![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
|
|
|
|
|
||
Vol. 11, Issue 8, 2775-2791, August 2000
*Department of Biochemistry, University of Geneva, 1211 Geneva 4, Switzerland; We present a biochemical and morphological characterization of
recycling endosomes containing the transferrin receptor in the
epithelial Madin-Darby canine kidney cell line. We find that recycling
endosomes are enriched in molecules known to regulate transferrin
recycling but lack proteins involved in early endosome membrane
dynamics, indicating that recycling endosomes are distinct from
conventional early endosomes. We also find that recycling endosomes are
less acidic than early endosomes because they lack a functional
vacuolar ATPase. Furthermore, we show that recycling endosomes can be
reached by apically internalized tracers, confirming that the apical
endocytic pathway intersects the transferrin pathway. Strikingly,
recycling endosomes are enriched in the raft lipids sphingomyelin and
cholesterol as well as in the raft-associated proteins caveolin-1 and
flotillin-1. These observations may suggest that a lipid-based sorting
mechanism operates along the Madin-Darby canine kidney recycling
pathway, contributing to the maintenance of cell polarity. Altogether,
our data indicate that recycling endosomes and early endosomes differ
functionally and biochemically and thus that different molecular
mechanisms regulate protein sorting and membrane traffic at each step
of the receptor recycling pathway.
Department of Physiology, Centre
Médical Universitaire, 1211 Geneva 4, Switzerland;
Centre for Microscopy and Microanalysis, Department of
Physiology and Pharmacology, and Centre for Molecular and Cellular
Biology, University of Queensland, Queensland 4072, Australia;
§Institute of Biochemistry, University of Lausanne,
Lausanne, Switzerland; and ¶Research Institute of
Molecular Pathology, Wien, Austria
Present address: Institute of
Molecular and Cell Biology, National University of Singapore, Singapore
117609, Republic of Singapore.
**
Corresponding author. E-mail address:
jean.gruenberg{at}biochem.unige.ch.
This article has been cited by other articles:
|
|
 |
|
  A. Francesconi, R. Kumari, and R. S. Zukin Regulation of Group I Metabotropic Glutamate Receptor Trafficking and Signaling by the Caveolar/Lipid Raft Pathway J. Neurosci., March 18, 2009; 29(11): 3590 - 3602. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Ferrari, A. Veligodskiy, U. Berge, M. S. Lucas, and R. Kroschewski ROCK-mediated contractility, tight junctions and channels contribute to the conversion of a preapical patch into apical surface during isochoric lumen initiation J. Cell Sci., November 1, 2008; 121(21): 3649 - 3663. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. H. Petersen, N. J. Faergeman, L. Yu, and D. Wustner Kinetic imaging of NPC1L1 and sterol trafficking between plasma membrane and recycling endosomes in hepatoma cells J. Lipid Res., September 1, 2008; 49(9): 2023 - 2037. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. P. Manderson, J. G. Kay, L. A. Hammond, D. L. Brown, and J. L. Stow Subcompartments of the macrophage recycling endosome direct the differential secretion of IL-6 and TNF{alpha} J. Cell Biol., October 3, 2007; 178(1): 57 - 69. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Leyt, N. Melamed-Book, J.-P. Vaerman, S. Cohen, A. M. Weiss, and B. Aroeti Cholesterol-sensitive Modulation of Transcytosis Mol. Biol. Cell, June 1, 2007; 18(6): 2057 - 2071. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. P. Bliss, A. M. Navratil, M. Breed, D. C. Skinner, C. M. Clay, and M. S. Roberson Signaling Complexes Associated with the Type I Gonadotropin-Releasing Hormone (GnRH) Receptor: Colocalization of Extracellularly Regulated Kinase 2 and GnRH Receptor within Membrane Rafts Mol. Endocrinol., February 1, 2007; 21(2): 538 - 549. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Michihara, K. Toda, M. Suenobu, K. Akasaki, and H. Tsuji Decrease of Cholesterol in Mouse Melanoma Causes Secretion of Lysosomal Enzymes J. Biochem., February 1, 2007; 141(2): 239 - 250. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. K. Muller, O. Wiborg, and J. Haase Subcellular Redistribution of the Serotonin Transporter by Secretory Carrier Membrane Protein 2 J. Biol. Chem., September 29, 2006; 281(39): 28901 - 28909. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. M. Palermo, S. L. Hafenstein, and C. R. Parrish Purified feline and canine transferrin receptors reveal complex interactions with the capsids of canine and feline parvoviruses that correspond to their host ranges. J. Virol., September 1, 2006; 80(17): 8482 - 8492. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Liebl, F. Difato, L. Hornikova, P. Mannova, J. Stokrova, and J. Forstova Mouse Polyomavirus Enters Early Endosomes, Requires Their Acidic pH for Productive Infection, and Meets Transferrin Cargo in Rab11-Positive Endosomes J. Virol., May 1, 2006; 80(9): 4610 - 4622. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. Hua, D. Sheff, D. Toomre, and I. Mellman Vectorial insertion of apical and basolateral membrane proteins in polarized epithelial cells revealed by quantitative 3D live cell imaging. J. Cell Biol., March 27, 2006; 172(7): 1035 - 1044. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. C.-H. Chen, P. J. Schweinsberg, S. Vashist, D. P. Mareiniss, E. J. Lambie, and B. D. Grant RAB-10 Is Required for Endocytic Recycling in the Caenorhabditis elegans Intestine Mol. Biol. Cell, March 1, 2006; 17(3): 1286 - 1297. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Ishikawa, Z. Yuan, N. Inoue, M. T. Skowronski, Y. Nakae, M. Shono, G. Cho, M. Yasui, P. Agre, and S. Nielsen Identification of AQP5 in lipid rafts and its translocation to apical membranes by activation of M3 mAChRs in interlobular ducts of rat parotid gland Am J Physiol Cell Physiol, November 1, 2005; 289(5): C1303 - C1311. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. Churchward, T. Rogasevskaia, J. Hofgen, J. Bau, and J. R. Coorssen Cholesterol facilitates the native mechanism of Ca2+-triggered membrane fusion J. Cell Sci., October 15, 2005; 118(20): 4833 - 4848. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Pol, S. Martin, M. A. Fernandez, M. Ingelmo-Torres, C. Ferguson, C. Enrich, and R. G. Parton Cholesterol and Fatty Acids Regulate Dynamic Caveolin Trafficking through the Golgi Complex and between the Cell Surface and Lipid Bodies Mol. Biol. Cell, April 1, 2005; 16(4): 2091 - 2105. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Mielenz, C. Vettermann, M. Hampel, C. Lang, A. Avramidou, M. Karas, and H.-M. Jack Lipid Rafts Associate with Intracellular B Cell Receptors and Exhibit a B Cell Stage-Specific Protein Composition J. Immunol., March 15, 2005; 174(6): 3508 - 3517. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. A. Spencer, P. Wang, D. Li, J. S. Russel, D. H. Blank, J. Huuskonen, P. E. Fielding, and C. J. Fielding Benzophenone-containing cholesterol surrogates: synthesis and biological evaluation J. Lipid Res., August 1, 2004; 45(8): 1510 - 1518. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Naslavsky, R. Weigert, and J. G. Donaldson Characterization of a Nonclathrin Endocytic Pathway: Membrane Cargo and Lipid Requirements Mol. Biol. Cell, August 1, 2004; 15(8): 3542 - 3552. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Rhainds, P. Bourgeois, G. Bourret, K. Huard, L. Falstrault, and L. Brissette Localization and regulation of SR-BI in membrane rafts of HepG2 cells J. Cell Sci., July 1, 2004; 117(15): 3095 - 3105. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. E. Soccio and J. L. Breslow Intracellular Cholesterol Transport Arterioscler. Thromb. Vasc. Biol., July 1, 2004; 24(7): 1150 - 1160. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. t. Vruchte, E. Lloyd-Evans, R. J. Veldman, D. C. A. Neville, R. A. Dwek, F. M. Platt, W. J. van Blitterswijk, and D. J. Sillence Accumulation of Glycosphingolipids in Niemann-Pick C Disease Disrupts Endosomal Transport J. Biol. Chem., June 18, 2004; 279(25): 26167 - 26175. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Hueffer, L. M. Palermo, and C. R. Parrish Parvovirus Infection of Cells by Using Variants of the Feline Transferrin Receptor Altering Clathrin-Mediated Endocytosis, Membrane Domain Localization, and Capsid-Binding Domains J. Virol., June 1, 2004; 78(11): 5601 - 5611. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Hoekstra, D. Tyteca, and S. C. D. van IJzendoorn The subapical compartment: a traffic center in membrane polarity development J. Cell Sci., May 1, 2004; 117(11): 2183 - 2192. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. V. Burgos, C. Klattenhoff, E. de la Fuente, A. Rigotti, and A. Gonzalez Cholesterol depletion induces PKA-mediated basolateral-to-apical transcytosis of the scavenger receptor class B type I in MDCK cells PNAS, March 16, 2004; 101(11): 3845 - 3850. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Sharma, F. Pampinella, C. Nemes, M. Benharouga, J. So, K. Du, K. G. Bache, B. Papsin, N. Zerangue, H. Stenmark, et al. Misfolding diverts CFTR from recycling to degradation: quality control at early endosomes J. Cell Biol., March 15, 2004; 164(6): 923 - 933. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. P. Dolan, T. P. Phelan, D. Ilkovitch, L. Qi, W. F. Wade, T. M. Laufer, and S. Ostrand-Rosenberg Invariant Chain and the MHC Class II Cytoplasmic Domains Regulate Localization of MHC Class II Molecules to Lipid Rafts in Tumor Cell-Based Vaccines J. Immunol., January 15, 2004; 172(2): 907 - 914. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Singh, D. Charkowicz, and D. Mascarenhas Insulin-like Growth Factor-independent Effects Mediated by a C-terminal Metal-binding Domain of Insulin-like Growth Factor Binding Protein-3 J. Biol. Chem., January 2, 2004; 279(1): 477 - 487. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. G. Panchal, G. Ruthel, T. A. Kenny, G. H. Kallstrom, D. Lane, S. S. Badie, L. Li, S. Bavari, and M. J. Aman In vivo oligomerization and raft localization of Ebola virus protein VP40 during vesicular budding PNAS, December 23, 2003; 100(26): 15936 - 15941. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. de Gassart, C. Geminard, B. Fevrier, G. Raposo, and M. Vidal Lipid raft-associated protein sorting in exosomes Blood, December 15, 2003; 102(13): 4336 - 4344. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. L. TUMA and A. L. HUBBARD Transcytosis: Crossing Cellular Barriers Physiol Rev, July 1, 2003; 83(3): 871 - 932. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. K. Nyasae, A. L. Hubbard, and P. L. Tuma Transcytotic Efflux from Early Endosomes Is Dependent on Cholesterol and Glycosphingolipids in Polarized Hepatic Cells Mol. Biol. Cell, July 1, 2003; 14(7): 2689 - 2705. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. A. Huber, K. Pfaller, and I. Vietor Organelle Proteomics: Implications for Subcellular Fractionation in Proteomics Circ. Res., May 16, 2003; 92(9): 962 - 968. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. P. Souto, G. Vallega, J. Wharton, J. Vinten, J. Tranum-Jensen, and P. F. Pilch Immunopurification and Characterization of Rat Adipocyte Caveolae Suggest Their Dissociation from Insulin Signaling J. Biol. Chem., May 9, 2003; 278(20): 18321 - 18329. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Hoekstra, O. Maier, J. M. van der Wouden, T. A. Slimane, and S. C. D. van IJzendoorn Membrane dynamics and cell polarity: the role of sphingolipids J. Lipid Res., May 1, 2003; 44(5): 869 - 877. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Duclos, R. Corsini, and M. Desjardins Remodeling of endosomes during lysosome biogenesis involves `kiss and run' fusion events regulated by rab5 J. Cell Sci., March 1, 2003; 116(5): 907 - 918. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Chroni, T. Liu, I. Gorshkova, H.-Y. Kan, Y. Uehara, A. von Eckardstein, and V. I. Zannis The Central Helices of ApoA-I Can Promote ATP-binding Cassette Transporter A1 (ABCA1)-mediated Lipid Efflux. AMINO ACID RESIDUES 220-231 OF THE WILD-TYPE ApoA-I ARE REQUIRED FOR LIPID EFFLUX IN VITRO AND HIGH DENSITY LIPOPROTEIN FORMATION IN VIVO J. Biol. Chem., February 21, 2003; 278(9): 6719 - 6730. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Otsuki, T. Itoh, and T. Takenawa Neural Wiskott-Aldrich Syndrome Protein Is Recruited to Rafts and Associates with Endophilin A in Response to Epidermal Growth Factor J. Biol. Chem., February 14, 2003; 278(8): 6461 - 6469. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Mannova and J. Forstova Mouse Polyomavirus Utilizes Recycling Endosomes for a Traffic Pathway Independent of COPI Vesicle Transport J. Virol., February 1, 2003; 77(3): 1672 - 1681. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Narayan, R. J. O. Barnard, and J. A. T. Young Two Retroviral Entry Pathways Distinguished by Lipid Raft Association of the Viral Receptor and Differences in Viral Infectivity J. Virol., February 1, 2003; 77(3): 1977 - 1983. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. A. Slimane, G. Trugnan, S. C.D. van IJzendoorn, and D. Hoekstra Raft-mediated Trafficking of Apical Resident Proteins Occurs in Both Direct and Transcytotic Pathways in Polarized Hepatic Cells: Role of Distinct Lipid Microdomains Mol. Biol. Cell, February 1, 2003; 14(2): 611 - 624. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
O. Maier and D. Hoekstra Trans-Golgi Network and Subapical Compartment of HepG2 Cells Display Different Properties in Sorting and Exiting of Sphingolipids J. Biol. Chem., January 3, 2003; 278(1): 164 - 173. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. I. Mundy, T. Machleidt, Y.-s. Ying, R. G. W. Anderson, and G. S. Bloom Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton J. Cell Sci., November 15, 2002; 115(22): 4327 - 4339. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. H. van der Luit, M. Budde, P. Ruurs, M. Verheij, and W. J. van Blitterswijk Alkyl-lysophospholipid Accumulates in Lipid Rafts and Induces Apoptosis via Raft-dependent Endocytosis and Inhibition of Phosphatidylcholine Synthesis J. Biol. Chem., October 11, 2002; 277(42): 39541 - 39547. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Holtta-Vuori, K. Tanhuanpaa, W. Mobius, P. Somerharju, and E. Ikonen Modulation of Cellular Cholesterol Transport and Homeostasis by Rab11 Mol. Biol. Cell, September 1, 2002; 13(9): 3107 - 3122. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Kobayashi, M.-H. Beuchat, J. Chevallier, A. Makino, N. Mayran, J.-M. Escola, C. Lebrand, P. Cosson, T. Kobayashi, and J. Gruenberg Separation and Characterization of Late Endosomal Membrane Domains J. Biol. Chem., August 23, 2002; 277(35): 32157 - 32164. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Wustner, A. Herrmann, M. Hao, and F. R. Maxfield Rapid Nonvesicular Transport of Sterol between the Plasma Membrane Domains of Polarized Hepatic Cells J. Biol. Chem., August 9, 2002; 277(33): 30325 - 30336. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Mairhofer, M. Steiner, W. Mosgoeller, R. Prohaska, and U. Salzer Stomatin is a major lipid-raft component of platelet alpha granules Blood, July 18, 2002; 100(3): 897 - 904. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. van Meer and Q. Lisman Sphingolipid Transport: Rafts and Translocators J. Biol. Chem., July 12, 2002; 277(29): 25855 - 25858. [Full Text] [PDF]
|
|
|
|
|
|
M. Simons, E.-M. Kramer, P. Macchi, S. Rathke-Hartlieb, J. Trotter, K.-A. Nave, and J. B. Schulz Overexpression of the myelin proteolipid protein leads to accumulation of cholesterol and proteolipid protein in endosomes/lysosomes: implications for Pelizaeus-Merzbacher disease J. Cell Biol., April 15, 2002; 157(2): 327 - 336. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. Gerke and S. E. Moss Annexins: From Structure to Function Physiol Rev, April 1, 2002; 82(2): 331 - 371. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Mohrmann, R. Leijendekker, L. Gerez, and P. van der Sluijs rab4 Regulates Transport to the Apical Plasma Membrane in Madin-Darby Canine Kidney Cells J. Biol. Chem., March 15, 2002; 277(12): 10474 - 10481. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. Alonso and J. Millan The role of lipid rafts in signalling and membrane trafficking in T lymphocytes J. Cell Sci., March 13, 2002; 114(22): 3957 - 3965. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Kolesnikova, H. Bugany, H.-D. Klenk, and S. Becker VP40, the Matrix Protein of Marburg Virus, Is Associated with Membranes of the Late Endosomal Compartment J. Virol., February 15, 2002; 76(4): 1825 - 1838. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. Demaurex pH Homeostasis of Cellular Organelles Physiology, February 1, 2002; 17(1): 1 - 5. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Lange, J. Ye, M. Rigney, and T. L. Steck Dynamics of lysosomal cholesterol in Niemann-Pick type C and normal human fibroblasts J. Lipid Res., February 1, 2002; 43(2): 198 - 204. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 X. Li, T. Galli, S. Leu, J. B Wade, E. J Weinman, G. Leung, A. Cheong, D. Louvard, and M. Donowitz Na+-H+ exchanger 3 (NHE3) is present in lipid rafts in the rabbit ileal brush border: a role for rafts in trafficking and rapid stimulation of NHE3 J. Physiol., December 1, 2001; 537(2): 537 - 552. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Falguieres, F. Mallard, C. Baron, D. Hanau, C. Lingwood, B. Goud, J. Salamero, and L. Johannes Targeting of Shiga Toxin B-Subunit to Retrograde Transport Route in Association with Detergent-resistant Membranes Mol. Biol. Cell, August 1, 2001; 12(8): 2453 - 2468. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Puertollano, J. A. Martinez-Menarguez, A. Batista, J. Ballesta, and M. A. Alonso An Intact Dilysine-like Motif in the Carboxyl Terminus of MAL Is Required for Normal Apical Transport of the Influenza Virus Hemagglutinin Cargo Protein in Epithelial Madin-Darby Canine Kidney Cells Mol. Biol. Cell, June 1, 2001; 12(6): 1869 - 1883. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Pol, R. Luetterforst, M. Lindsay, S. Heino, E. Ikonen, and R. G. Parton A Caveolin Dominant Negative Mutant Associates with Lipid Bodies and Induces Intracellular Cholesterol Imbalance J. Cell Biol., March 5, 2001; 152(5): 1057 - 1070. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S Lusa, T. Blom, E. Eskelinen, E Kuismanen, J. Mansson, K Simons, and E Ikonen Depletion of rafts in late endocytic membranes is controlled by NPC1-dependent recycling of cholesterol to the plasma membrane J. Cell Sci., January 5, 2001; 114(10): 1893 - 1900. [Abstract] [PDF]
|
|
|
|
|
|
H. Shogomori and A. H. Futerman Cholera Toxin Is Found in Detergent-insoluble Rafts/Domains at the Cell Surface of Hippocampal Neurons but Is Internalized via a Raft-independent Mechanism J. Biol. Chem., March 16, 2001; 276(12): 9182 - 9188. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Simons, E.-M. Kramer, P. Macchi, S. Rathke-Hartlieb, J. Trotter, K.-A. Nave, and J. B. Schulz Overexpression of the myelin proteolipid protein leads to accumulation of cholesterol and proteolipid protein in endosomes/lysosomes: implications for Pelizaeus-Merzbacher disease J. Cell Biol., April 15, 2002; 157(2): 327 - 336. [Abstract] [Full Text] [PDF]
|
|
