Protein kinase A activity is necessary for fission and fusion of Golgi to endoplasmic reticulum retrograde tubules
It is becoming increasingly accepted that together with vesicles, tubules play a major role in the transfer of cargo between different cellular compartments. In contrast to our understanding of the molecular mechanisms of vesicular transport, little is known about tubular transport. How signal trans...
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| creator | Tenorio, María J Luchsinger, Charlotte Mardones, Gonzalo A |
| description | It is becoming increasingly accepted that together with vesicles, tubules play a major role in the transfer of cargo between different cellular compartments. In contrast to our understanding of the molecular mechanisms of vesicular transport, little is known about tubular transport. How signal transduction molecules regulate these two modes of membrane transport processes is also poorly understood. In this study we investigated whether protein kinase A (PKA) activity regulates the retrograde, tubular transport of Golgi matrix proteins from the Golgi to the endoplasmic reticulum (ER). We found that Golgi-to-ER retrograde transport of the Golgi matrix proteins giantin, GM130, GRASP55, GRASP65, and p115 was impaired in the presence of PKA inhibitors. In addition, we unexpectedly found accumulation of tubules containing both Golgi matrix proteins and resident Golgi transmembrane proteins. These tubules were still attached to the Golgi and were highly dynamic. Our data suggest that both fission and fusion of retrograde tubules are mechanisms regulated by PKA activity. |
| doi_str_mv | 10.1371/journal.pone.0135260 |
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In contrast to our understanding of the molecular mechanisms of vesicular transport, little is known about tubular transport. How signal transduction molecules regulate these two modes of membrane transport processes is also poorly understood. In this study we investigated whether protein kinase A (PKA) activity regulates the retrograde, tubular transport of Golgi matrix proteins from the Golgi to the endoplasmic reticulum (ER). We found that Golgi-to-ER retrograde transport of the Golgi matrix proteins giantin, GM130, GRASP55, GRASP65, and p115 was impaired in the presence of PKA inhibitors. In addition, we unexpectedly found accumulation of tubules containing both Golgi matrix proteins and resident Golgi transmembrane proteins. These tubules were still attached to the Golgi and were highly dynamic. Our data suggest that both fission and fusion of retrograde tubules are mechanisms regulated by PKA activity.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0135260</identifier><identifier>PMID: 26258546</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Autoantigens - genetics ; Autoantigens - metabolism ; Biological Transport ; Cargo compartments ; Cell Line ; Cellular signal transduction ; Cyclic AMP-Dependent Protein Kinases - antagonists & inhibitors ; Cyclic AMP-Dependent Protein Kinases - genetics ; Cyclic AMP-Dependent Protein Kinases - metabolism ; Endoplasmic reticulum ; Endoplasmic Reticulum - drug effects ; Endoplasmic Reticulum - metabolism ; Endoplasmic Reticulum - ultrastructure ; Enzymes ; Fibroblasts - drug effects ; Fibroblasts - metabolism ; Fibroblasts - ultrastructure ; Fission ; Gene Expression ; Golgi apparatus ; Golgi Apparatus - drug effects ; Golgi Apparatus - metabolism ; Golgi Apparatus - ultrastructure ; HeLa Cells ; Humans ; Immunoglobulins ; Kinases ; MCF-7 Cells ; Membrane Fusion - drug effects ; Membrane Fusion - physiology ; Membrane proteins ; Membrane Proteins - genetics ; Membrane Proteins - metabolism ; Molecular chains ; Molecular modelling ; Phase transitions ; Phosphorylation ; Physiology ; Protein kinase A ; Protein Kinase Inhibitors - pharmacology ; Protein kinases ; Proteins ; Rats ; Retrograde transport ; Signal processing ; Signal Transduction ; Time-Lapse Imaging ; Transport processes ; Transport Vesicles - metabolism ; Transport Vesicles - ultrastructure ; Tubules ; Vesicular Transport Proteins - genetics ; Vesicular Transport Proteins - metabolism</subject><ispartof>PloS one, 2015-08, Vol.10 (8), p.e0135260-e0135260</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Tenorio et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Tenorio et al 2015 Tenorio et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-cb518312c6c6b23eafe62cc864529846e7272bf487cc352cb1b977c53d3460ef3</citedby><cites>FETCH-LOGICAL-c692t-cb518312c6c6b23eafe62cc864529846e7272bf487cc352cb1b977c53d3460ef3</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/PMC4530959/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4530959/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26258546$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Johannes, Ludger</contributor><creatorcontrib>Tenorio, María J</creatorcontrib><creatorcontrib>Luchsinger, Charlotte</creatorcontrib><creatorcontrib>Mardones, Gonzalo A</creatorcontrib><title>Protein kinase A activity is necessary for fission and fusion of Golgi to endoplasmic reticulum retrograde tubules</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>It is becoming increasingly accepted that together with vesicles, tubules play a major role in the transfer of cargo between different cellular compartments. In contrast to our understanding of the molecular mechanisms of vesicular transport, little is known about tubular transport. How signal transduction molecules regulate these two modes of membrane transport processes is also poorly understood. In this study we investigated whether protein kinase A (PKA) activity regulates the retrograde, tubular transport of Golgi matrix proteins from the Golgi to the endoplasmic reticulum (ER). We found that Golgi-to-ER retrograde transport of the Golgi matrix proteins giantin, GM130, GRASP55, GRASP65, and p115 was impaired in the presence of PKA inhibitors. In addition, we unexpectedly found accumulation of tubules containing both Golgi matrix proteins and resident Golgi transmembrane proteins. These tubules were still attached to the Golgi and were highly dynamic. Our data suggest that both fission and fusion of retrograde tubules are mechanisms regulated by PKA activity.</description><subject>Animals</subject><subject>Autoantigens - genetics</subject><subject>Autoantigens - metabolism</subject><subject>Biological Transport</subject><subject>Cargo compartments</subject><subject>Cell Line</subject><subject>Cellular signal transduction</subject><subject>Cyclic AMP-Dependent Protein Kinases - antagonists & inhibitors</subject><subject>Cyclic AMP-Dependent Protein Kinases - genetics</subject><subject>Cyclic AMP-Dependent Protein Kinases - metabolism</subject><subject>Endoplasmic reticulum</subject><subject>Endoplasmic Reticulum - drug effects</subject><subject>Endoplasmic Reticulum - metabolism</subject><subject>Endoplasmic Reticulum - ultrastructure</subject><subject>Enzymes</subject><subject>Fibroblasts - drug effects</subject><subject>Fibroblasts - metabolism</subject><subject>Fibroblasts - ultrastructure</subject><subject>Fission</subject><subject>Gene Expression</subject><subject>Golgi apparatus</subject><subject>Golgi Apparatus - drug effects</subject><subject>Golgi Apparatus - metabolism</subject><subject>Golgi Apparatus - ultrastructure</subject><subject>HeLa Cells</subject><subject>Humans</subject><subject>Immunoglobulins</subject><subject>Kinases</subject><subject>MCF-7 Cells</subject><subject>Membrane Fusion - drug effects</subject><subject>Membrane Fusion - physiology</subject><subject>Membrane proteins</subject><subject>Membrane Proteins - genetics</subject><subject>Membrane Proteins - metabolism</subject><subject>Molecular chains</subject><subject>Molecular modelling</subject><subject>Phase transitions</subject><subject>Phosphorylation</subject><subject>Physiology</subject><subject>Protein kinase A</subject><subject>Protein Kinase Inhibitors - pharmacology</subject><subject>Protein kinases</subject><subject>Proteins</subject><subject>Rats</subject><subject>Retrograde transport</subject><subject>Signal processing</subject><subject>Signal Transduction</subject><subject>Time-Lapse Imaging</subject><subject>Transport processes</subject><subject>Transport Vesicles - metabolism</subject><subject>Transport Vesicles - ultrastructure</subject><subject>Tubules</subject><subject>Vesicular Transport Proteins - genetics</subject><subject>Vesicular Transport Proteins - metabolism</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk11v0zAUhiMEYqPwDxBYQkJw0RJ_xE5ukKoJRqVJQ3zdWo5zkrq4cWc7E_v3uGs2NWgXyBc-sp_z2u-xT5a9xPkCU4E_bNzge2UXO9fDIse0IDx_lJ3iipI5Jzl9fBSfZM9C2OR5QUvOn2YnhJOiLBg_zfxX7yKYHv02vQqAlkjpaK5NvEEmoB40hKD8DWqdR60Jwbgeqb5B7XAbuhadO9sZFB2CvnE7q8LWaOQhGj3YYbuPvOu8agDFoR4shOfZk1bZAC_GeZb9_Pzpx9mX-cXl-epseTHXvCJxrusClxQTzTWvCQXVAidal5wVpCoZB0EEqVtWCq2TeV3juhJCF7ShjOfQ0ln2-qC7sy7IsVxBYpFTRhkjJBGrA9E4tZE7b7bJqnTKyNsF5zupfDJiQQqBNRcNK1qgLE2KVVBVWGtclQLXkLQ-jqcN9RYaDX30yk5Epzu9WcvOXUtW0LwqqiTwbhTw7mqAEOXWBA3Wqh7ccLi3wIKny8-yN_-gD7sbqU4lA6ZvXTpX70XlkpEixyWp8kQtHqDSaCA9ZPpbrUnrk4T3k4TERPgTOzWEIFffv_0_e_lryr49YtegbFwHZ4eY_lmYguwAau9C8NDeFxnnct8ad9WQ-9aQY2uktFfHD3SfdNcL9C-yQQmb</recordid><startdate>20150810</startdate><enddate>20150810</enddate><creator>Tenorio, María J</creator><creator>Luchsinger, Charlotte</creator><creator>Mardones, Gonzalo A</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20150810</creationdate><title>Protein kinase A activity is necessary for fission and fusion of Golgi to endoplasmic reticulum retrograde tubules</title><author>Tenorio, María J ; Luchsinger, Charlotte ; Mardones, Gonzalo A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-cb518312c6c6b23eafe62cc864529846e7272bf487cc352cb1b977c53d3460ef3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Autoantigens - genetics</topic><topic>Autoantigens - metabolism</topic><topic>Biological Transport</topic><topic>Cargo compartments</topic><topic>Cell Line</topic><topic>Cellular signal transduction</topic><topic>Cyclic AMP-Dependent Protein Kinases - antagonists & inhibitors</topic><topic>Cyclic AMP-Dependent Protein Kinases - genetics</topic><topic>Cyclic AMP-Dependent Protein Kinases - metabolism</topic><topic>Endoplasmic reticulum</topic><topic>Endoplasmic Reticulum - drug effects</topic><topic>Endoplasmic Reticulum - metabolism</topic><topic>Endoplasmic Reticulum - ultrastructure</topic><topic>Enzymes</topic><topic>Fibroblasts - drug effects</topic><topic>Fibroblasts - metabolism</topic><topic>Fibroblasts - ultrastructure</topic><topic>Fission</topic><topic>Gene Expression</topic><topic>Golgi apparatus</topic><topic>Golgi Apparatus - drug effects</topic><topic>Golgi Apparatus - metabolism</topic><topic>Golgi Apparatus - ultrastructure</topic><topic>HeLa Cells</topic><topic>Humans</topic><topic>Immunoglobulins</topic><topic>Kinases</topic><topic>MCF-7 Cells</topic><topic>Membrane Fusion - drug effects</topic><topic>Membrane Fusion - physiology</topic><topic>Membrane proteins</topic><topic>Membrane Proteins - genetics</topic><topic>Membrane Proteins - metabolism</topic><topic>Molecular chains</topic><topic>Molecular modelling</topic><topic>Phase transitions</topic><topic>Phosphorylation</topic><topic>Physiology</topic><topic>Protein kinase A</topic><topic>Protein Kinase Inhibitors - pharmacology</topic><topic>Protein kinases</topic><topic>Proteins</topic><topic>Rats</topic><topic>Retrograde transport</topic><topic>Signal processing</topic><topic>Signal Transduction</topic><topic>Time-Lapse Imaging</topic><topic>Transport processes</topic><topic>Transport Vesicles - metabolism</topic><topic>Transport Vesicles - ultrastructure</topic><topic>Tubules</topic><topic>Vesicular Transport Proteins - genetics</topic><topic>Vesicular Transport Proteins - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Tenorio, María J</creatorcontrib><creatorcontrib>Luchsinger, Charlotte</creatorcontrib><creatorcontrib>Mardones, Gonzalo 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>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tenorio, María J</au><au>Luchsinger, Charlotte</au><au>Mardones, Gonzalo A</au><au>Johannes, Ludger</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Protein kinase A activity is necessary for fission and fusion of Golgi to endoplasmic reticulum retrograde tubules</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-08-10</date><risdate>2015</risdate><volume>10</volume><issue>8</issue><spage>e0135260</spage><epage>e0135260</epage><pages>e0135260-e0135260</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>It is becoming increasingly accepted that together with vesicles, tubules play a major role in the transfer of cargo between different cellular compartments. In contrast to our understanding of the molecular mechanisms of vesicular transport, little is known about tubular transport. How signal transduction molecules regulate these two modes of membrane transport processes is also poorly understood. In this study we investigated whether protein kinase A (PKA) activity regulates the retrograde, tubular transport of Golgi matrix proteins from the Golgi to the endoplasmic reticulum (ER). We found that Golgi-to-ER retrograde transport of the Golgi matrix proteins giantin, GM130, GRASP55, GRASP65, and p115 was impaired in the presence of PKA inhibitors. In addition, we unexpectedly found accumulation of tubules containing both Golgi matrix proteins and resident Golgi transmembrane proteins. These tubules were still attached to the Golgi and were highly dynamic. Our data suggest that both fission and fusion of retrograde tubules are mechanisms regulated by PKA activity.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26258546</pmid><doi>10.1371/journal.pone.0135260</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Autoantigens - genetics Autoantigens - metabolism Biological Transport Cargo compartments Cell Line Cellular signal transduction Cyclic AMP-Dependent Protein Kinases - antagonists & inhibitors Cyclic AMP-Dependent Protein Kinases - genetics Cyclic AMP-Dependent Protein Kinases - metabolism Endoplasmic reticulum Endoplasmic Reticulum - drug effects Endoplasmic Reticulum - metabolism Endoplasmic Reticulum - ultrastructure Enzymes Fibroblasts - drug effects Fibroblasts - metabolism Fibroblasts - ultrastructure Fission Gene Expression Golgi apparatus Golgi Apparatus - drug effects Golgi Apparatus - metabolism Golgi Apparatus - ultrastructure HeLa Cells Humans Immunoglobulins Kinases MCF-7 Cells Membrane Fusion - drug effects Membrane Fusion - physiology Membrane proteins Membrane Proteins - genetics Membrane Proteins - metabolism Molecular chains Molecular modelling Phase transitions Phosphorylation Physiology Protein kinase A Protein Kinase Inhibitors - pharmacology Protein kinases Proteins Rats Retrograde transport Signal processing Signal Transduction Time-Lapse Imaging Transport processes Transport Vesicles - metabolism Transport Vesicles - ultrastructure Tubules Vesicular Transport Proteins - genetics Vesicular Transport Proteins - metabolism |
| title | Protein kinase A activity is necessary for fission and fusion of Golgi to endoplasmic reticulum retrograde tubules |
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