Endosome maturation

Being deeply connected to signalling, cell dynamics, growth, regulation, and defence, endocytic processes are linked to almost all aspects of cell life and disease. In this review, we focus on endosomes in the classical endocytic pathway, and on the programme of changes that lead to the formation and maturation of late endosomes/multivesicular bodies. The maturation programme entails a dramatic transformation of these dynamic organelles disconnecting them functionally and spatially from early endosomes and preparing them for their unidirectional role as a feeder pathway to lysosomes.

[1]  Barbara Karten,et al.  Mechanisms and consequences of impaired lipid trafficking in Niemann-Pick type C1-deficient mammalian cells. , 2009, Biochimica et biophysica acta.

[2]  P. Kane The Where, When, and How of Organelle Acidification by the Yeast Vacuolar H+-ATPase , 2006, Microbiology and Molecular Biology Reviews.

[3]  Graça Raposo,et al.  Exosomes--vesicular carriers for intercellular communication. , 2009, Current opinion in cell biology.

[4]  A. Helenius,et al.  Transport of macrophage Fc receptors and Fc receptor-bound ligands to lysosomes , 1986, The Journal of experimental medicine.

[5]  J. Klumperman,et al.  Bilayered clathrin coats on endosomal vacuoles are involved in protein sorting toward lysosomes. , 2002, Molecular biology of the cell.

[6]  R. Murphy,et al.  Effect of Bafilomycin A1 and Nocodazole on Endocytic Transport in HeLa Cells: Implications for Viral Uncoating and Infection , 1998, Journal of Virology.

[7]  D. Billadeau,et al.  A FAM21-containing WASH complex regulates retromer-dependent sorting. , 2009, Developmental cell.

[8]  Roop Mallik,et al.  Tug-of-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes , 2009, Proceedings of the National Academy of Sciences.

[9]  Harald Stenmark,et al.  Role of Rab5 in the Recruitment of hVps34/p150 to the Early Endosome , 2002, Traffic.

[10]  F. Gu,et al.  An endosomal beta COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes , 1996, The Journal of cell biology.

[11]  S. Grinstein,et al.  Modulation of Rab5 and Rab7 Recruitment to Phagosomes by Phosphatidylinositol 3-Kinase , 2003, Molecular and Cellular Biology.

[12]  M. Okada,et al.  The novel lipid raft adaptor p18 controls endosome dynamics by anchoring the MEK–ERK pathway to late endosomes , 2009, The EMBO journal.

[13]  Ingrid Roxrud,et al.  ESCRT & Co , 2010, Biology of the cell.

[14]  D. Ausiello,et al.  V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway , 2006, Nature Cell Biology.

[15]  J. Paul Luzio,et al.  Lysosomes: fusion and function , 2007, Nature Reviews Molecular Cell Biology.

[16]  P. van Kerkhof,et al.  The ubiquitin-proteasome pathway regulates lysosomal degradation of the growth hormone receptor and its ligand. , 2001, Biochemical Society transactions.

[17]  R. Parton,et al.  A lipid associated with the antiphospholipid syndrome regulates endosome structure and function , 1998, Nature.

[18]  K. Takei,et al.  Fission of Tubular Endosomes Triggers Endosomal Acidification and Movement , 2011, PloS one.

[19]  Pier Paolo Di Fiore,et al.  The Eps8 protein coordinates EGF receptor signalling through Rac and trafficking through Rab5 , 2000, Nature.

[20]  P. Pimpl,et al.  Retromer recycles vacuolar sorting receptors from the trans-Golgi network. , 2010, The Plant journal : for cell and molecular biology.

[21]  I. Bahar,et al.  [Epidermal growth factor receptor]. , 1994, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[22]  B. Habermann,et al.  Modulation of Receptor Recycling and Degradation by the Endosomal Kinesin KIF16B , 2005, Cell.

[23]  Sarah E. Ewald,et al.  The ectodomain of Toll-like receptor 9 is cleaved to generate a functional receptor , 2008, Nature.

[24]  F. G. van der Goot,et al.  Intra-endosomal membrane traffic. , 2006, Trends in cell biology.

[25]  F. Gu,et al.  Functional Dissection of COP-I Subunits in the Biogenesis of Multivesicular Endosomes , 1997, The Journal of cell biology.

[26]  E. V. van Donselaar,et al.  Recycling Compartments and the Internal Vesicles of Multivesicular Bodies Harbor Most of the Cholesterol Found in the Endocytic Pathway , 2003, Traffic.

[27]  C. Futter,et al.  Multivesicular bodies: co-ordinated progression to maturity , 2008, Current opinion in cell biology.

[28]  Miguel C. Seabra,et al.  Rab27a and Rab27b control different steps of the exosome secretion pathway , 2010, Nature Cell Biology.

[29]  N. Pedersen,et al.  Ultrastructural characterization of giant endosomes induced by GTPase-deficient Rab5 , 2009, Histochemistry and Cell Biology.

[30]  R. Bell,et al.  A Protein Interaction Network for Ecm29 Links the 26 S Proteasome to Molecular Motors and Endosomal Components* , 2010, The Journal of Biological Chemistry.

[31]  K. Nakayama,et al.  Tollip and Tom1 Form a Complex and Recruit Ubiquitin-conjugated Proteins onto Early Endosomes* , 2004, Journal of Biological Chemistry.

[32]  K. Ravichandran,et al.  Identification of two evolutionarily conserved genes regulating processing of engulfed apoptotic cells , 2010, Nature.

[33]  C. Mitchell,et al.  TBC domain family, member 15 is a novel mammalian Rab GTPase-activating protein with substrate preference for Rab7. , 2005, Biochemical and biophysical research communications.

[34]  T. Noda,et al.  Rubicon and PLEKHM1 Negatively Regulate the Endocytic/Autophagic Pathway via a Novel Rab7-binding Domain , 2010, Molecular biology of the cell.

[35]  D. Reijngoud,et al.  Effect of ionophores on intralysosomal pH. , 1976, Biochimica et biophysica acta.

[36]  N. Pedersen,et al.  Ubiquitination of alpha 5 beta 1 integrin controls fibroblast migration through lysosomal degradation of fibronectin-integrin complexes. , 2010, Developmental cell.

[37]  I. Mellman,et al.  Activation of Lysosomal Function During Dendritic Cell Maturation , 2003, Science.

[38]  M. W. Wooten,et al.  TrkA Receptor Endolysosomal Degradation is Both Ubiquitin and Proteasome Dependent , 2008, Traffic.

[39]  J. Gruenberg,et al.  Ion flux and the function of endosomes and lysosomes: pH is just the start , 2011, BioEssays : news and reviews in molecular, cellular and developmental biology.

[40]  A. Shisheva PIKfyve: Partners, significance, debates and paradoxes , 2008, Cell biology international.

[41]  Michael J Rust,et al.  Ligands for Clathrin-Mediated Endocytosis Are Differentially Sorted into Distinct Populations of Early Endosomes , 2006, Cell.

[42]  C. Brett,et al.  Vps-c Complexes: Gatekeepers of Endolysosomal Traffic This Review Comes from a Themed Issue on Membranes and Organelles Edited Vps-c Complexes: Molecular Organization Cellular Functions and Regulation , 2022 .

[43]  N. Ohgami,et al.  Roles of Endogenously Synthesized Sterols in the Endocytic Pathway* , 2006, Journal of Biological Chemistry.

[44]  M. Schliwa,et al.  Powering membrane traffic in endocytosis and recycling , 2006, Nature Reviews Molecular Cell Biology.

[45]  M. Waterfield,et al.  A selective PIKfyve inhibitor blocks PtdIns(3,5)P2 production and disrupts endomembrane transport and retroviral budding , 2008, EMBO reports.

[46]  J. Garin,et al.  Regulation of the V-ATPase along the Endocytic Pathway Occurs through Reversible Subunit Association and Membrane Localization , 2008, PloS one.

[47]  Marino Zerial,et al.  Identification of the Switch in Early-to-Late Endosome Transition , 2010, Cell.

[48]  S. Munro,et al.  Organelle identity and the signposts for membrane traffic , 2005, Nature.

[49]  C. Bucci,et al.  RILP is required for the proper morphology and function of late endosomes , 2007, Journal of Cell Science.

[50]  Michael Forgac,et al.  Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology , 2007, Nature Reviews Molecular Cell Biology.

[51]  H. Geuze,et al.  Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump , 1995, The Journal of cell biology.

[52]  D. Lambright,et al.  TBC-2 Regulates RAB-5/RAB-7-mediated Endosomal Trafficking in Caenorhabditis elegans , 2010, Molecular biology of the cell.

[53]  Qing Jun Wang,et al.  The Beclin 1-VPS34 complex--at the crossroads of autophagy and beyond. , 2010, Trends in cell biology.

[54]  N. Mizushima,et al.  Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. , 2008, Molecular biology of the cell.

[55]  S. Emr,et al.  Fab1p PtdIns(3)P 5-Kinase Function Essential for Protein Sorting in the Multivesicular Body , 1998, Cell.

[56]  K. Köhrer,et al.  Multilamellar endosome-like compartment accumulates in the yeast vps28 vacuolar protein sorting mutant. , 1996, Molecular biology of the cell.

[57]  M. Velluz,et al.  In vitro budding of intralumenal vesicles into late endosomes is regulated by Alix and Tsg101. , 2008, Molecular biology of the cell.

[58]  R. Legouis,et al.  Developmental and cellular functions of the ESCRT machinery in pluricellular organisms , 2010, Biology of the cell.

[59]  M. Welch,et al.  WASH and the Arp2/3 complex regulate endosome shape and trafficking , 2010, Cytoskeleton.

[60]  K. Sandhoff,et al.  Lysosomal degradation of membrane lipids , 2010, FEBS letters.

[61]  D. Teis,et al.  Localization of the MP1-MAPK scaffold complex to endosomes is mediated by p14 and required for signal transduction. , 2002, Developmental cell.

[62]  R. Murphy,et al.  Transferrin recycling and dextran transport to lysosomes is differentially affected by bafilomycin, nocodazole, and low temperature , 2005, Cell and Tissue Research.

[63]  W. Wickner,et al.  Remodeling of organelle-bound actin is required for yeast vacuole fusion , 2002, The Journal of cell biology.

[64]  J. Klumperman,et al.  Imaging and imagination: understanding the endo-lysosomal system , 2008, Histochemistry and Cell Biology.

[65]  K. Struhl,et al.  TFIIS Enhances Transcriptional Elongation through an Artificial Arrest Site In Vivo , 2001, Molecular and Cellular Biology.

[66]  Z. Sheng,et al.  Snapin: a SNARE–associated protein implicated in synaptic transmission , 1999, Nature Neuroscience.

[67]  P. Woodman ESCRT proteins, endosome organization and mitogenic receptor down-regulation. , 2009, Biochemical Society transactions.

[68]  S. Emr,et al.  Fab1p Is Essential for PtdIns(3)P 5-Kinase Activity and the Maintenance of Vacuolar Size and Membrane Homeostasis , 1998, The Journal of cell biology.

[69]  T. Jentsch,et al.  CLC Chloride Channels and Transporters: From Genes to Protein Structure, Pathology and Physiology , 2008, Critical reviews in biochemistry and molecular biology.

[70]  S. Emr,et al.  Vps27 recruits ESCRT machinery to endosomes during MVB sorting , 2003, The Journal of cell biology.

[71]  A. Helenius,et al.  Caveolin-1 is ubiquitinated and targeted to intralumenal vesicles in endolysosomes for degradation , 2010, The Journal of cell biology.

[72]  L. Weisman,et al.  PI(3,5)P(2) controls membrane trafficking by direct activation of mucolipin Ca(2+) release channels in the endolysosome. , 2010, Nature communications.

[73]  A. Wandinger-Ness,et al.  Human VPS 34 and p 150 are Rab 7 Interacting Partners , 2003 .

[74]  K. Takegawa,et al.  Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. , 1993, Science.

[75]  R. Teasdale,et al.  Defining Macropinocytosis , 2009, Traffic.

[76]  C. Ostrowicz,et al.  The Mon1-Ccz1 Complex Is the GEF of the Late Endosomal Rab7 Homolog Ypt7 , 2010, Current Biology.

[77]  J. Tian,et al.  Snapin Facilitates the Synchronization of Synaptic Vesicle Fusion , 2009, Neuron.

[78]  B. André,et al.  K63-linked ubiquitin chains as a specific signal for protein sorting into the multivesicular body pathway , 2009, The Journal of cell biology.

[79]  S. Caplan,et al.  The early endosome: a busy sorting station for proteins at the crossroads. , 2010, Histology and histopathology.

[80]  M. Ahmadian,et al.  Armus Is a Rac1 Effector that Inactivates Rab7 and Regulates E-Cadherin Degradation , 2010, Current Biology.

[81]  A. Wolkoff,et al.  Microtubule-dependent movement of late endocytic vesicles in vitro: requirements for Dynein and Kinesin. , 2004, Molecular biology of the cell.

[82]  W. Hong,et al.  RILP interacts with VPS22 and VPS36 of ESCRT-II and regulates their membrane recruitment. , 2006, Biochemical and biophysical research communications.

[83]  Ming Zhang,et al.  Rab7: roles in membrane trafficking and disease. , 2009, Bioscience reports.

[84]  Y. Kalaidzidis,et al.  Rab Conversion as a Mechanism of Progression from Early to Late Endosomes , 2005, Cell.

[85]  M. Zerial,et al.  Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments , 1990, Cell.

[86]  K. Zimmer,et al.  Lysosome proteins are redistributed during expression of a GTP-hydrolysis-defective rab5a. , 2001, Journal of cell science.

[87]  C. Futter,et al.  EGF stimulates annexin 1‐dependent inward vesiculation in a multivesicular endosome subpopulation , 2006, The EMBO journal.

[88]  A. Wolkoff,et al.  Reconstitution of ATP-dependent movement of endocytic vesicles along microtubules in vitro: an oscillatory bidirectional process. , 2000, Molecular biology of the cell.

[89]  Jean Gruenberg,et al.  The biogenesis of multivesicular endosomes , 2004, Nature Reviews Molecular Cell Biology.

[90]  S. Leppla,et al.  Membrane insertion of anthrax protective antigen and cytoplasmic delivery of lethal factor occur at different stages of the endocytic pathway , 2004, The Journal of cell biology.

[91]  Sushmita Mukherjee,et al.  Endocytic Sorting of Lipid Analogues Differing Solely in the Chemistry of Their Hydrophobic Tails , 1999, The Journal of cell biology.

[92]  F. Maxfield,et al.  Endocytic recycling , 2004, Nature Reviews Molecular Cell Biology.

[93]  W. Zwart,et al.  Activation of endosomal dynein motors by stepwise assembly of Rab7–RILP–p150Glued, ORP1L, and the receptor βlll spectrin , 2007, The Journal of cell biology.

[94]  J. Hurley The ESCRT complexes , 2010, Critical reviews in biochemistry and molecular biology.

[95]  Y. Kalaidzidis,et al.  Systems survey of endocytosis by multiparametric image analysis , 2010, Nature.

[96]  J. Bonifacino,et al.  Retrograde transport from endosomes to the trans-Golgi network , 2006, Nature Reviews Molecular Cell Biology.

[97]  G. D’Angelo,et al.  Function and dysfunction of the PI system in membrane trafficking , 2008, The EMBO journal.

[98]  M. Fivaz,et al.  Late Endosomal Cholesterol Accumulation Leads to Impaired Intra-Endosomal Trafficking , 2007, PloS one.

[99]  Anthony A. Hyman,et al.  Rab5 regulates motility of early endosomes on microtubules , 1999, Nature Cell Biology.

[100]  M. J. Clague,et al.  Endocytosis: the DUB version. , 2006, Trends in cell biology.

[101]  G. Raposo,et al.  A lumenal domain-dependent pathway for sorting to intralumenal vesicles of multivesicular endosomes involved in organelle morphogenesis. , 2006, Developmental cell.

[102]  M. Lindsay,et al.  Localization of phosphatidylinositol 3‐phosphate in yeast and mammalian cells , 2000, The EMBO journal.

[103]  C. Melief,et al.  MHC II in Dendritic Cells is Targeted to Lysosomes or T Cell‐Induced Exosomes Via Distinct Multivesicular Body Pathways , 2009, Traffic.

[104]  I. Vernos,et al.  Kinesin‐2 is a Motor for Late Endosomes and Lysosomes , 2005, Traffic.

[105]  A. Shisheva,et al.  Mammalian Cell Morphology and Endocytic Membrane Homeostasis Require Enzymatically Active Phosphoinositide 5-Kinase PIKfyve* , 2001, The Journal of Biological Chemistry.

[106]  J P Luzio,et al.  The role of calcium and other ions in sorting and delivery in the late endocytic pathway. , 2007, Biochemical Society transactions.

[107]  M. Krieger,et al.  A Single Point Mutation in -COP Results in Temperature-sensitive, Lethal Defects in Membrane Transport in a Chinese Hamster Ovary Cell Mutant (*) , 1996, The Journal of Biological Chemistry.

[108]  R. Steinman,et al.  Endocytosis and the recycling of plasma membrane , 1983, The Journal of cell biology.

[109]  R. Michell,et al.  Phosphatidylinositol 3,5-bisphosphate and Fab1p/PIKfyve underPPIn endo-lysosome function. , 2009, The Biochemical journal.

[110]  O. Weisz Acidification and protein traffic. , 2003, International review of cytology.

[111]  O. Staub,et al.  Regulation of stability and function of the epithelial Na+ channel (ENaC) by ubiquitination , 1997, The EMBO journal.

[112]  M. Babst A Protein's Final ESCRT , 2005, Traffic.

[113]  I. Mellman,et al.  Brefeldin A and the endocytic pathway Possible implications for membrane traffic and sorting , 1992, FEBS letters.

[114]  S. Emr,et al.  Phosphoinositide signaling and turnover: PtdIns(3)P, a regulator of membrane traffic, is transported to the vacuole and degraded by a process that requires lumenal vacuolar hydrolase activities , 1998, The EMBO journal.

[115]  H. Riezman,et al.  Involvement of Ypt7p, a small GTPase, in traffic from late endosome to the vacuole in yeast. , 1993, Journal of cell science.

[116]  Qiming Sun,et al.  Rubicon controls endosome maturation as a Rab7 effector , 2010, Proceedings of the National Academy of Sciences.

[117]  S. Brodie,et al.  Membrane flow during pinocytosis. A stereologic analysis , 1976, The Journal of cell biology.

[118]  W. Wickner,et al.  The GTPase Ypt7p of Saccharomyces cerevisiae is required on both partner vacuoles for the homotypic fusion step of vacuole inheritance. , 1995, The EMBO journal.

[119]  D. Lambright,et al.  Rab GEFs and GAPs. , 2010, Current opinion in cell biology.

[120]  K. Howell,et al.  Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro , 1989, The Journal of cell biology.

[121]  J. Lötvall,et al.  Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells , 2007, Nature Cell Biology.

[122]  M. Peñalva Endocytosis in filamentous fungi: Cinderella gets her reward. , 2010, Current opinion in microbiology.

[123]  M. Zerial,et al.  Membrane association of Rab5 mediated by GDP-dissociation inhibitor and accompanied by GDP/GTP exchange , 1994, Nature.

[124]  F. Gu,et al.  Biogenesis of transport intermediates in the endocytic pathway , 1999, FEBS letters.

[125]  U. Rescher,et al.  Annexin A8 regulates late endosome organization and function. , 2008, Molecular biology of the cell.

[126]  J. Hurley,et al.  Membrane budding and scission by the ESCRT machinery: it's all in the neck , 2010, Nature Reviews Molecular Cell Biology.

[127]  M. Futai,et al.  The V-type H+-ATPase in vesicular trafficking: targeting, regulation and function , 2008, Current Opinion in Cell Biology.

[128]  Bianca Habermann,et al.  APPL Proteins Link Rab5 to Nuclear Signal Transduction via an Endosomal Compartment , 2004, Cell.

[129]  J. Besterman,et al.  Endocytosis: a review of mechanisms and plasma membrane dynamics. , 1983, The Biochemical journal.

[130]  C. Bartheld,et al.  Multivesicular bodies in neurons: Distribution, protein content, and trafficking functions , 2011, Progress in Neurobiology.

[131]  F. Maxfield,et al.  Endosome acidification and the pathways of receptor-mediated endocytosis. , 1987, Advances in experimental medicine and biology.

[132]  J. Tooze,et al.  In AtT20 and HeLa cells brefeldin A induces the fusion of tubular endosomes and changes their distribution and some of their endocytic properties , 1992, The Journal of cell biology.

[133]  A. Shisheva,et al.  ArPIKfyve homomeric and heteromeric interactions scaffold PIKfyve and Sac3 in a complex to promote PIKfyve activity and functionality. , 2008, Journal of molecular biology.

[134]  C. Ostrowicz,et al.  Yeast vacuole fusion: A model system for eukaryotic endomembrane dynamics , 2008, Autophagy.

[135]  B Poole,et al.  Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[136]  H. Goodson,et al.  Late endosome motility depends on lipids via the small GTPase Rab7 , 2002, The EMBO journal.

[137]  C. Samakovlis,et al.  Fab1 phosphatidylinositol 3-phosphate 5-kinase controls trafficking but not silencing of endocytosed receptors. , 2006, Molecular biology of the cell.

[138]  T. Schroer,et al.  Microtubule- and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells , 1990, Cell.

[139]  A. Helenius,et al.  Kinetics of endosome acidification detected by mutant and wild‐type Semliki Forest virus. , 1986, The EMBO journal.

[140]  S. Gygi,et al.  The ubiquitin–proteasome system regulates membrane fusion of yeast vacuoles , 2007, The EMBO journal.

[141]  G. Prestwich,et al.  Lysobisphosphatidic Acid Controls Endosomal Cholesterol Levels* , 2008, Journal of Biological Chemistry.

[142]  R. Parton,et al.  Annexin A2-dependent polymerization of actin mediates endosome biogenesis. , 2009, Developmental cell.

[143]  E. J. V. van Zoelen,et al.  Ligand-induced Lysosomal Epidermal Growth Factor Receptor (EGFR) Degradation Is Preceded by Proteasome-dependent EGFR De-ubiquitination* , 2003, Journal of Biological Chemistry.

[144]  C. Futter,et al.  Distinct roles for Tsg101 and Hrs in multivesicular body formation and inward vesiculation. , 2006, Molecular biology of the cell.

[145]  L. E. Johannessen,et al.  Ubiquitination and proteasomal activity is required for transport of the EGF receptor to inner membranes of multivesicular bodies , 2002, The Journal of cell biology.

[146]  G. Griffiths,et al.  Isolation and characterization of early endosomes, late endosomes and terminal lysosomes: their role in protein degradation. , 1996, Journal of cell science.

[147]  E. Derivery,et al.  The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. , 2009, Developmental cell.

[148]  C. Bucci,et al.  RILP interacts with the VPS22 component of the ESCRT-II complex. , 2006, Biochemical and biophysical research communications.

[149]  C. Ungermann,et al.  Guiding Endosomal Maturation , 2010, Cell.

[150]  H. Fares,et al.  Caenorhabditis elegans SAND‐1 is essential for RAB‐7 function in endosomal traffic , 2007, The EMBO journal.

[151]  Satyajit Mayor,et al.  Pathways of clathrin-independent endocytosis , 2007, Nature Reviews Molecular Cell Biology.

[152]  D. Klionsky,et al.  Yeast homotypic vacuole fusion requires the Ccz1–Mon1 complex during the tethering/docking stage , 2003, The Journal of cell biology.

[153]  Ludger Hengst,et al.  Endocytosis in yeast: Evidence for the involvement of a small GTP-binding protein (Ypt7p) , 1992, Cell.

[154]  Brian P Ceresa,et al.  Rab7 Regulates Late Endocytic Trafficking Downstream of Multivesicular Body Biogenesis and Cargo Sequestration* , 2009, Journal of Biological Chemistry.

[155]  Niloufer G Irani,et al.  Receptor endocytosis and signaling in plants. , 2009, Current opinion in plant biology.

[156]  I. Mellman,et al.  Inhibition of Endosome Function in CHO Cells Bearing a Temperature-sensitive Defect in the Coatomer (COPI) Component ε-COP , 1997, The Journal of cell biology.

[157]  Ira Mellman,et al.  Cell biology of antigen processing in vitro and in vivo. , 2005, Annual review of immunology.

[158]  Owen J. Driskell,et al.  Dynein is required for receptor sorting and the morphogenesis of early endosomes , 2007, Nature Cell Biology.

[159]  G. Whittaker,et al.  The Ubiquitin‐Vacuolar Protein Sorting System is Selectively Required During Entry of Influenza Virus into Host Cells , 2003, Traffic.

[160]  Scott D. Emr,et al.  New Component of the Vacuolar Class C-Vps Complex Couples Nucleotide Exchange on the Ypt7 Gtpase to Snare-Dependent Docking and Fusion , 2000, The Journal of cell biology.

[161]  H. Stenmark,et al.  FYVE and coiled-coil domains determine the specific localisation of Hrs to early endosomes. , 2001, Journal of cell science.

[162]  P. Walther,et al.  Fusion between phagosomes, early and late endosomes: a role for actin in fusion between late, but not early endocytic organelles. , 2003, Molecular biology of the cell.

[163]  K. Shokat,et al.  PIKfyve Regulation of Endosome-Linked Pathways , 2009, Traffic.

[164]  A. Wolkoff,et al.  Microtubule and Motor-Dependent Endocytic Vesicle Sorting in Vitro , 2000, The Journal of cell biology.

[165]  K. Ravichandran,et al.  Phagosome maturation: going through the acid test , 2008, Nature Reviews Molecular Cell Biology.

[166]  G. Bjørkøy,et al.  FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end–directed vesicle transport , 2010, The Journal of cell biology.

[167]  M. J. Clague,et al.  Vacuolar ATPase activity is required for endosomal carrier vesicle formation. , 1994, The Journal of biological chemistry.

[168]  A. Wandinger-Ness,et al.  Human VPS34 and p150 are Rab7 Interacting Partners , 2003, Traffic.

[169]  G. Griffiths,et al.  Cytoplasmic dynein-dependent vesicular transport from early to late endosomes [published erratum appears in J Cell Biol 1994 Feb;124(3):397] , 1993, The Journal of cell biology.

[170]  Ari Helenius,et al.  Virus entry by endocytosis. , 2010, Annual review of biochemistry.

[171]  P. Woodman,et al.  Depletion of TSG101 forms a mammalian `Class E' compartment: a multicisternal early endosome with multiple sorting defects , 2005, Journal of Cell Science.

[172]  I. Madshus,et al.  Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes , 2002, Nature Cell Biology.

[173]  Harald Stenmark,et al.  The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins , 2009, Nature.

[174]  A. Sorkin,et al.  Endocytosis and signalling: intertwining molecular networks , 2009, Nature Reviews Molecular Cell Biology.

[175]  A. Helenius,et al.  Rab7 Associates with Early Endosomes to Mediate Sorting and Transport of Semliki Forest Virus to Late Endosomes , 2005, PLoS biology.

[176]  H. Pelham,et al.  Specific retrieval of the exocytic SNARE Snc1p from early yeast endosomes. , 2000, Molecular biology of the cell.

[177]  L. Santambrogio,et al.  Microautophagy of cytosolic proteins by late endosomes. , 2011, Developmental cell.

[178]  V. Rybin,et al.  ATP-dependent membrane assembly of F-actin facilitates membrane fusion. , 2001, Molecular biology of the cell.

[179]  G. Lukács,et al.  The ESCRT-III subunit hVps24 is required for degradation but not silencing of the epidermal growth factor receptor. , 2006, Molecular biology of the cell.

[180]  H. Pelham Insights from yeast endosomes. , 2002, Current opinion in cell biology.

[181]  C. Wilhelm,et al.  Different Microtubule Motors Move Early and Late Endocytic Compartments , 2008, Traffic.

[182]  Zuoyan Zhu,et al.  C. elegans Rab GTPase activating protein TBC-2 promotes cell corpse degradation by regulating the small GTPase RAB-5 , 2009, Development.

[183]  C. Futter,et al.  Down-regulation of epidermal growth factor receptor signalling within multivesicular bodies. , 2009, Biochemical Society transactions.

[184]  Michael J Rust,et al.  Visualizing infection of individual influenza viruses , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[185]  J. Bonifacino,et al.  Interactions of GGA3 with the ubiquitin sorting machinery , 2004, Nature Cell Biology.

[186]  J. Lippincott-Schwartz,et al.  Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic , 1991, Cell.

[187]  Marino Zerial,et al.  Rab proteins as membrane organizers , 2001, Nature Reviews Molecular Cell Biology.

[188]  J. Dixon,et al.  Myotubularin phosphatases: policing 3-phosphoinositides. , 2006, Trends in cell biology.

[189]  A. Shisheva,et al.  PIKfyve-ArPIKfyve-Sac3 Core Complex , 2009, The Journal of Biological Chemistry.

[190]  A. Brech,et al.  Multivesicular Endosome Biogenesis in the Absence of ESCRTs , 2009, Traffic.

[191]  V. Oberle,et al.  Fluorescent lipid probes: some properties and applications (a review). , 2002, Chemistry and physics of lipids.

[192]  Andreas Deutsch,et al.  Membrane identity and GTPase cascades regulated by toggle and cut-out switches , 2008, Molecular systems biology.

[193]  J. Backer,et al.  The Late Endosome is Essential for mTORC1 Signaling , 2010, Molecular biology of the cell.

[194]  B. Deurs,et al.  Delivery to lysosomes in the human carcinoma cell line HEp-2 involves an actin filament-facilitated fusion between mature endosomes and preexisting lysosomes. , 1995, European journal of cell biology.

[195]  D. Gallwitz,et al.  Primary structure and biochemical characterization of yeast GTPase-activating proteins with substrate preference for the transport GTPase Ypt7p. , 1999, European journal of biochemistry.

[196]  V. Rybin,et al.  Functional synergy between Rab5 effector Rabaptin-5 and exchange factor Rabex-5 when physically associated in a complex. , 2001, Molecular biology of the cell.

[197]  A. Shisheva,et al.  Phosphatidylinositol 5-Phosphate Biosynthesis Is Linked to PIKfyve and Is Involved in Osmotic Response Pathway in Mammalian Cells* , 2002, The Journal of Biological Chemistry.

[198]  D. Bilder,et al.  The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. , 2005, Developmental cell.

[199]  S. Emr,et al.  ESCRT-I Core and ESCRT-II GLUE Domain Structures Reveal Role for GLUE in Linking to ESCRT-I and Membranes , 2006, Cell.

[200]  N. Demaurex,et al.  Endosome-to-cytosol transport of viral nucleocapsids , 2005, Nature Cell Biology.

[201]  A. Wandinger-Ness,et al.  The proteasome alpha-subunit XAPC7 interacts specifically with Rab7 and late endosomes. , 2004, The Journal of biological chemistry.

[202]  A. Rudensky,et al.  Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells , 2001, The Journal of cell biology.

[203]  K. Altendorf,et al.  Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[204]  R. Piper,et al.  Biogenesis and function of multivesicular bodies. , 2007, Annual review of cell and developmental biology.

[205]  M. Kaksonen,et al.  Harnessing actin dynamics for clathrin-mediated endocytosis , 2006, Nature Reviews Molecular Cell Biology.

[206]  C. Klein,et al.  p14–MP1-MEK1 signaling regulates endosomal traffic and cellular proliferation during tissue homeostasis , 2006, The Journal of cell biology.

[207]  B. Grant,et al.  Intracellular trafficking. , 2006, WormBook : the online review of C. elegans biology.

[208]  Jacques Neefjes,et al.  The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors , 2001, Current Biology.

[209]  N. Hirokawa,et al.  Kinesin superfamily motor proteins and intracellular transport , 2009, Nature Reviews Molecular Cell Biology.

[210]  Eigen R. Peralta,et al.  Differential Effects of TBC1D15 and Mammalian Vps39 on Rab7 Activation State, Lysosomal Morphology, and Growth Factor Dependence* , 2010, The Journal of Biological Chemistry.

[211]  W. Wickner,et al.  Rho1p and Cdc42p act after Ypt7p to regulate vacuole docking , 2001, The EMBO journal.

[212]  A. Helenius,et al.  Virus Entry into Animal Cells , 1989, Advances in Virus Research.

[213]  J. Bonifacino,et al.  Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7 , 2008, The Journal of cell biology.

[214]  J. Taylor,et al.  HDAC6 controls autophagosome maturation essential for ubiquitin‐selective quality‐control autophagy , 2010, The EMBO journal.

[215]  L. Collinson,et al.  JCB Article , 2001 .

[216]  P. Chavrier,et al.  The rab7 GTPase resides on a vesicular compartment connected to lysosomes. , 1995, Journal of cell science.

[217]  B. Deurs,et al.  Rab7: a key to lysosome biogenesis. , 2000, Molecular biology of the cell.

[218]  M. Labouesse,et al.  The phosphoinositide kinase PIKfyve/Fab1p regulates terminal lysosome maturation in Caenorhabditis elegans. , 2006, Molecular biology of the cell.

[219]  F. Barr,et al.  A GTPase-activating protein controls Rab5 function in endocytic trafficking , 2005, Nature Cell Biology.

[220]  A. Wandinger-Ness,et al.  The Proteasome α-Subunit XAPC7 Interacts Specifically with Rab7 and Late Endosomes* , 2004, Journal of Biological Chemistry.

[221]  K. Cortese,et al.  The vacuolar ATPase is required for physiological as well as pathological activation of the Notch receptor , 2010, Development.

[222]  Stefan Matile,et al.  Role of LBPA and Alix in Multivesicular Liposome Formation and Endosome Organization , 2004, Science.

[223]  S. Grinstein,et al.  Regulation of Vacuolar pH and Its Modulation by Some Microbial Species , 2007, Microbiology and Molecular Biology Reviews.

[224]  Petra Schwille,et al.  Ceramide Triggers Budding of Exosome Vesicles into Multivesicular Endosomes , 2008, Science.

[225]  M. Kanzaki,et al.  Functional Dissection of Lipid and Protein Kinase Signals of PIKfyve Reveals the Role of PtdIns 3,5-P2 Production for Endomembrane Integrity* , 2002, The Journal of Biological Chemistry.

[226]  W. Möbius,et al.  Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A–C , 2010, The Journal of cell biology.

[227]  J. Bonifacino,et al.  Ubiquitin binding and conjugation regulate the recruitment of Rabex‐5 to early endosomes , 2008, The EMBO journal.

[228]  F. Platt,et al.  Common and Uncommon Pathogenic Cascades in Lysosomal Storage Diseases* , 2010, The Journal of Biological Chemistry.

[229]  S. Pfeffer Multiple routes of protein transport from endosomes to the trans Golgi network , 2009, FEBS letters.

[230]  C. Bucci,et al.  Microtubules are involved in bafilomycin A1-induced tubulation and Rab5-dependent vacuolation of early endosomes. , 1997, European journal of cell biology.

[231]  R. Finley,et al.  Active PIKfyve Associates with and Promotes the Membrane Attachment of the Late Endosome-to-trans-Golgi Network Transport Factor Rab9 Effector p40* , 2003, Journal of Biological Chemistry.

[232]  M. Zerial,et al.  Phosphatidylinositol-3-OH kinases are Rab5 effectors , 1999, Nature Cell Biology.

[233]  I. Mellman Endocytosis and molecular sorting. , 1996, Annual review of cell and developmental biology.

[234]  Michelangelo Foti,et al.  PIKfyve controls fluid phase endocytosis but not recycling/degradation of endocytosed receptors or sorting of procathepsin D by regulating multivesicular body morphogenesis. , 2003, Molecular biology of the cell.

[235]  E. Eskelinen New insights into the mechanisms of macroautophagy in mammalian cells. , 2008, International review of cell and molecular biology.

[236]  J. Luzio,et al.  The Role of Intraorganellar Ca2+In Late Endosome–Lysosome Heterotypic Fusion and in the Reformation of Lysosomes from Hybrid Organelles , 2000, The Journal of cell biology.

[237]  Yuko Hirota,et al.  A role for Rab5 activity in the biogenesis of endosomal and lysosomal compartments. , 2007, Biochemical and biophysical research communications.

[238]  O. Voinnet,et al.  Control of RNA silencing and localization by endolysosomes. , 2010, Trends in cell biology.

[239]  H. Stenmark,et al.  Eap45 in Mammalian ESCRT-II Binds Ubiquitin via a Phosphoinositide-interacting GLUE Domain*♦ , 2005, Journal of Biological Chemistry.

[240]  P. Cosson,et al.  Separation and Characterization of Late Endosomal Membrane Domains* , 2002, The Journal of Biological Chemistry.

[241]  Qian Cai,et al.  Snapin-Regulated Late Endosomal Transport Is Critical for Efficient Autophagy-Lysosomal Function in Neurons , 2010, Neuron.

[242]  Marino Zerial,et al.  A Novel Rab5 GDP/GTP Exchange Factor Complexed to Rabaptin-5 Links Nucleotide Exchange to Effector Recruitment and Function , 1997, Cell.

[243]  A. Corbett,et al.  The subcellular localization of the Niemann-Pick Type C proteins depends on the adaptor complex AP-3 , 2007, Journal of Cell Science.

[244]  O. Gerasimenko,et al.  Calcium uptake via endocytosis with rapid release from acidifying endosomes , 1998, Current Biology.

[245]  P. Saftig,et al.  Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function , 2009, Nature Reviews Molecular Cell Biology.

[246]  R. Kahn,et al.  Intravesicular acidification correlates with binding of ADP-ribosylation factor to microsomal membranes. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[247]  Sushmita Mukherjee,et al.  Membrane domains. , 2004, Annual review of cell and developmental biology.

[248]  Ronald D. Vale,et al.  Regulators of the cytoplasmic dynein motor , 2009, Nature Reviews Molecular Cell Biology.

[249]  A. M. Riley,et al.  Identification of Mammalian Vps24p as an Effector of Phosphatidylinositol 3,5-Bisphosphate-dependent Endosome Compartmentalization* , 2003, Journal of Biological Chemistry.

[250]  J. Backer,et al.  Role of Rab 5 in the Recruitment of hVps 34 / p 150 to the Early Endosome , 2002 .

[251]  H. Stenmark,et al.  Endocytosis and signaling. , 2011, Current opinion in cell biology.