Translocation of nutrient transporters to cell membrane via Golgi bypass in Aspergillus nidulans
Nutrient transporters, being polytopic membrane proteins, are believed, but not formally shown, to traffic from their site of synthesis, the ER, to the plasma membrane through Golgi‐dependent vesicular trafficking. Here, we develop a novel genetic system to investigate the trafficking of a neosynthe...
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creator | Dimou, Sofia Martzoukou, Olga Dionysopoulou, Mariangela Bouris, Vangelis Amillis, Sotiris Diallinas, George |
description | Nutrient transporters, being polytopic membrane proteins, are believed, but not formally shown, to traffic from their site of synthesis, the ER, to the plasma membrane through Golgi‐dependent vesicular trafficking. Here, we develop a novel genetic system to investigate the trafficking of a neosynthesized model transporter, the well‐studied UapA purine transporter of
Aspergillus nidulans
. We show that sorting of neosynthesized UapA to the plasma membrane (PM) bypasses the Golgi and does not necessitate key Rab GTPases, AP adaptors, microtubules or endosomes. UapA PM localization is found to be dependent on functional COPII vesicles, actin polymerization, clathrin heavy chain and the PM t‐SNARE SsoA. Actin polymerization proved to primarily affect COPII vesicle formation, whereas the essential role of ClaH seems indirect and less clear. We provide evidence that other evolutionary and functionally distinct transporters of
A. nidulans
also follow the herein identified Golgi‐independent trafficking route of UapA. Importantly, our findings suggest that specific membrane cargoes drive the formation of distinct COPII subpopulations that bypass the Golgi to be sorted non‐polarly to the PM, and thus serving house‐keeping cell functions.
Synopsis
Nutrient transporter translocation to the cell membrane operates via a novel trafficking route that does not involve functioning of the Golgi in fungi.
Transporter translocation from the endoplasmic reticulum (ER) to the plasma membrane (PM) depends on COPII vesicle formation.
Golgi and known post‐Golgi secretory routes are non‐essential for transporter biogenesis.
The mechanisms regulating trafficking of nutrient transporters and apical cargoes are distinct.
Graphical Abstract
Nutrient transporter translocation to the cell membrane operates via a novel trafficking route that does not involve functioning of the Golgi in fungi. |
doi_str_mv | 10.15252/embr.201949929 |
format | Article |
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Aspergillus nidulans
. We show that sorting of neosynthesized UapA to the plasma membrane (PM) bypasses the Golgi and does not necessitate key Rab GTPases, AP adaptors, microtubules or endosomes. UapA PM localization is found to be dependent on functional COPII vesicles, actin polymerization, clathrin heavy chain and the PM t‐SNARE SsoA. Actin polymerization proved to primarily affect COPII vesicle formation, whereas the essential role of ClaH seems indirect and less clear. We provide evidence that other evolutionary and functionally distinct transporters of
A. nidulans
also follow the herein identified Golgi‐independent trafficking route of UapA. Importantly, our findings suggest that specific membrane cargoes drive the formation of distinct COPII subpopulations that bypass the Golgi to be sorted non‐polarly to the PM, and thus serving house‐keeping cell functions.
Synopsis
Nutrient transporter translocation to the cell membrane operates via a novel trafficking route that does not involve functioning of the Golgi in fungi.
Transporter translocation from the endoplasmic reticulum (ER) to the plasma membrane (PM) depends on COPII vesicle formation.
Golgi and known post‐Golgi secretory routes are non‐essential for transporter biogenesis.
The mechanisms regulating trafficking of nutrient transporters and apical cargoes are distinct.
Graphical Abstract
Nutrient transporter translocation to the cell membrane operates via a novel trafficking route that does not involve functioning of the Golgi in fungi.</description><identifier>ISSN: 1469-221X</identifier><identifier>EISSN: 1469-3178</identifier><identifier>DOI: 10.15252/embr.201949929</identifier><identifier>PMID: 32452614</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>Actin ; Adapters ; Aspergillus nidulans ; Aspergillus nidulans - genetics ; Cell Membrane ; Cell membranes ; Clathrin ; EMBO20 ; Endoplasmic reticulum ; Endosomes ; Fungal Proteins - genetics ; Fungi ; Golgi Apparatus ; Golgi cells ; Localization ; Membrane proteins ; Membranes ; Microtubules ; Nutrients ; polarity ; Polymerization ; secretion ; SNAP receptors ; Subpopulations ; traffic ; Trafficking ; Translocation</subject><ispartof>EMBO reports, 2020-07, Vol.21 (7), p.e49929-n/a</ispartof><rights>The Author(s) 2020</rights><rights>2020 The Authors</rights><rights>2020 The Authors.</rights><rights>2020 EMBO</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5139-f1d0183c36514ced2b5441e7a4ebb546554a84ba92a5735fadd0161573215da73</citedby><cites>FETCH-LOGICAL-c5139-f1d0183c36514ced2b5441e7a4ebb546554a84ba92a5735fadd0161573215da73</cites><orcidid>0000-0002-3426-726X ; 0000-0001-5445-484X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7332984/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7332984/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,1417,1433,27924,27925,41120,42189,45574,45575,46409,46833,51576,53791,53793</link.rule.ids><linktorsrc>$$Uhttps://doi.org/10.15252/embr.201949929$$EView_record_in_Springer_Nature$$FView_record_in_$$GSpringer_Nature</linktorsrc><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32452614$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Dimou, Sofia</creatorcontrib><creatorcontrib>Martzoukou, Olga</creatorcontrib><creatorcontrib>Dionysopoulou, Mariangela</creatorcontrib><creatorcontrib>Bouris, Vangelis</creatorcontrib><creatorcontrib>Amillis, Sotiris</creatorcontrib><creatorcontrib>Diallinas, George</creatorcontrib><title>Translocation of nutrient transporters to cell membrane via Golgi bypass in Aspergillus nidulans</title><title>EMBO reports</title><addtitle>EMBO Rep</addtitle><addtitle>EMBO Rep</addtitle><description>Nutrient transporters, being polytopic membrane proteins, are believed, but not formally shown, to traffic from their site of synthesis, the ER, to the plasma membrane through Golgi‐dependent vesicular trafficking. Here, we develop a novel genetic system to investigate the trafficking of a neosynthesized model transporter, the well‐studied UapA purine transporter of
Aspergillus nidulans
. We show that sorting of neosynthesized UapA to the plasma membrane (PM) bypasses the Golgi and does not necessitate key Rab GTPases, AP adaptors, microtubules or endosomes. UapA PM localization is found to be dependent on functional COPII vesicles, actin polymerization, clathrin heavy chain and the PM t‐SNARE SsoA. Actin polymerization proved to primarily affect COPII vesicle formation, whereas the essential role of ClaH seems indirect and less clear. We provide evidence that other evolutionary and functionally distinct transporters of
A. nidulans
also follow the herein identified Golgi‐independent trafficking route of UapA. Importantly, our findings suggest that specific membrane cargoes drive the formation of distinct COPII subpopulations that bypass the Golgi to be sorted non‐polarly to the PM, and thus serving house‐keeping cell functions.
Synopsis
Nutrient transporter translocation to the cell membrane operates via a novel trafficking route that does not involve functioning of the Golgi in fungi.
Transporter translocation from the endoplasmic reticulum (ER) to the plasma membrane (PM) depends on COPII vesicle formation.
Golgi and known post‐Golgi secretory routes are non‐essential for transporter biogenesis.
The mechanisms regulating trafficking of nutrient transporters and apical cargoes are distinct.
Graphical Abstract
Nutrient transporter translocation to the cell membrane operates via a novel trafficking route that does not involve functioning of the Golgi in fungi.</description><subject>Actin</subject><subject>Adapters</subject><subject>Aspergillus nidulans</subject><subject>Aspergillus nidulans - genetics</subject><subject>Cell Membrane</subject><subject>Cell membranes</subject><subject>Clathrin</subject><subject>EMBO20</subject><subject>Endoplasmic reticulum</subject><subject>Endosomes</subject><subject>Fungal Proteins - genetics</subject><subject>Fungi</subject><subject>Golgi Apparatus</subject><subject>Golgi cells</subject><subject>Localization</subject><subject>Membrane proteins</subject><subject>Membranes</subject><subject>Microtubules</subject><subject>Nutrients</subject><subject>polarity</subject><subject>Polymerization</subject><subject>secretion</subject><subject>SNAP receptors</subject><subject>Subpopulations</subject><subject>traffic</subject><subject>Trafficking</subject><subject>Translocation</subject><issn>1469-221X</issn><issn>1469-3178</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc1rGzEQxUVJifN17q0IesnFjj53Vz0UEuM6hZRCSCA3VburdRW00kbaTfB_H7l2HDdQctLA_ObpvRkAPmE0wZxwcqbbMkwIwoIJQcQHcIBZJsYU58XepiYE343AYYz3CCEu8mIfjChhnGSYHYDfN0G5aH2leuMd9A10Qx-Mdj3sV53Oh16HCHsPK20tbFcfKqfho1Fw7u3CwHLZqRihcfA8djosjLVDhM7Ug00Cx-Bjo2zUJ5v3CNx-n91ML8dXv-Y_pudX44pjKsYNrhEuaEUzjlmla1JyxrDOFdNlKjPOmSpYqQRRPKe8UXXiM5xqgnmtcnoEvq11u6FsdV2lBEFZ2QXTqrCUXhn5b8eZP3LhH2VOKREFSwKnG4HgHwYde9mauMqc0vohSsJQJhgriiKhX96g934ILsVLFBYZ4jTPEnW2pqrgYwy62ZrBSP69nlwtU26vlyY-72bY8i_nSsDXNfBkrF6-pydnPy-ud9XRejimObfQ4dX1_ww9A6lduK8</recordid><startdate>20200703</startdate><enddate>20200703</enddate><creator>Dimou, Sofia</creator><creator>Martzoukou, Olga</creator><creator>Dionysopoulou, Mariangela</creator><creator>Bouris, Vangelis</creator><creator>Amillis, Sotiris</creator><creator>Diallinas, George</creator><general>Nature Publishing Group UK</general><general>Blackwell Publishing Ltd</general><general>John Wiley and Sons Inc</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>7QL</scope><scope>7T5</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-3426-726X</orcidid><orcidid>https://orcid.org/0000-0001-5445-484X</orcidid></search><sort><creationdate>20200703</creationdate><title>Translocation of nutrient transporters to cell membrane via Golgi bypass in Aspergillus nidulans</title><author>Dimou, Sofia ; Martzoukou, Olga ; Dionysopoulou, Mariangela ; Bouris, Vangelis ; Amillis, Sotiris ; Diallinas, George</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5139-f1d0183c36514ced2b5441e7a4ebb546554a84ba92a5735fadd0161573215da73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Actin</topic><topic>Adapters</topic><topic>Aspergillus nidulans</topic><topic>Aspergillus nidulans - genetics</topic><topic>Cell Membrane</topic><topic>Cell membranes</topic><topic>Clathrin</topic><topic>EMBO20</topic><topic>Endoplasmic reticulum</topic><topic>Endosomes</topic><topic>Fungal Proteins - genetics</topic><topic>Fungi</topic><topic>Golgi Apparatus</topic><topic>Golgi cells</topic><topic>Localization</topic><topic>Membrane proteins</topic><topic>Membranes</topic><topic>Microtubules</topic><topic>Nutrients</topic><topic>polarity</topic><topic>Polymerization</topic><topic>secretion</topic><topic>SNAP receptors</topic><topic>Subpopulations</topic><topic>traffic</topic><topic>Trafficking</topic><topic>Translocation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Dimou, Sofia</creatorcontrib><creatorcontrib>Martzoukou, Olga</creatorcontrib><creatorcontrib>Dionysopoulou, Mariangela</creatorcontrib><creatorcontrib>Bouris, Vangelis</creatorcontrib><creatorcontrib>Amillis, Sotiris</creatorcontrib><creatorcontrib>Diallinas, George</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Immunology Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>EMBO reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext_linktorsrc</fulltext></delivery><addata><au>Dimou, Sofia</au><au>Martzoukou, Olga</au><au>Dionysopoulou, Mariangela</au><au>Bouris, Vangelis</au><au>Amillis, Sotiris</au><au>Diallinas, George</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Translocation of nutrient transporters to cell membrane via Golgi bypass in Aspergillus nidulans</atitle><jtitle>EMBO reports</jtitle><stitle>EMBO Rep</stitle><addtitle>EMBO Rep</addtitle><date>2020-07-03</date><risdate>2020</risdate><volume>21</volume><issue>7</issue><spage>e49929</spage><epage>n/a</epage><pages>e49929-n/a</pages><issn>1469-221X</issn><eissn>1469-3178</eissn><abstract>Nutrient transporters, being polytopic membrane proteins, are believed, but not formally shown, to traffic from their site of synthesis, the ER, to the plasma membrane through Golgi‐dependent vesicular trafficking. Here, we develop a novel genetic system to investigate the trafficking of a neosynthesized model transporter, the well‐studied UapA purine transporter of
Aspergillus nidulans
. We show that sorting of neosynthesized UapA to the plasma membrane (PM) bypasses the Golgi and does not necessitate key Rab GTPases, AP adaptors, microtubules or endosomes. UapA PM localization is found to be dependent on functional COPII vesicles, actin polymerization, clathrin heavy chain and the PM t‐SNARE SsoA. Actin polymerization proved to primarily affect COPII vesicle formation, whereas the essential role of ClaH seems indirect and less clear. We provide evidence that other evolutionary and functionally distinct transporters of
A. nidulans
also follow the herein identified Golgi‐independent trafficking route of UapA. Importantly, our findings suggest that specific membrane cargoes drive the formation of distinct COPII subpopulations that bypass the Golgi to be sorted non‐polarly to the PM, and thus serving house‐keeping cell functions.
Synopsis
Nutrient transporter translocation to the cell membrane operates via a novel trafficking route that does not involve functioning of the Golgi in fungi.
Transporter translocation from the endoplasmic reticulum (ER) to the plasma membrane (PM) depends on COPII vesicle formation.
Golgi and known post‐Golgi secretory routes are non‐essential for transporter biogenesis.
The mechanisms regulating trafficking of nutrient transporters and apical cargoes are distinct.
Graphical Abstract
Nutrient transporter translocation to the cell membrane operates via a novel trafficking route that does not involve functioning of the Golgi in fungi.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>32452614</pmid><doi>10.15252/embr.201949929</doi><tpages>19</tpages><orcidid>https://orcid.org/0000-0002-3426-726X</orcidid><orcidid>https://orcid.org/0000-0001-5445-484X</orcidid><oa>free_for_read</oa></addata></record> |
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source | Springer Nature OA Free Journals |
subjects | Actin Adapters Aspergillus nidulans Aspergillus nidulans - genetics Cell Membrane Cell membranes Clathrin EMBO20 Endoplasmic reticulum Endosomes Fungal Proteins - genetics Fungi Golgi Apparatus Golgi cells Localization Membrane proteins Membranes Microtubules Nutrients polarity Polymerization secretion SNAP receptors Subpopulations traffic Trafficking Translocation |
title | Translocation of nutrient transporters to cell membrane via Golgi bypass in Aspergillus nidulans |
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