Identification of discrete classes of endosome-derived small vesicles as a major cellular pool for recycling membrane proteins
Vesicles carrying recycling plasma membrane proteins from early endosomes have not yet been characterized. Using Chinese hamster ovary cells transfected with the facilitative glucose transporter, GLUT4, we identified two classes of discrete, yet similarly sized, small vesicles that are derived from...
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Veröffentlicht in: | Molecular biology of the cell 2001-04, Vol.12 (4), p.981-995 |
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description | Vesicles carrying recycling plasma membrane proteins from early endosomes have not yet been characterized. Using Chinese hamster ovary cells transfected with the facilitative glucose transporter, GLUT4, we identified two classes of discrete, yet similarly sized, small vesicles that are derived from early endosomes. We refer to these postendosomal vesicles as endocytic small vesicles or ESVs. One class of ESVs contains a sizable fraction of the pool of the transferrin receptor, and the other contains 40% of the total cellular pool of GLUT4 and is enriched in the insulin-responsive aminopeptidase (IRAP). The ESVs contain cellubrevin and Rab4 but are lacking other early endosomal markers, such as EEA1 or syntaxin13. The ATP-, temperature-, and cytosol-dependent formation of ESVs has been reconstituted in vitro from endosomal membranes. Guanosine 5'-[gamma-thio]triphosphate and neomycin, but not brefeldin A, inhibit budding of the ESVs in vitro. A monoclonal antibody recognizing the GLUT4 cytoplasmic tail perturbs the in vitro targeting of GLUT4 to the ESVs without interfering with the incorporation of IRAP or TfR. We suggest that cytosolic proteins mediate the incorporation of recycling membrane proteins into discrete populations of ESVs that serve as carrier vesicles to store and then transport the cargo from early endosomes, either directly or indirectly, to the cell surface. |
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Using Chinese hamster ovary cells transfected with the facilitative glucose transporter, GLUT4, we identified two classes of discrete, yet similarly sized, small vesicles that are derived from early endosomes. We refer to these postendosomal vesicles as endocytic small vesicles or ESVs. One class of ESVs contains a sizable fraction of the pool of the transferrin receptor, and the other contains 40% of the total cellular pool of GLUT4 and is enriched in the insulin-responsive aminopeptidase (IRAP). The ESVs contain cellubrevin and Rab4 but are lacking other early endosomal markers, such as EEA1 or syntaxin13. The ATP-, temperature-, and cytosol-dependent formation of ESVs has been reconstituted in vitro from endosomal membranes. Guanosine 5'-[gamma-thio]triphosphate and neomycin, but not brefeldin A, inhibit budding of the ESVs in vitro. A monoclonal antibody recognizing the GLUT4 cytoplasmic tail perturbs the in vitro targeting of GLUT4 to the ESVs without interfering with the incorporation of IRAP or TfR. We suggest that cytosolic proteins mediate the incorporation of recycling membrane proteins into discrete populations of ESVs that serve as carrier vesicles to store and then transport the cargo from early endosomes, either directly or indirectly, to the cell surface.</description><identifier>ISSN: 1059-1524</identifier><identifier>EISSN: 1939-4586</identifier><identifier>DOI: 10.1091/mbc.12.4.981</identifier><identifier>PMID: 11294901</identifier><language>eng</language><publisher>United States: The American Society for Cell Biology</publisher><subject>Aminopeptidases - metabolism ; Animals ; Brefeldin A - pharmacology ; Cell-Free System ; CHO Cells ; Cricetinae ; Cystinyl Aminopeptidase ; Endocytosis - physiology ; Endosomes - metabolism ; Endosomes - physiology ; Glucose Transporter Type 4 ; GTP Phosphohydrolases - metabolism ; Membrane Proteins - metabolism ; Monosaccharide Transport Proteins - genetics ; Monosaccharide Transport Proteins - metabolism ; Muscle Proteins ; Neomycin - pharmacology ; Protein Synthesis Inhibitors - pharmacology ; Transferrin - metabolism ; Vesicle-Associated Membrane Protein 3</subject><ispartof>Molecular biology of the cell, 2001-04, Vol.12 (4), p.981-995</ispartof><rights>Copyright © 2001, The American Society for Cell Biology 2001</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c408t-9dff67034e2a4b67e6929f55f806ab9f18fdf3bbfe381214e576d128c28931863</citedby><cites>FETCH-LOGICAL-c408t-9dff67034e2a4b67e6929f55f806ab9f18fdf3bbfe381214e576d128c28931863</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC32281/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC32281/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/11294901$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Pfeffer, Suzanne R.</contributor><creatorcontrib>Lim, S N</creatorcontrib><creatorcontrib>Bonzelius, F</creatorcontrib><creatorcontrib>Low, S H</creatorcontrib><creatorcontrib>Wille, H</creatorcontrib><creatorcontrib>Weimbs, T</creatorcontrib><creatorcontrib>Herman, G A</creatorcontrib><title>Identification of discrete classes of endosome-derived small vesicles as a major cellular pool for recycling membrane proteins</title><title>Molecular biology of the cell</title><addtitle>Mol Biol Cell</addtitle><description>Vesicles carrying recycling plasma membrane proteins from early endosomes have not yet been characterized. Using Chinese hamster ovary cells transfected with the facilitative glucose transporter, GLUT4, we identified two classes of discrete, yet similarly sized, small vesicles that are derived from early endosomes. We refer to these postendosomal vesicles as endocytic small vesicles or ESVs. One class of ESVs contains a sizable fraction of the pool of the transferrin receptor, and the other contains 40% of the total cellular pool of GLUT4 and is enriched in the insulin-responsive aminopeptidase (IRAP). The ESVs contain cellubrevin and Rab4 but are lacking other early endosomal markers, such as EEA1 or syntaxin13. The ATP-, temperature-, and cytosol-dependent formation of ESVs has been reconstituted in vitro from endosomal membranes. Guanosine 5'-[gamma-thio]triphosphate and neomycin, but not brefeldin A, inhibit budding of the ESVs in vitro. A monoclonal antibody recognizing the GLUT4 cytoplasmic tail perturbs the in vitro targeting of GLUT4 to the ESVs without interfering with the incorporation of IRAP or TfR. We suggest that cytosolic proteins mediate the incorporation of recycling membrane proteins into discrete populations of ESVs that serve as carrier vesicles to store and then transport the cargo from early endosomes, either directly or indirectly, to the cell surface.</description><subject>Aminopeptidases - metabolism</subject><subject>Animals</subject><subject>Brefeldin A - pharmacology</subject><subject>Cell-Free System</subject><subject>CHO Cells</subject><subject>Cricetinae</subject><subject>Cystinyl Aminopeptidase</subject><subject>Endocytosis - physiology</subject><subject>Endosomes - metabolism</subject><subject>Endosomes - physiology</subject><subject>Glucose Transporter Type 4</subject><subject>GTP Phosphohydrolases - metabolism</subject><subject>Membrane Proteins - metabolism</subject><subject>Monosaccharide Transport Proteins - genetics</subject><subject>Monosaccharide Transport Proteins - metabolism</subject><subject>Muscle Proteins</subject><subject>Neomycin - pharmacology</subject><subject>Protein Synthesis Inhibitors - pharmacology</subject><subject>Transferrin - metabolism</subject><subject>Vesicle-Associated Membrane Protein 3</subject><issn>1059-1524</issn><issn>1939-4586</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2001</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVUUuLFDEQDqK46-rNs-TkyR5TSbo7AS-y-FhY8KLnkE4qa5akMyY9A3vxt5t1Bx9QUEXVV4-vPkJeAtsB0_A2L24HfCd3WsEjcg5a6EGOanrcYzbqAUYuz8iz1m4ZAymn-Sk5A-Baagbn5OeVx3WLITq7xbLSEqiPzVXckLpkW8N2n8PVl1YyDh5rPKKnLduU6BFbdKlDbDea7W2p1GFKh2Qr3ZeSaOiZiu7Opbje0Ix5qXZFuq9lw7i25-RJsKnhi5O_IN8-fvh6-Xm4_vLp6vL99eAkU9ugfQjTzIREbuUyzThprsM4BsUmu-gAKvggliWgUMBB4jhPHrhyXGkBahIX5N3D3P1hyehd51xtMvsas613ptho_q-s8bu5KUcjOFfQ21-f2mv5ccC2mdyf1Il2LuXQzDwz2V8rOvDNA9DV0lrF8GcFMHMvl-lyGeBGGv177qt_z_oLPukjfgHWo5Tp</recordid><startdate>20010401</startdate><enddate>20010401</enddate><creator>Lim, S N</creator><creator>Bonzelius, F</creator><creator>Low, S H</creator><creator>Wille, H</creator><creator>Weimbs, T</creator><creator>Herman, G A</creator><general>The American Society for Cell Biology</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20010401</creationdate><title>Identification of discrete classes of endosome-derived small vesicles as a major cellular pool for recycling membrane proteins</title><author>Lim, S N ; Bonzelius, F ; Low, S H ; Wille, H ; Weimbs, T ; Herman, G A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c408t-9dff67034e2a4b67e6929f55f806ab9f18fdf3bbfe381214e576d128c28931863</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2001</creationdate><topic>Aminopeptidases - metabolism</topic><topic>Animals</topic><topic>Brefeldin A - pharmacology</topic><topic>Cell-Free System</topic><topic>CHO Cells</topic><topic>Cricetinae</topic><topic>Cystinyl Aminopeptidase</topic><topic>Endocytosis - physiology</topic><topic>Endosomes - metabolism</topic><topic>Endosomes - physiology</topic><topic>Glucose Transporter Type 4</topic><topic>GTP Phosphohydrolases - metabolism</topic><topic>Membrane Proteins - metabolism</topic><topic>Monosaccharide Transport Proteins - genetics</topic><topic>Monosaccharide Transport Proteins - metabolism</topic><topic>Muscle Proteins</topic><topic>Neomycin - pharmacology</topic><topic>Protein Synthesis Inhibitors - pharmacology</topic><topic>Transferrin - metabolism</topic><topic>Vesicle-Associated Membrane Protein 3</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lim, S N</creatorcontrib><creatorcontrib>Bonzelius, F</creatorcontrib><creatorcontrib>Low, S H</creatorcontrib><creatorcontrib>Wille, H</creatorcontrib><creatorcontrib>Weimbs, T</creatorcontrib><creatorcontrib>Herman, G A</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular biology of the cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lim, S N</au><au>Bonzelius, F</au><au>Low, S H</au><au>Wille, H</au><au>Weimbs, T</au><au>Herman, G A</au><au>Pfeffer, Suzanne R.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Identification of discrete classes of endosome-derived small vesicles as a major cellular pool for recycling membrane proteins</atitle><jtitle>Molecular biology of the cell</jtitle><addtitle>Mol Biol Cell</addtitle><date>2001-04-01</date><risdate>2001</risdate><volume>12</volume><issue>4</issue><spage>981</spage><epage>995</epage><pages>981-995</pages><issn>1059-1524</issn><eissn>1939-4586</eissn><abstract>Vesicles carrying recycling plasma membrane proteins from early endosomes have not yet been characterized. Using Chinese hamster ovary cells transfected with the facilitative glucose transporter, GLUT4, we identified two classes of discrete, yet similarly sized, small vesicles that are derived from early endosomes. We refer to these postendosomal vesicles as endocytic small vesicles or ESVs. One class of ESVs contains a sizable fraction of the pool of the transferrin receptor, and the other contains 40% of the total cellular pool of GLUT4 and is enriched in the insulin-responsive aminopeptidase (IRAP). The ESVs contain cellubrevin and Rab4 but are lacking other early endosomal markers, such as EEA1 or syntaxin13. The ATP-, temperature-, and cytosol-dependent formation of ESVs has been reconstituted in vitro from endosomal membranes. Guanosine 5'-[gamma-thio]triphosphate and neomycin, but not brefeldin A, inhibit budding of the ESVs in vitro. A monoclonal antibody recognizing the GLUT4 cytoplasmic tail perturbs the in vitro targeting of GLUT4 to the ESVs without interfering with the incorporation of IRAP or TfR. We suggest that cytosolic proteins mediate the incorporation of recycling membrane proteins into discrete populations of ESVs that serve as carrier vesicles to store and then transport the cargo from early endosomes, either directly or indirectly, to the cell surface.</abstract><cop>United States</cop><pub>The American Society for Cell Biology</pub><pmid>11294901</pmid><doi>10.1091/mbc.12.4.981</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Aminopeptidases - metabolism Animals Brefeldin A - pharmacology Cell-Free System CHO Cells Cricetinae Cystinyl Aminopeptidase Endocytosis - physiology Endosomes - metabolism Endosomes - physiology Glucose Transporter Type 4 GTP Phosphohydrolases - metabolism Membrane Proteins - metabolism Monosaccharide Transport Proteins - genetics Monosaccharide Transport Proteins - metabolism Muscle Proteins Neomycin - pharmacology Protein Synthesis Inhibitors - pharmacology Transferrin - metabolism Vesicle-Associated Membrane Protein 3 |
title | Identification of discrete classes of endosome-derived small vesicles as a major cellular pool for recycling membrane proteins |
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