Progress in Molecular and Subcellular Biology Editors Christophe Lamaze · Ian Prior Endocytosis and Signaling Progress in Molecular and Subcellular Biology Volume 57 Editor-in-chief Werner E. G. Müller, Mainz, Germany Series editors Heinz C. Schröder, Mainz, Germany Ðurðica Ugarković, Zagreb, Croatia This series gives an insight into the most current, cutting edge topics in molecular biology, including applications in biotechnology and molecular medicine. In the recent years, the progress of research in the frontier area of molecular and cell biology has resulted in an overwhelming amount of data on the structural components and molecular machineries of the cell and its organelles and the complexity of intra- and intercellular communication. The molecular basis of hereditary and acquired diseases is beginning to be unravelled, and profound new insights into development and evolutionary biology, as well as the genetically driven formation of 3D biological architectures, have been gained from molecular approaches. Topical volumes, written and edited by acknowledged experts in the field, present the most recent findings and their implications for future research. This series is indexed in PubMed. More information about this series at http://www.springer.com/series/388 Christophe Lamaze Ian Prior (cid:129) Editors Endocytosis and Signaling 123 Editors Christophe Lamaze IanPrior MembraneDynamics andMechanicsof Department ofCellular andMolecular Intracellular SignalingLaboratory, Physiology,Institute of Translational CNRSUMR3666, INSERMU1143, Medicine Institut Curie—Centre deRecherche University of Liverpool PSLResearch University Liverpool, UK Paris, France ISSN 0079-6484 ISSN 2197-8484 (electronic) Progressin Molecular andSubcellular Biology ISBN978-3-319-96703-5 ISBN978-3-319-96704-2 (eBook) https://doi.org/10.1007/978-3-319-96704-2 LibraryofCongressControlNumber:2018948712 ©SpringerInternationalPublishingAG,partofSpringerNature2018 Thisworkissubjecttocopyright.AllrightsarereservedbythePublisher,whetherthewholeorpart of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission orinformationstorageandretrieval,electronicadaptation,computersoftware,orbysimilarordissimilar methodologynowknownorhereafterdeveloped. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publicationdoesnotimply,evenintheabsenceofaspecificstatement,thatsuchnamesareexemptfrom therelevantprotectivelawsandregulationsandthereforefreeforgeneraluse. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authorsortheeditorsgiveawarranty,expressorimplied,withrespecttothematerialcontainedhereinor for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictionalclaimsinpublishedmapsandinstitutionalaffiliations. ThisSpringerimprintispublishedbytheregisteredcompanySpringerNatureSwitzerlandAG Theregisteredcompanyaddressis:Gewerbestrasse11,6330Cham,Switzerland Preface It is now widely appreciated that cell signalling is highly context dependent. The location and concentration of signalling nodes regulate their activation cycles and engagement with distinct effector pathways. Whilst many cell signalling pathways are initiated from the cell surface, endocytosis provides an opportunity for modu- lation oftheoutputofsignalling networks.Inthisbook,wewillhighlighthowthe endosomalsystemhelpstoorganiseandregulatesignallingpathways.Inaseriesof reviews,wewillfirstlyfocusontheendocyticandendosomalsystemanddescribe how these subcellular platforms sort and regulate a wide range of signalling pathway components and phenotypic outputs. We will then review the latest sci- entific insights into how endocytic trafficking and subcellular location modulate a set of major pathways essential for normal cellular function and organism development. Paris, France Christophe Lamaze Liverpool, UK Ian Prior v Contents 1 The Endosomal Network: Mediators and Regulators of Endosome Maturation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 Maria Podinovskaia and Anne Spang 2 Integration of the Endocytic System into the Network of Cellular Functions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39 Noga Budick-Harmelin and Marta Miaczynska 3 GTPases Rac1 and Ras Signaling from Endosomes . . . . . . . . . . . . 65 Francesc Tebar, Carlos Enrich, Carles Rentero and Thomas Grewal 4 ESCRT and Membrane Protein Ubiquitination . . . . . . . . . . . . . . . 107 Simona M. Migliano and David Teis 5 Retromer and Its Role in Regulating Signaling at Endosomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137 Matthew N. J. Seaman 6 The Lysosome and Intracellular Signalling. . . . . . . . . . . . . . . . . . . 151 Geoffrey G. Hesketh, Lena Wartosch, Luther J. Davis, Nicholas A. Bright and J. Paul Luzio 7 Interplay of Endocytosis and Growth Factor Receptor Signalling. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 181 Rachel Moore, Marta Giralt Pujol, Zhou Zhu and Elizabeth Smythe 8 Role of the Endocytosis of Caveolae in Intracellular Signaling and Metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 203 Olivia Muriel, Miguel Sánchez-Álvarez, Raffaele Strippoli and Miguel Angel del Pozo 9 EGFR Trafficking in Physiology and Cancer . . . . . . . . . . . . . . . . . 235 Giusi Caldieri, Maria Grazia Malabarba, Pier Paolo Di Fiore and Sara Sigismund vii viii Contents 10 Evolving View of Membrane Trafficking and Signaling Systems for G Protein-Coupled Receptors . . . . . . . . . . . . . . . . . . . . . . . . . . 273 Silvia Sposini and Aylin C. Hanyaloglu 11 Endosomal Trafficking During Mitosis and Notch-Dependent Asymmetric Division. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 301 Alicia Daeden and Marcos Gonzalez-Gaitan Chapter 1 The Endosomal Network: Mediators and Regulators of Endosome Maturation MariaPodinovskaiaandAnneSpang Contents 1.1 EndosomeMaturationOverview .............................................. 2 1.2 EndosomeFunctions ....................................................... 5 1.3 MediatorsofEndosomeMaturation ........................................... 7 1.3.1 Phosphoinositides ................................................... 7 1.3.2 RabGTPases ....................................................... 8 1.3.3 Tethers ............................................................. 9 1.3.4 ESCRTs ............................................................ 10 1.3.5 V-ATPase .......................................................... 10 1.3.6 AdditionalMediatorsofVacuolarpH ................................... 11 1.3.7 Cytoskeleton ........................................................ 12 1.4 CoordinationofEndosomeMaturation ........................................ 13 1.4.1 SortingCompartments ................................................ 14 1.4.2 RabConversion ..................................................... 15 1.4.3 Rab5Regulation ..................................................... 16 1.4.4 Rab7Regulation ..................................................... 16 1.4.5 PIPConversion ...................................................... 17 1.4.6 PIPRegulation ...................................................... 17 1.4.7 V-ATPaseRegulation ................................................. 18 1.5 ContributionsofOtherOrganellestoEndosomeMaturation ....................... 20 1.5.1 ER ................................................................ 20 1.5.2 LipidDroplets ...................................................... 21 1.5.3 CrosstalkwiththeAutophagyPathway ................................. 22 1.6 PerturbationsofEndosomeMaturationinDisease ............................... 22 1.7 Conclusions ............................................................... 24 References ..................................................................... 24 Abstract Endocytosisisameansforthecelltosampleitsenvironmentfornutrients and regulate plasma membrane (PM) composition and area. Whereas the majority ofinternalizedcargoisrecycledbacktothecellsurface,selectmaterialissenttothe B M.Podinovskaia·A.Spang( ) Biozentrum,UniversityofBasel,Klingelbergstrasse70,4056Basel,Switzerland e-mail:[email protected] M.Podinovskaia e-mail:[email protected] ©SpringerInternationalPublishingAG,partofSpringerNature2018 1 C.LamazeandI.Prior(eds.),EndocytosisandSignaling,ProgressinMolecular andSubcellularBiology57,https://doi.org/10.1007/978-3-319-96704-2_1 2 M.PodinovskaiaandA.Spang lysosomefordegradation.Endosomesfurtherplaymajorrolesincentralcellactiv- ities as diverse as establishment of cell polarity and signaling, lysosomal storage andimmunity.Thecomplexityofendosomalfunctionsisreflectedbytheextensive changestoendosomepropertiesastheymature.Theidentityofindividualendosomes isinfluencedbythepresenceofspecificRabGTPasesandphosphoinositides(PIPs), whichcoordinatemembranetrafficandfacilitateendosomalfunctions.Motorsand tethersdirecttheendosomestotherequiredlocationsandmoderatefusionwithother organelles.Themaintenanceoftheelaborateendosomalnetworkissupportedbythe ERandthetrans-Golginetwork(TGN),whichpromotetheexchangeofmembrane components, provide enzymes, and assist with signaling. Additionally, V-ATPase is emerging as an underappreciated coordinator of endosome maturation and cell signaling. The inputs of the various mediators of endosome maturation are tightly regulated and coordinated to ensure appropriate maintenance and functioning of endosomesateachstageofthematurationprocess.Perturbationsinendosomemat- urationareimplicatedindevastatingdiseases,suchasneurodegenerationandcancer, andtheendosomematurationprocessesaremanipulatedandexploitedbyintracellu- larpathogenstomeettheirownneeds.Agreaterunderstandingofcoordinationand fine-tuningofendosomematurationwillhelpusaddressvariouspathologiesmore effectively. Abbreviations EE Earlyendosome CI-M6PR Cation-independentmannose-6-phosphatereceptor ILV Intraluminalvesicle LE Lateendosome MVB Multivesicularbody PIP Phosphoinositidephosphate PM Plasmamembrane TfR Transferrinreceptor TGN Trans-Golginetwork 1.1 EndosomeMaturation Overview Plasma membrane (PM) turnover and ingestion of extracellular material relies on a variety of endocytic pathways. The best studied pathway is clathrin-dependent endocytosis,whichentailsrecognitionofcargoviaspecificreceptors,development ofclathrin-coatedpit,andformationofsubsequentclathrin-coatedvesicle(Doherty and McMahon 2009). Indiscriminate fluid sampling is concerted by macropinocy- tosis (Buckley and King 2017). A number of alternative endocytic pathways have beendescribedandmaybecategorized bytheirPM-associatedmediators,suchas