, Christoforidis S (2016) VEGF induces signalling and angiogenesis by directing VEGFR2 internalisation through macropinocytosis. J Cell Sci 129:4091–4104PubMedGoogle Scholar
  6. Behnia R, Munro S (2005) Organelle identity and the signposts for membrane traffic. Nature 438:597–604CrossRefPubMedGoogle Scholar
  7. Blouin CM, Hamon Y, Gonnord P, Boularan C, Kagan J, Viaris de Lesegno C, Ruez R, Mailfert S, Bertaux N, Loew D, Wunder C, Johannes L, Vogt G, Contreras FX, Marguet D, Casanova JL, Gales C, He HT, Lamaze C (2016) Glycosylation-dependent IFN-gammaR partitioning in lipid and actin nanodomains is critical for JAK activation. Cell 166:920–934CrossRefPubMedGoogle Scholar
  8. Blume-Jensen P, Hunter T (2001) Oncogenic kinase signalling. Nature 411:355–365CrossRefPubMedGoogle Scholar
  9. Blumer J, Rey J, Dehmelt L, Mazel T, Wu YW, Bastiaens P, Goody RS, Itzen A (2013) RabGEFs are a major determinant for specific Rab membrane targeting. J Cell Biol 200:287–300CrossRefPubMedPubMedCentralGoogle Scholar
  10. Boucrot E, Ferreira AP, Almeida-Souza L, Debard S, Vallis Y, Howard G, Bertot L, Sauvonnet N, Mcmahon HT (2015) Endophilin marks and controls a clathrin-independent endocytic pathway. Nature 517:460–465CrossRefGoogle Scholar
  11. Brankatschk B, Wichert SP, Johnson SD, Schaad O, Rossner MJ, Gruenberg J (2012) Regulation of the EGF transcriptional response by endocytic sorting. Sci Signal 5:ra21Google Scholar
  12. Brodsky FM (2012) Diversity of clathrin function: new tricks for an old protein. Annu Rev Cell Dev Biol 28:309–336CrossRefPubMedGoogle Scholar
  13. Buckley CM, King JS (2017) Drinking problems: Mechanisms of macropinosome formation and maturation. FEBS JGoogle Scholar
  14. Caldieri G, Barbieri E, Nappo G, Raimondi A, Bonora M, Conte A, Verhoef L, Confalonieri S, Malabarba MG, Bianchi F, Cuomo A, Bonaldi T, Martini E, Mazza D, Pinton P, Tacchetti C, Polo S, Di Fiore PP, Sigismund S (2017) Reticulon 3-dependent ER-PM contact sites control EGFR nonclathrin endocytosis. Science 356:617–624CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cauvin C, Rosendale M, Gupta-Rossi N, Rocancourt M, Larraufie P, Salomon R, Perrais D, Echard A (2016) Rab35 GTPase triggers switch-like recruitment of the lowe syndrome lipid phosphatase OCRL on newborn endosomes. Curr Biol 26:120–128CrossRefPubMedGoogle Scholar
  16. Cavalli V, Vilbois F, Corti M, Marcote MJ, Tamura K, Karin M, Arkinstall S, Gruenberg J (2001) The stress-induced MAP kinase p38 regulates endocytic trafficking via the GDI:Rab5 complex. Mol Cell 7:421–432CrossRefPubMedGoogle Scholar
  17. Chen PH, Bendris N, Hsiao YJ, Reis CR, Mettlen M, Chen HY, Yu SL, Schmid SL (2017) Crosstalk between CLCb/Dyn1-mediated adaptive Clathrin-mediated endocytosis and epidermal growth factor receptor signaling increases metastasis. Dev Cell 40(278–288):e5Google Scholar
  18. Christoforidis S, Mcbride HM, Burgoyne RD, Zerial M (1999) The Rab5 effector EEA1 is a core component of endosome docking. Nature 397:621–625CrossRefPubMedGoogle Scholar
  19. Corallino S, Malabarba MG, Zobel M, Di Fiore PP, Scita G (2015) Epithelial-to-Mesenchymal plasticity harnesses endocytic circuitries. Front Oncol 5:45CrossRefPubMedPubMedCentralGoogle Scholar
  20. Cullen PJ, Korswagen HC (2011) Sorting nexins provide diversity for retromer-dependent trafficking events. Nat Cell Biol 14:29–37CrossRefPubMedPubMedCentralGoogle Scholar
  21. D’Souza RC, Knittle AM, Nagaraj N, Van Dinther M, Choudhary C, Ten Dijke P, Mann M, Sharma K (2014) Time-resolved dissection of early phosphoproteome and ensuing proteome changes in response to TGF-beta. Sci Signal 7:rs5Google Scholar
  22. Danson C, Brown E, Hemmings OJ, Mcgough IJ, Yarwood S, Heesom KJ, Carlton JG, Martin-Serrano J, May MT, Verkade P, Cullen PJ (2013) SNX15 links clathrin endocytosis to the PtdIns3P early endosome independently of the APPL1 endosome. J Cell Sci 126:4885–4899CrossRefPubMedPubMedCentralGoogle Scholar
  23. Davidson EH (1993) Later embryogenesis: regulatory circuitry in morphogenetic fields. Development 118:665–690PubMedGoogle Scholar
  24. De Renzis S, Sonnichsen B, Zerial M (2002) Divalent Rab effectors regulate the sub-compartmental organization and sorting of early endosomes. Nat Cell Biol 14:14Google Scholar
  25. Del Conte-Zerial P, Brusch L, Rink JC, Collinet C, Kalaidzidis Y, Zerial M, Deutsch A (2008) Membrane identity and GTPase cascades regulated by toggle and cut-out switches. Mol Syst Biol 4:206PubMedPubMedCentralGoogle Scholar
  26. Di Guglielmo GM, Baass PC, Ou WJ, Posner BI, Bergeron JJ (1994) Compartmentalization of SHC, GRB2 and mSOS, and hyperphosphorylation of Raf-1 by EGF but not insulin in liver parenchyma. EMBO J 13:4269–4277PubMedPubMedCentralCrossRefGoogle Scholar
  27. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL (2003) Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 5:410–421CrossRefPubMedGoogle Scholar
  28. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651–657CrossRefPubMedGoogle Scholar
  29. Donaldson JG, Johnson DL, Dutta D (2016) Rab and Arf G proteins in endosomal trafficking and cell surface homeostasis. Small GTPases 7:247–251CrossRefPubMedPubMedCentralGoogle Scholar
  30. Doyotte A, Russell MR, Hopkins CR, Woodman PG (2005) Depletion of TSG101 forms a mammalian “Class E” compartment: a multicisternal early endosome with multiple sorting defects. J Cell Sci 118:3003–3017CrossRefPubMedGoogle Scholar
  31. Doyotte A, Mironov A, Mckenzie E, Woodman P (2008) The Bro1-related protein HD-PTP/PTPN23 is required for endosomal cargo sorting and multivesicular body morphogenesis. Proc Natl Acad Sci U S A 105:6308–6313CrossRefPubMedPubMedCentralGoogle Scholar
  32. Elfenbein A, Lanahan A, Zhou TX, Yamasaki A, Tkachenko E, Matsuda M, Simons M (2012) Syndecan 4 regulates FGFR1 signaling in endothelial cells by directing macropinocytosis. Sci Signal 5:ra36Google Scholar
  33. Er EE, Mendoza MC, Mackey AM, Rameh LE, Blenis J (2013) AKT facilitates EGFR trafficking and degradation by phosphorylating and activating PIKfyve. Sci Signal 6:ra45Google Scholar
  34. Flores-Rodriguez N, Kenwright DA, Chung PH, Harrison AW, Stefani F, Waigh TA, Allan VJ, Woodman PG (2015) ESCRT-0 marks an APPL1-independent transit route for EGFR between the cell surface and the EEA1-positive early endosome. J Cell Sci 128:755–767CrossRefPubMedPubMedCentralGoogle Scholar
  35. Fortian A, Dionne LK, Hong SH, Kim W, Gygi SP, Watkins SC, Sorkin A (2015) Endocytosis of ubiquitylation-deficient EGFR mutants via Clathrin-coated pits is mediated by ubiquitylation. Traffic 16:1137–1154CrossRefPubMedPubMedCentralGoogle Scholar
  36. Foti M, Moukil MA, Dudognon P, Carpentier JL (2004) Insulin and IGF-1 receptor trafficking and signalling. Novartis Found Symp 262:125–141; discussion 141–147, 265–268Google Scholar
  37. Francavilla C, Papetti M, Rigbolt KT, Pedersen AK, Sigurdsson JO, Cazzamali G, Karemore G, Blagoev B, Olsen JV (2016) Multilayered proteomics reveals molecular switches dictating ligand-dependent EGFR trafficking. Nat Struct Mol Biol 23:608–618CrossRefPubMedGoogle Scholar
  38. French AR, Sudlow GP, Wiley HS, Lauffenburger DA (1994) Postendocytic trafficking of epidermal growth factor-receptor complexes is mediated through saturable and specific endosomal interactions. J Biol Chem 269:15749–15755PubMedGoogle Scholar
  39. Goh LK, Sorkin A (2013) Endocytosis of receptor tyrosine kinases. Cold Spring Harb Perspect Biol 5:a017459CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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 189:871–883CrossRefPubMedPubMedCentralGoogle Scholar
  41. Grecco HE, Schmick M, Bastiaens PI (2011) Signaling from the living plasma membrane. Cell 144:897–909CrossRefPubMedGoogle Scholar
  42. Haas AK, Fuchs E, Kopajtich R, Barr FA (2005) A GTPase-activating protein controls Rab5 function in endocytic trafficking. Nat Cell Biol 7:887–893CrossRefPubMedGoogle Scholar
  43. Hommelgaard AM, Lerdrup M, Van Deurs B (2004) Association with membrane protrusions makes ErbB2 an internalization-resistant receptor. Mol Biol Cell 15:1557–1567CrossRefPubMedPubMedCentralGoogle Scholar
  44. Horiuchi H, Lippe R, Mcbride HM, Rubino M, Woodman P, Stenmark H, Rybin V, Wilm M, Ashman K, Mann M, Zerial M (1997) A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell 90:1149–1159CrossRefPubMedGoogle Scholar
  45. Hurley JH, Emr SD (2006) The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu Rev Biophys Biomol Struct 35:277–298CrossRefPubMedPubMedCentralGoogle Scholar
  46. Kalaidzidis I, Miaczynska M, Brewinska-Olchowik M, Hupalowska A, Ferguson C, Parton RG, Kalaidzidis Y, Zerial M (2015) APPL endosomes are not obligatory endocytic intermediates but act as stable cargo-sorting compartments. J Cell Biol 211:123–144CrossRefPubMedPubMedCentralGoogle Scholar
  47. Kalin S, Hirschmann DT, Buser DP, Spiess M (2015) Rabaptin5 is recruited to endosomes by Rab4 and Rabex5 to regulate endosome maturation. J Cell Sci 128:4126–4137CrossRefPubMedGoogle Scholar
  48. Kermorgant S, Parker PJ (2008) Receptor trafficking controls weak signal delivery: a strategy used by c-Met for STAT3 nuclear accumulation. J Cell Biol 182:855–863CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kholodenko BN (2003) Four-dimensional organization of protein kinase signaling cascades: the roles of diffusion, endocytosis and molecular motors. J Exp Biol 206:2073–2082CrossRefPubMedGoogle Scholar
  50. Kholodenko BN, Birtwistle MR (2009) Four-dimensional dynamics of MAPK information processing systems. Wiley Interdiscip Rev Syst Biol Med 1:28–44CrossRefPubMedPubMedCentralGoogle Scholar
  51. Kong C, Su X, Chen PI, Stahl PD (2007) Rin1 interacts with signal-transducing adaptor molecule (STAM) and mediates epidermal growth factor receptor trafficking and degradation. J Biol Chem 282:15294–15301CrossRefPubMedGoogle Scholar
  52. Lemmon MA, Schlessinger J (2010) Cell signaling by receptor tyrosine kinases. Cell 141:1117–1134CrossRefPubMedPubMedCentralGoogle Scholar
  53. Li D, Shao L, Chen BC, Zhang X, Zhang M, Moses B, Milkie DE, Beach JR, Hammer JA, Pasham M, Kirchhausen T, Baird MA, Davidson MW, Xu P, Betzig E (2015) Advanced imaging. Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics. Science 349:aab3500Google Scholar
  54. Liu K, Xing R, Jian Y, Gao Z, Ma X, Sun X, Li Y, Xu M, Wang X, Jing Y, Guo W, Yang C (2017) WDR91 is a Rab7 effector required for neuronal development. J Cell Biol 216:3307–3321CrossRefPubMedPubMedCentralGoogle Scholar
  55. Lloyd TE, Atkinson R, Wu MN, Zhou Y, Pennetta G, Bellen HJ (2002) Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108:261–269CrossRefPubMedGoogle Scholar
  56. Lu H, Bilder D (2005) Endocytic control of epithelial polarity and proliferation in Drosophila. Nat Cell Biol 7:1232–1239CrossRefPubMedGoogle Scholar
  57. Mace G, Miaczynska M, Zerial M, Nebreda AR (2005) Phosphorylation of EEA1 by p38 MAP kinase regulates mu opioid receptor endocytosis. EMBO J 24:3235–3246CrossRefPubMedPubMedCentralGoogle Scholar
  58. Maib H, Smythe E, Ayscough K (2017) Forty years on: clathrin-coated pits continue to fascinate. Mol Biol Cell 28:843–847CrossRefPubMedPubMedCentralGoogle Scholar
  59. Malerod L, Stuffers S, Brech A, Stenmark H (2007) Vps22/EAP30 in ESCRT-II mediates endosomal sorting of growth factor and chemokine receptors destined for lysosomal degradation. Traffic 8:1617–1629Google Scholar
  60. Mattissek C, Teis D (2014) The role of the endosomal sorting complexes required for transport (ESCRT) in tumorigenesis. Mol Membr Biol 31:111–119CrossRefPubMedPubMedCentralGoogle Scholar
  61. Mayor S, Riezman H (2004) Sorting GPI-anchored proteins. Nat Rev Mol Cell Biol 5:110–120CrossRefPubMedGoogle Scholar
  62. Mayor S, Parton RG, Donaldson JG (2014) Clathrin-independent pathways of endocytosis. Cold Spring Harb Perspect Biol 6Google Scholar
  63. Mcclintock JL, Ceresa BP (2010) Transforming growth factor-{alpha} enhances corneal epithelial cell migration by promoting EGFR recycling. Invest Ophthalmol Vis Sci 51:3455–3461CrossRefPubMedPubMedCentralGoogle Scholar
  64. Menard L, Parker PJ, Kermorgant S (2014) Receptor tyrosine kinase c-Met controls the cytoskeleton from different endosomes via different pathways. Nat Commun 5:3907CrossRefPubMedGoogle Scholar
  65. Miaczynska M, Christoforidis S, Giner A, Shevchenko A, Uttenweiler-Joseph S, Habermann B, Wilm M, Parton RG, Zerial M (2004) APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 116:445–456CrossRefPubMedGoogle Scholar
  66. Mineo C, Gill GN, Anderson RG (1999) Regulated migration of epidermal growth factor receptor from caveolae. J Biol Chem 274:30636–30643CrossRefPubMedGoogle Scholar
  67. Montagnac G, De Forges H, Smythe E, Gueudry C, Romao M, Salamero J, Chavrier P (2011) Decoupling of activation and effector binding underlies ARF6 priming of fast endocytic recycling. Curr Biol 21:574–579CrossRefPubMedGoogle Scholar
  68. Nada S, Hondo A, Kasai A, Koike M, Saito K, Uchiyama Y, Okada M (2009) The novel lipid raft adaptor p18 controls endosome dynamics by anchoring the MEK-ERK pathway to late endosomes. EMBO J 28:477–489CrossRefPubMedPubMedCentralGoogle Scholar
  69. Norris A, Tammineni P, Wang S, Gerdes J, Murr A, Kwan KY, Cai Q, Grant BD (2017) SNX-1 and RME-8 oppose the assembly of HGRS-1/ESCRT-0 degradative microdomains on endosomes. Proc Natl Acad Sci U S A 114:E307–E316CrossRefPubMedPubMedCentralGoogle Scholar
  70. Parachoniak CA, Luo Y, Abella JV, Keen JH, Park M (2011) GGA3 functions as a switch to promote Met receptor recycling, essential for sustained ERK and cell migration. Dev Cell 20:751–763CrossRefPubMedPubMedCentralGoogle Scholar
  71. Pfeffer SR (2017) Rab GTPases: master regulators that establish the secretory and endocytic pathways. Mol Biol Cell 28:712–715CrossRefPubMedPubMedCentralGoogle Scholar
  72. Pinilla-Macua I, Watkins SC, Sorkin A (2016) Endocytosis separates EGF receptors from endogenous fluorescently labeled HRas and diminishes receptor signaling to MAP kinases in endosomes. Proc Natl Acad Sci U S A 113:2122–2127CrossRefPubMedPubMedCentralGoogle Scholar
  73. Raiborg C, Bache KG, Gillooly DJ, Madshus IH, Stang E, Stenmark H (2002) Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat Cell Biol 4:394–398CrossRefPubMedGoogle Scholar
  74. Reis CR, Chen PH, Srinivasan S, Aguet F, Mettlen M, Schmid SL (2015) Crosstalk between Akt/GSK3beta signaling and dynamin-1 regulates clathrin-mediated endocytosis. EMBO J 34:2132–2146CrossRefPubMedPubMedCentralGoogle Scholar
  75. Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122:735–749CrossRefPubMedGoogle Scholar
  76. Robinson MS (2015) Forty Years of Clathrin-coated Vesicles. Traffic 16:1210–1238CrossRefPubMedGoogle Scholar
  77. Runyan CE, Schnaper HW, Poncelet AC (2005) The role of internalization in transforming growth factor beta1-induced Smad2 association with Smad anchor for receptor activation (SARA) and Smad2-dependent signaling in human mesangial cells. J Biol Chem 280:8300–8308CrossRefPubMedGoogle Scholar
  78. Schenck A, Goto-Silva L, Collinet C, Rhinn M, Giner A, Habermann B, Brand M, Zerial M (2008) The endosomal protein Appl1 mediates Akt substrate specificity and cell survival in vertebrate development. Cell 133:486–497CrossRefPubMedGoogle Scholar
  79. Schiefermeier N, Scheffler JM, De Araujo ME, Stasyk T, Yordanov T, Ebner HL, Offterdinger M, Munck S, Hess MW, Wickstrom SA, Lange A, Wunderlich W, Fassler R, Teis D, Huber LA (2014) The late endosomal p14-MP1 (LAMTOR2/3) complex regulates focal adhesion dynamics during cell migration. J Cell Biol 205:525–540CrossRefPubMedPubMedCentralGoogle Scholar
  80. Schmid SL, Sorkin A, Zerial M (2014) Endocytosis: past, present, and future. Cold Spring Harb Perspect Biol 6:a022509CrossRefPubMedPubMedCentralGoogle Scholar
  81. Schmidt O, Teis D (2012) The ESCRT machinery. Curr Biol 22:R116–R120CrossRefPubMedPubMedCentralGoogle Scholar
  82. Schmierer B, Hill CS (2007) TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility. Nat Rev Mol Cell Biol 8:970–982CrossRefPubMedGoogle Scholar
  83. Schoneberg J, Lee IH, Iwasa JH, Hurley JH (2017) Reverse-topology membrane scission by the ESCRT proteins. Nat Rev Mol Cell Biol 18:5–17CrossRefPubMedGoogle Scholar
  84. Semerdjieva S, Shortt B, Maxwell E, Singh S, Fonarev P, Hansen J, Schiavo G, Grant BD, Smythe E (2008) Co-ordinated regulation of AP2 uncoating from clathrin coated vesicles by Rab5 and hRME-6. J Cell Biol 183:499–511CrossRefPubMedPubMedCentralGoogle Scholar
  85. Shin HW, Hayashi M, Christoforidis S, Lacas-Gervais S, Hoepfner S, Wenk MR, Modregger J, Uttenweiler-Joseph S, Wilm M, Nystuen A, Frankel WN, Solimena M, De Camilli P, Zerial M (2005) An enzymatic cascade of Rab5 effectors regulates phosphoinositide turnover in the endocytic pathway. J Cell Biol 170:607–618CrossRefPubMedPubMedCentralGoogle Scholar
  86. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, Transidico P, Di Fiore PP, Polo S (2005) Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci U S A 102:2760–2765CrossRefPubMedPubMedCentralGoogle Scholar
  87. Sigismund S, Argenzio E, Tosoni D, Cavallaro E, Polo S, Di Fiore PP (2008) Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev Cell 15:209–219CrossRefPubMedGoogle Scholar
  88. Sigismund S, Algisi V, Nappo G, Conte A, Pascolutti R, Cuomo A, Bonaldi T, Argenzio E, Verhoef LG, Maspero E, Bianchi F, Capuani F, Ciliberto A, Polo S, Di Fiore PP (2013) Threshold-controlled ubiquitination of the EGFR directs receptor fate. EMBO J 32:2140–2157CrossRefPubMedPubMedCentralGoogle Scholar
  89. Simonsen A, Lippe R, Christoforidis S, Gaullier JM, Brech A, Callaghan J, Toh BH, Murphy C, Zerial M, Stenmark H (1998) EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394:494–498CrossRefPubMedGoogle Scholar
  90. Sorkin A, von Zastrow M (2009) Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 10:609–622CrossRefPubMedPubMedCentralGoogle Scholar
  91. Sousa LP, Lax I, Shen H, Ferguson SM, De Camilli P, Schlessinger J (2012) Suppression of EGFR endocytosis by dynamin depletion reveals that EGFR signaling occurs primarily at the plasma membrane. Proc Natl Acad Sci U S A 109:4419–4424CrossRefPubMedPubMedCentralGoogle Scholar
  92. Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10:513–525CrossRefPubMedGoogle Scholar
  93. Su X, Kong C, Stahl PD (2007) GAPex-5 mediates ubiquitination, trafficking, and degradation of epidermal growth factor receptor. J Biol Chem 282:21278–21284CrossRefPubMedGoogle Scholar
  94. Tall GG, Barbieri MA, Stahl PD, Horazdovsky BF (2001) Ras-activated endocytosis is mediated by the Rab5 guanine nucleotide exchange activity of RIN1. Dev Cell 1:73–82CrossRefPubMedGoogle Scholar
  95. Teis D, Wunderlich W, Huber LA (2002) Localization of the MP1-MAPK scaffold complex to endosomes is mediated by p14 and required for signal transduction. Dev Cell 3:803–814CrossRefPubMedGoogle Scholar
  96. Teis D, Taub N, Kurzbauer R, Hilber D, De Araujo ME, Erlacher M, Offterdinger M, Villunger A, Geley S, Bohn G, Klein C, Hess MW, Huber LA (2006) p14-MP1-MEK1 signaling regulates endosomal traffic and cellular proliferation during tissue homeostasis. J Cell Biol 175:861–868CrossRefPubMedPubMedCentralGoogle Scholar
  97. Tomas A, Vaughan SO, Burgoyne T, Sorkin A, Hartley JA, Hochhauser D, Futter CE (2015) WASH and Tsg101/ALIX-dependent diversion of stress-internalized EGFR from the canonical endocytic pathway. Nat Commun 6:7324CrossRefPubMedPubMedCentralGoogle Scholar
  98. Traub LM, Bonifacino JS (2013) Cargo Recognition in Clathrin-Mediated Endocytosis. Cold Spring Harb Perspect Biol 5Google Scholar
  99. Tsukazaki T, Chiang TA, Davison AF, Attisano L, Wrana JL (1998) SARA, a FYVE domain protein that recruits Smad2 to the TGFbeta receptor. Cell 95:779–791CrossRefPubMedGoogle Scholar
  100. Vaccari T, Bilder D (2005) The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev Cell 9:687–698CrossRefPubMedGoogle Scholar
  101. Vieira AV, Lamaze C, Schmid SL (1996) Control of egf receptor signaling by clathrin-mediated endocytosis. Science 274:2086–2089CrossRefPubMedGoogle Scholar
  102. Villasenor R, Nonaka H, Del Conte-Zerial P, Kalaidzidis Y, Zerial M (2015) Regulation of EGFR signal transduction by analogue-to-digital conversion in endosomes. Elife 4Google Scholar
  103. Villasenor R, Kalaidzidis Y, Zerial M (2016) Signal processing by the endosomal system. Curr Opin Cell Biol 39:53–60CrossRefPubMedGoogle Scholar
  104. Vogel GF, Ebner HL, De Araujo ME, Schmiedinger T, Eiter O, Pircher H, Gutleben K, Witting B, Teis D, Huber LA, Hess MW (2015) Ultrastructural morphometry points to a new role for LAMTOR2 in regulating the Endo/Lysosomal system. Traffic 16:617–634CrossRefPubMedGoogle Scholar
  105. Wandinger-Ness A, Zerial M (2014) Rab proteins and the compartmentalization of the endosomal system. Cold Spring Harb Perspect Biol 6:a022616CrossRefPubMedPubMedCentralGoogle Scholar
  106. Yan H, Jahanshahi M, Horvath EA, Liu HY, Pfleger CM (2010) Rabex-5 ubiquitin ligase activity restricts Ras signaling to establish pathway homeostasis in Drosophila. Curr Biol 20:1378–1382CrossRefPubMedPubMedCentralGoogle Scholar
  107. Zeigerer A, Wuttke A, Marsico G, Seifert S, Kalaidzidis Y, Zerial M (2017) Functional properties of hepatocytes in vitro are correlated with cell polarity maintenance. Exp Cell Res 350:242–252CrossRefPubMedGoogle Scholar
  108. Zhang YS, Aleman J, Shin SR, Kilic T, Kim D, Mousavi Shaegh SA, Massa S, Riahi R, Chae S, Hu N, Avci H, Zhang W, Silvestri A, Sanati Nezhad A, Manbohi A, De Ferrari F, Polini A, Calzone G, Shaikh N, Alerasool P, Budina E, Kang J, Bhise N, Ribas J, Pourmand A, Skardal A, Shupe T, Bishop CE, Dokmeci MR, Atala A, Khademhosseini A (2017) Multisensor-integrated organs-on-chips platform for automated and continual in situ monitoring of organoid behaviors. Proc Natl Acad Sci U S A 114:E2293–E2302CrossRefPubMedPubMedCentralGoogle Scholar
  109. Zoncu R, Perera RM, Balkin DM, Pirruccello M, Toomre D, De Camilli P (2009) A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 136:1110–1121CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Rachel Moore
    • 1
  • Marta Giralt Pujol
    • 1
  • Zhou Zhu
    • 1
  • Elizabeth Smythe
    • 1
  1. 1.Department of Biomedical Science, Centre for Membrane Interactions and DynamicsUniversity of SheffieldSheffieldUK

Personalised recommendations