The endocytic pathway: a mosaic of domains

Organelles in the endocytic pathway are composed of a mosaic of structural and functional regions. These regions consist, at least in part, of specialized protein–lipid domains within the plane of the membrane, or of protein complexes associated with specific membrane lipids. Whereas some of these molecular assemblies can be found in more than one compartment, a given combination seems to be unique to each compartment, indicating that membrane organization might be modular.

[1]  T. Linke,et al.  Lysosomal Degradation on Vesicular Membrane Surfaces , 1998, The Journal of Biological Chemistry.

[2]  R. Parton,et al.  Regulated internalization of caveolae , 1994, The Journal of cell biology.

[3]  M. Komada,et al.  Hrs, a FYVE finger protein localized to early endosomes, is implicated in vesicular traffic and required for ventral folding morphogenesis. , 1999, Genes & development.

[4]  J. Neefjes,et al.  Multivesicular body morphogenesis requires phosphatidyl-inositol 3-kinase activity , 1999, Current Biology.

[5]  A. Brisson,et al.  Trimers, dimers of trimers, and trimers of trimers are common building blocks of annexin a5 two-dimensional crystals. , 2001, Journal of structural biology.

[6]  C. Hopkins,et al.  Movement of internalized ligand–receptor complexes along a continuous endosomal reticulum , 1990, Nature.

[7]  Marino Zerial,et al.  Distinct Membrane Domains on Endosomes in the Recycling Pathway Visualized by Multicolor Imaging of Rab4, Rab5, and Rab11 , 2000, The Journal of cell biology.

[8]  H. Geuze.  The role of endosomes and lysosomes in MHC class II functioning. , 1998, Immunology today.

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

[10]  A. Dautry‐Varsat,et al.  Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. , 2001, Molecular cell.

[11]  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.

[12]  M. Lindsay,et al.  The tetraspanin CD63/lamp3 cycles between endocytic and secretory compartments in human endothelial cells. , 2000, Molecular biology of the cell.

[13]  V. Rybin,et al.  Oligomeric Complexes Link Rab5 Effectors with NSF and Drive Membrane Fusion via Interactions between EEA1 and Syntaxin 13 , 1999, Cell.

[14]  M. Lindsay,et al.  Interaction of antiphospholipid antibodies with late endosomes of human endothelial cells. , 1999 .

[15]  Xiaolong Wei,et al.  Hrs Interacts with Sorting Nexin 1 and Regulates Degradation of Epidermal Growth Factor Receptor* , 2001, The Journal of Biological Chemistry.

[16]  E. Babiychuk,et al.  Annexins in Cell Membrane Dynamics , 2000, The Journal of cell biology.

[17]  R. Kellner,et al.  Specific release of membrane-bound annexin II and cortical cytoskeletal elements by sequestration of membrane cholesterol. , 1997, Molecular biology of the cell.

[18]  W. Hong,et al.  SNX3 regulates endosomal function through its PX-domain-mediated interaction with PtdIns(3)P , 2001, Nature Cell Biology.

[19]  E. Ikonen,et al.  Roles of lipid rafts in membrane transport. , 2001, Current opinion in cell biology.

[20]  K. Simons,et al.  Jamming the endosomal system: lipid rafts and lysosomal storage diseases. , 2000, Trends in cell biology.

[21]  C. Futter,et al.  Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes , 1996, The Journal of cell biology.

[22]  R. Bacallao,et al.  pH-induced microtubule-dependent redistribution of late endosomes in neuronal and epithelial cells , 1991, The Journal of cell biology.

[23]  F. Maxfield,et al.  Cholesterol distribution in living cells: fluorescence imaging using dehydroergosterol as a fluorescent cholesterol analog. , 1998, Biophysical journal.

[24]  I. Mellman,et al.  The mannose 6-phosphate receptor and the biogenesis of lysosomes , 1988, Cell.

[25]  A. Dautry‐Varsat,et al.  Molecular Characterization of the Signal Responsible for the Targeting of the Interleukin 2 Receptor β Chain toward Intracellular Degradation* , 1998, The Journal of Biological Chemistry.

[26]  B. Goud,et al.  Rab proteins. , 1998, Biochimica et biophysica acta.

[27]  R. Woodworth,et al.  Exocytosis of pinocytosed fluid in cultured cells: kinetic evidence for rapid turnover and compartmentation , 1981, The Journal of cell biology.

[28]  R. Schekman,et al.  Coatomer, Arf1p, and nucleotide are required to bud coat protein complex I-coated vesicles from large synthetic liposomes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[29]  S. Moss,et al.  Annexins and membrane dynamics. , 1997, Biochimica et biophysica acta.

[30]  M. Zerial,et al.  Rabaptin-5 is a direct effector of the small GTPase Rab5 in endocytic membrane fusion , 1995, Cell.

[31]  A. Dautry‐Varsat,et al.  Involvement of the ubiquitin/proteasome system in sorting of the interleukin 2 receptor beta chain to late endocytic compartments. , 2001, Molecular biology of the cell.

[32]  N. Morrice,et al.  A novel role for Rab5–GDI in ligand sequestration into clathrin-coated pits , 1998, Current Biology.

[33]  I. Mellman,et al.  Cytoplasmic coat proteins involved in endosome function , 1995, Cell.

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

[35]  S. Mayor,et al.  Bafilomycin A1 Treatment Retards Transferrin Receptor Recycling More than Bulk Membrane Recycling* , 1997, The Journal of Biological Chemistry.

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

[37]  T. Stevens,et al.  VPS21 controls entry of endocytosed and biosynthetic proteins into the yeast prevacuolar compartment. , 2000, Molecular biology of the cell.

[38]  Marino Zerial,et al.  EEA1 links PI(3)K function to Rab5 regulation of endosome fusion , 1998, Nature.

[39]  P. Hollenbeck,et al.  Radial extension of macrophage tubular lysosomes supported by kinesin , 1990, Nature.

[40]  M. Komada,et al.  Hrs, a Tyrosine Kinase Substrate with a Conserved Double Zinc Finger Domain, Is Localized to the Cytoplasmic Surface of Early Endosomes* , 1997, The Journal of Biological Chemistry.

[41]  H. Geuze,et al.  Selective Enrichment of Tetraspan Proteins on the Internal Vesicles of Multivesicular Endosomes and on Exosomes Secreted by Human B-lymphocytes* , 1998, The Journal of Biological Chemistry.

[42]  R. Scheller,et al.  Syntaxin 13 Mediates Cycling of Plasma Membrane Proteins via Tubulovesicular Recycling Endosomes , 1998, The Journal of cell biology.

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

[44]  M. Patterson,et al.  The Niemann-Pick C1 Protein Resides in a Vesicular Compartment Linked to Retrograde Transport of Multiple Lysosomal Cargo* , 1999, The Journal of Biological Chemistry.

[45]  D. Hirsh,et al.  Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells , 2001, Nature Cell Biology.

[46]  Paul Tempst,et al.  PtdIns(3)P regulates the neutrophil oxidase complex by binding to the PX domain of p40phox , 2001, Nature Cell Biology.

[47]  K. Paiha,et al.  Both Calmodulin and the Unconventional Myosin Myr4 Regulate Membrane Trafficking Along the Recycling Pathway of MDCK Cells , 2000, Traffic.

[48]  Richard H. Scheller,et al.  SNARE-mediated membrane fusion , 2001, Nature Reviews Molecular Cell Biology.

[49]  R. Scheller,et al.  SNARE Protein Trafficking in Polarized MDCK Cells , 2000, Traffic.

[50]  B. Kay,et al.  The EH network. , 1999, Experimental cell research.

[51]  S. Smerdon,et al.  The structural basis of Arfaptin-mediated cross-talk between Rac and Arf signalling pathways , 2001, Nature.

[52]  G. Apodaca,et al.  Endocytic Traffic in Polarized Epithelial Cells: Role of the Actin and Microtubule Cytoskeleton , 2001, Traffic.

[53]  Lucas Pelkmans,et al.  Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER , 2001, Nature Cell Biology.

[54]  R. Havel,et al.  A tubular endosomal fraction from rat liver: biochemical evidence of receptor sorting by default. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[55]  M. Yaffe,et al.  The PX domains of p47phox and p40phox bind to lipid products of PI(3)K , 2001, Nature Cell Biology.

[56]  G. Griffiths,et al.  Evidence for retrograde traffic between terminal lysosomes and the prelysosomal/late endosome compartment. , 1994, Journal of cell science.

[57]  M. Mann,et al.  p95-APP1 links membrane transport to Rac-mediated reorganization of actin , 2000, Nature Cell Biology.

[58]  M. Aridor,et al.  Traffic Jam: A Compendium of Human Diseases that Affect Intracellular Transport Processes , 2000, Traffic.

[59]  J. Luzio,et al.  Fusion of Lysosomes with Late Endosomes Produces a Hybrid Organelle of Intermediate Density and Is NSF Dependent , 1998, The Journal of cell biology.

[60]  H. Horstmann,et al.  Immunocytochemical characterization of the endocytic and phagolysosomal compartments in peritoneal macrophages , 1992, The Journal of cell biology.

[61]  P. Verkade,et al.  Induction of Caveolae in the Apical Plasma Membrane of Madin-Darby Canine Kidney Cells , 2000, The Journal of cell biology.

[62]  G. Raposo,et al.  Truncated Brush Border Myosin I Affects Membrane Traffic in Polarized Epithelial Cells , 2000, Traffic.

[63]  L. Huber,et al.  The recycling endosome of Madin-Darby canine kidney cells is a mildly acidic compartment rich in raft components. , 2000, Molecular biology of the cell.

[64]  H. Radhakrishna,et al.  Separation of Membrane Trafficking and Actin Remodeling Functions of ARF6 with an Effector Domain Mutant , 2000, Molecular and Cellular Biology.

[65]  H. Stenmark,et al.  The Rab5 Effector EEA1 Interacts Directly with Syntaxin-6* , 1999, The Journal of Biological Chemistry.

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

[67]  A. Brown,et al.  Transacylase and phospholipases in the synthesis of bis(monoacylglycero)phosphate. , 1996, Biochemistry.

[68]  F. Maxfield,et al.  Characterization of Rapid Membrane Internalization and Recycling* , 2000, The Journal of Biological Chemistry.

[69]  R. Kellner,et al.  Annexin II is a major component of fusogenic endosomal vesicles , 1993, The Journal of cell biology.

[70]  F. Maxfield,et al.  Membrane transport in the endocytic pathway. , 1995, Current opinion in cell biology.

[71]  Juan S. Bonifacino,et al.  Human Vam6p promotes lysosome clustering and fusion in vivo , 2001, The Journal of cell biology.

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

[73]  D. Cutler,et al.  Lysosomal Targeting of P-selectin Is Mediated by a Novel Sequence within Its Cytoplasmic Tail* , 1998, The Journal of Biological Chemistry.

[74]  A. Miyashita,et al.  Molecular cloning of a novel 130-kDa cytoplasmic protein, Ankhzn, containing Ankyrin repeats hooked to a zinc finger motif. , 1999, Biochemical and biophysical research communications.

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

[76]  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.

[77]  D. Botstein,et al.  Visualization of receptor-mediated endocytosis in yeast. , 1999, Molecular biology of the cell.

[78]  M. Kleijmeer,et al.  Follicular Dendritic Cells Carry MHC Class II-Expressing Microvesicles at Their Surface1 , 2000, The Journal of Immunology.

[79]  M. Krieger,et al.  Isolation of three classes of conditional lethal Chinese hamster ovary cell mutants with temperature-dependent defects in low density lipoprotein receptor stability and intracellular membrane transport. , 1994, The Journal of biological chemistry.

[80]  S. Emr,et al.  Phox domain interaction with PtdIns(3)P targets the Vam7 t-SNARE to vacuole membranes , 2001, Nature Cell Biology.

[81]  T. Kirchhausen,et al.  Three ways to make a vesicle , 2000, Nature Reviews Molecular Cell Biology.

[82]  R. Palmiter,et al.  Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport , 1999, Nature Cell Biology.

[83]  C. Haft,et al.  Overexpression of a Novel Sorting Nexin, SNX15, Affects Endosome Morphology and Protein Trafficking , 2000, Traffic.

[84]  F. Maxfield,et al.  Role of Membrane Organization and Membrane Domains in Endocytic Lipid Trafficking , 2000, Traffic.

[85]  A. Beyer,et al.  Cloning, characterisation, and functional expression of the Mus musculus SKD1 gene in yeast demonstrates that the mouse SKD1 and the yeast VPS4 genes are orthologues and involved in intracellular protein trafficking. , 1999, Gene.

[86]  D. Ausiello,et al.  Intra-endosomal pH-sensitive Recruitment of the Arf-nucleotide Exchange Factor ARNO and Arf6 from Cytoplasm to Proximal Tubule Endosomes* , 2001, The Journal of Biological Chemistry.

[87]  V. Puri,et al.  Membrane Traffic in Sphingolipid Storage Diseases , 2000, Traffic.

[88]  V. Gerke,et al.  The subcellular distribution of early endosomes is affected by the annexin II2p11(2) complex , 1993, The Journal of cell biology.

[89]  D. Hall,et al.  Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling , 2001, Nature Cell Biology.

[90]  Linda Hicke,et al.  Ubiquitin and proteasomes: Protein regulation by monoubiquitin , 2001, Nature Reviews Molecular Cell Biology.

[91]  K. von Figura,et al.  μ1A‐adaptin‐deficient mice: lethality, loss of AP‐1 binding and rerouting of mannose 6‐phosphate receptors , 2000, The EMBO journal.

[92]  K. Mostov,et al.  Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes , 1994, The Journal of cell biology.

[93]  I. Mellman,et al.  Developmental Regulation of Invariant Chain Proteolysis Controls MHC Class II Trafficking in Mouse Dendritic Cells , 1998, Cell.

[94]  L. Traub,et al.  Sorting in the endosomal system in yeast and animal cells. , 2000, Current opinion in cell biology.

[95]  H. Geuze,et al.  A novel class of clathrin-coated vesicles budding from endosomes , 1996, The Journal of cell biology.

[96]  A. Dierich,et al.  The Steroidogenic Acute Regulatory Protein Homolog MLN64, a Late Endosomal Cholesterol-binding Protein* , 2001, The Journal of Biological Chemistry.

[97]  W. Fischer,et al.  Novel stereoconfiguration in lyso-bis-phosphatidic acid of cultured BHK-cells. , 1974, Chemistry and physics of lipids.

[98]  P. De Camilli,et al.  Tetanus toxin-mediated cleavage of cellubrevin impairs exocytosis of transferrin receptor-containing vesicles in CHO cells , 1994, The Journal of cell biology.

[99]  J. Trowsdale,et al.  Accumulation of HLA-DM, a regulator of antigen presentation, in MHC class II compartments. , 1994, Science.

[100]  S. Mayor,et al.  Cholesterol‐dependent retention of GPI‐anchored proteins in endosomes , 1998, The EMBO journal.

[101]  R. Kurten,et al.  Enhanced Degradation of EGF Receptors by a Sorting Nexin, SNX1 , 1996, Science.

[102]  Toshihide Kobayashi,et al.  Localization of Lysobisphosphatidic Acid-Rich Membrane Domains in Late Endosomes , 2001, Biological chemistry.

[103]  Barbara J. Reaves,et al.  Loss of cation-independent mannose 6-phosphate receptor expression promotes the accumulation of lysobisphosphatidic acid in multilamellar bodies. , 2000, Journal of cell science.

[104]  Ira Mellman,et al.  The Receptor Recycling Pathway Contains Two Distinct Populations of Early Endosomes with Different Sorting Functions , 1999, The Journal of cell biology.

[105]  L. Van Aelst,et al.  A role for POR1, a Rac1‐interacting protein, in ARF6‐mediated cytoskeletal rearrangements , 1997, The EMBO journal.

[106]  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.

[107]  J. Gruenberg,et al.  Endocytosis and signaling cascades: a close encounter , 2001, FEBS letters.

[108]  S. Emr,et al.  Mammalian Tumor Susceptibility Gene 101 (TSG101) and the Yeast Homologue, Vps23p, Both Function in Late Endosomal Trafficking , 2000, Traffic.

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

[110]  R. Parton,et al.  Axonal and dendritic endocytic pathways in cultured neurons. , 1992 .

[111]  M. Zerial,et al.  Rabenosyn-5, a Novel Rab5 Effector, Is Complexed with Hvps45 and Recruited to Endosomes through a Fyve Finger Domain , 2000, The Journal of cell biology.

[112]  Y. Le Marchand-Brustel,et al.  A FYVE-finger-containing protein, Rabip4, is a Rab4 effector involved in early endosomal traffic. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[113]  M. Lindsay,et al.  Interaction of anti-phospholipid antibodies with late endosomes of human endothelial cells. , 1999, Arteriosclerosis, thrombosis, and vascular biology.

[114]  N. Kitamura,et al.  Early Endosomal Localization of Hrs Requires a Sequence within the Proline- and Glutamine-rich Region but Not the FYVE Finger* , 2000, The Journal of Biological Chemistry.

[115]  F. Maxfield,et al.  Iterative fractionation of recycling receptors from lysosomally destined ligands in an early sorting endosome , 1989, The Journal of cell biology.

[116]  S. Emr,et al.  The role of phosphoinositides in membrane transport. , 2001, Current opinion in cell biology.

[117]  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.

[118]  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.

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

[120]  Jean Gruenberg,et al.  Nef-Induced CD4 Degradation A Diacidic-Based Motif in Nef Functions as a Lysosomal Targeting Signal through the Binding of β-COP in Endosomes , 1999, Cell.

[121]  C. Carlin,et al.  EGF receptor residues Leu679, Leu680 mediate selective sorting of ligand‐receptor complexes in early endosomal compartments , 2000, Journal of cellular physiology.

[122]  Scott D. Emr,et al.  A Membrane Coat Complex Essential for Endosome-to-Golgi Retrograde Transport in Yeast , 1998, The Journal of cell biology.

[123]  S. Pfeffer,et al.  Membrane transport: Retromer to the rescue , 2001, Current Biology.

[124]  P. L. Campbell,et al.  EEA1, an Early Endosome-Associated Protein. , 1995, The Journal of Biological Chemistry.

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

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

[127]  B. Tycko,et al.  Segregation of transferrin to a mildly acidic (pH 6.5) para-golgi compartment in the recycling pathway , 1984, Cell.

[128]  S. Grinstein,et al.  Role of COPI in Phagosome Maturation* , 2000, The Journal of Biological Chemistry.

[129]  F. Gu,et al.  ARF1 Regulates pH-dependent COP Functions in the Early Endocytic Pathway* , 2000, The Journal of Biological Chemistry.

[130]  F. Gu,et al.  Lipids, lipid domains and lipid-protein interactions in endocytic membrane traffic. , 1998, Seminars in cell & developmental biology.