Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes
Many aspects of plant development, including patterning and tropisms, are largely dependent on the asymmetric distribution of the plant signaling molecule auxin. Auxin transport inhibitors (ATIs), which interfere with directional auxin transport, have been essential tools in formulating this concept...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2008-03, Vol.105 (11), p.4489-4494 |
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| creator | Dhonukshe, Pankaj Grigoriev, Ilya Fischer, Rainer Tominaga, Motoki Robinson, David G Hašek, Jiří Paciorek, Tomasz Petrášek, Jan Seifertová, Daniela Tejos, Ricardo Meisel, Lee A Zažímalová, Eva Gadella, Theodorus W.J. Jr Stierhof, York-Dieter Ueda, Takashi Oiwa, Kazuhiro Akhmanova, Anna Brock, Roland Spang, Anne Friml, Jiří |
| description | Many aspects of plant development, including patterning and tropisms, are largely dependent on the asymmetric distribution of the plant signaling molecule auxin. Auxin transport inhibitors (ATIs), which interfere with directional auxin transport, have been essential tools in formulating this concept. However, despite the use of ATIs in plant research for many decades, the mechanism of ATI action has remained largely elusive. Using real-time live-cell microscopy, we show here that prominent ATIs such as 2,3,5-triiodobenzoic acid (TIBA) and 2-(1-pyrenoyl) benzoic acid (PBA) inhibit vesicle trafficking in plant, yeast, and mammalian cells. Effects on micropinocytosis, rab5-labeled endosomal motility at the periphery of HeLa cells and on fibroblast mobility indicate that ATIs influence actin cytoskeleton. Visualization of actin cytoskeleton dynamics in plants, yeast, and mammalian cells show that ATIs stabilize actin. Conversely, stabilizing actin by chemical or genetic means interferes with endocytosis, vesicle motility, auxin transport, and plant development, including auxin transport-dependent processes. Our results show that a class of ATIs act as actin stabilizers and advocate that actin-dependent trafficking of auxin transport components participates in the mechanism of auxin transport. These studies also provide an example of how the common eukaryotic process of actin-based vesicle motility can fulfill a plant-specific physiological role. |
| doi_str_mv | 10.1073/pnas.0711414105 |
| format | Article |
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Jr ; Stierhof, York-Dieter ; Ueda, Takashi ; Oiwa, Kazuhiro ; Akhmanova, Anna ; Brock, Roland ; Spang, Anne ; Friml, Jiří</creator><creatorcontrib>Dhonukshe, Pankaj ; Grigoriev, Ilya ; Fischer, Rainer ; Tominaga, Motoki ; Robinson, David G ; Hašek, Jiří ; Paciorek, Tomasz ; Petrášek, Jan ; Seifertová, Daniela ; Tejos, Ricardo ; Meisel, Lee A ; Zažímalová, Eva ; Gadella, Theodorus W.J. Jr ; Stierhof, York-Dieter ; Ueda, Takashi ; Oiwa, Kazuhiro ; Akhmanova, Anna ; Brock, Roland ; Spang, Anne ; Friml, Jiří</creatorcontrib><description>Many aspects of plant development, including patterning and tropisms, are largely dependent on the asymmetric distribution of the plant signaling molecule auxin. Auxin transport inhibitors (ATIs), which interfere with directional auxin transport, have been essential tools in formulating this concept. However, despite the use of ATIs in plant research for many decades, the mechanism of ATI action has remained largely elusive. Using real-time live-cell microscopy, we show here that prominent ATIs such as 2,3,5-triiodobenzoic acid (TIBA) and 2-(1-pyrenoyl) benzoic acid (PBA) inhibit vesicle trafficking in plant, yeast, and mammalian cells. Effects on micropinocytosis, rab5-labeled endosomal motility at the periphery of HeLa cells and on fibroblast mobility indicate that ATIs influence actin cytoskeleton. Visualization of actin cytoskeleton dynamics in plants, yeast, and mammalian cells show that ATIs stabilize actin. Conversely, stabilizing actin by chemical or genetic means interferes with endocytosis, vesicle motility, auxin transport, and plant development, including auxin transport-dependent processes. Our results show that a class of ATIs act as actin stabilizers and advocate that actin-dependent trafficking of auxin transport components participates in the mechanism of auxin transport. These studies also provide an example of how the common eukaryotic process of actin-based vesicle motility can fulfill a plant-specific physiological role.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0711414105</identifier><identifier>PMID: 18337510</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>2,3,5-triiodobenzoic acid ; 2-(1-pyrenoyl) benzoic acid ; Actins ; Actins - metabolism ; Arabidopsis - drug effects ; Arabidopsis - metabolism ; Arabidopsis thaliana ; auxin transport inhbitors ; Auxins ; Biological Sciences ; Biological Transport ; Botany ; cell biology ; Cell Line ; Cytoskeleton ; Cytoskeleton - metabolism ; Endocytosis ; Eukaryotes ; fibroblasts ; HeLa cells ; Indoleacetic Acids - antagonists & inhibitors ; Indoleacetic Acids - metabolism ; metabolic inhibitors ; Microfilaments ; neoplasms ; organelles ; Plant cells ; Plant development ; Plant growth ; Plants ; Proteins ; Saccharomyces cerevisiae ; Saccharomyces cerevisiae - drug effects ; Saccharomyces cerevisiae - metabolism ; Solvents ; Studies ; vesicles ; Yeasts</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2008-03, Vol.105 (11), p.4489-4494</ispartof><rights>Copyright 2008 The National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Mar 18, 2008</rights><rights>2008 by The National Academy of Sciences of the USA</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c618t-15bc20583485896c0ab5e12b87d7fdb067368c3c305d0648e30487bbb0aba5183</citedby><cites>FETCH-LOGICAL-c618t-15bc20583485896c0ab5e12b87d7fdb067368c3c305d0648e30487bbb0aba5183</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/105/11.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/25461444$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/25461444$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18337510$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Dhonukshe, Pankaj</creatorcontrib><creatorcontrib>Grigoriev, Ilya</creatorcontrib><creatorcontrib>Fischer, Rainer</creatorcontrib><creatorcontrib>Tominaga, Motoki</creatorcontrib><creatorcontrib>Robinson, David G</creatorcontrib><creatorcontrib>Hašek, Jiří</creatorcontrib><creatorcontrib>Paciorek, Tomasz</creatorcontrib><creatorcontrib>Petrášek, Jan</creatorcontrib><creatorcontrib>Seifertová, Daniela</creatorcontrib><creatorcontrib>Tejos, Ricardo</creatorcontrib><creatorcontrib>Meisel, Lee A</creatorcontrib><creatorcontrib>Zažímalová, Eva</creatorcontrib><creatorcontrib>Gadella, Theodorus W.J. Jr</creatorcontrib><creatorcontrib>Stierhof, York-Dieter</creatorcontrib><creatorcontrib>Ueda, Takashi</creatorcontrib><creatorcontrib>Oiwa, Kazuhiro</creatorcontrib><creatorcontrib>Akhmanova, Anna</creatorcontrib><creatorcontrib>Brock, Roland</creatorcontrib><creatorcontrib>Spang, Anne</creatorcontrib><creatorcontrib>Friml, Jiří</creatorcontrib><title>Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Many aspects of plant development, including patterning and tropisms, are largely dependent on the asymmetric distribution of the plant signaling molecule auxin. Auxin transport inhibitors (ATIs), which interfere with directional auxin transport, have been essential tools in formulating this concept. 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Our results show that a class of ATIs act as actin stabilizers and advocate that actin-dependent trafficking of auxin transport components participates in the mechanism of auxin transport. These studies also provide an example of how the common eukaryotic process of actin-based vesicle motility can fulfill a plant-specific physiological role.</description><subject>2,3,5-triiodobenzoic acid</subject><subject>2-(1-pyrenoyl) benzoic acid</subject><subject>Actins</subject><subject>Actins - metabolism</subject><subject>Arabidopsis - drug effects</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>auxin transport inhbitors</subject><subject>Auxins</subject><subject>Biological Sciences</subject><subject>Biological Transport</subject><subject>Botany</subject><subject>cell biology</subject><subject>Cell Line</subject><subject>Cytoskeleton</subject><subject>Cytoskeleton - metabolism</subject><subject>Endocytosis</subject><subject>Eukaryotes</subject><subject>fibroblasts</subject><subject>HeLa cells</subject><subject>Indoleacetic Acids - antagonists & inhibitors</subject><subject>Indoleacetic Acids - metabolism</subject><subject>metabolic inhibitors</subject><subject>Microfilaments</subject><subject>neoplasms</subject><subject>organelles</subject><subject>Plant cells</subject><subject>Plant development</subject><subject>Plant growth</subject><subject>Plants</subject><subject>Proteins</subject><subject>Saccharomyces cerevisiae</subject><subject>Saccharomyces cerevisiae - drug effects</subject><subject>Saccharomyces cerevisiae - metabolism</subject><subject>Solvents</subject><subject>Studies</subject><subject>vesicles</subject><subject>Yeasts</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFks9vFCEcxYnR2LV69qROPBgv0375NTAXk6Zp1aSJB-2ZMAzTZTsDKzCb7n8vm9101YOGAyR83oPHA6HXGM4wCHq-9jqdgcCYlQH8CVpgaHHdsBaeogUAEbVkhJ2gFymtAKDlEp6jEywpFRzDAi0v5gfnqxy1T-sQc-X80nUuh5gqN621i9XGJmdGW00hu9HlbaV9X2mTi8xsc0j3drQ5-Krfej05U3Rl7TY2JlvZ-V7Hbcg2vUTPBj0m--own6Lb66sfl1_qm2-fv15e3NSmwTLXmHeGAJeUSS7bxoDuuMWkk6IXQ99BI2gjDTUUeA8Nk5YCk6LrugJqXnKdok973_XcTbY31pdso1pHN5WbqKCd-nPHu6W6CxtFaEslbovBh4NBDD9nm7KaXDJ2HLW3YU5KACOYt_K_IAEpCaO4gO__Aldhjr68QmFKb0RKUaDzPWRiSCna4fHKGNSua7XrWh27Loq3vyc98odyC_DuAOyURzuuMFaMyV3Wj_8m1DCPY7YPuaBv9ugqlc_xyBLOGswYOx426KD0XXRJ3X4v8SiAFJwSQn8BlqbSOA</recordid><startdate>20080318</startdate><enddate>20080318</enddate><creator>Dhonukshe, Pankaj</creator><creator>Grigoriev, Ilya</creator><creator>Fischer, Rainer</creator><creator>Tominaga, Motoki</creator><creator>Robinson, David G</creator><creator>Hašek, Jiří</creator><creator>Paciorek, Tomasz</creator><creator>Petrášek, Jan</creator><creator>Seifertová, Daniela</creator><creator>Tejos, Ricardo</creator><creator>Meisel, Lee A</creator><creator>Zažímalová, Eva</creator><creator>Gadella, Theodorus W.J. 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Jr</au><au>Stierhof, York-Dieter</au><au>Ueda, Takashi</au><au>Oiwa, Kazuhiro</au><au>Akhmanova, Anna</au><au>Brock, Roland</au><au>Spang, Anne</au><au>Friml, Jiří</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2008-03-18</date><risdate>2008</risdate><volume>105</volume><issue>11</issue><spage>4489</spage><epage>4494</epage><pages>4489-4494</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Many aspects of plant development, including patterning and tropisms, are largely dependent on the asymmetric distribution of the plant signaling molecule auxin. Auxin transport inhibitors (ATIs), which interfere with directional auxin transport, have been essential tools in formulating this concept. However, despite the use of ATIs in plant research for many decades, the mechanism of ATI action has remained largely elusive. Using real-time live-cell microscopy, we show here that prominent ATIs such as 2,3,5-triiodobenzoic acid (TIBA) and 2-(1-pyrenoyl) benzoic acid (PBA) inhibit vesicle trafficking in plant, yeast, and mammalian cells. Effects on micropinocytosis, rab5-labeled endosomal motility at the periphery of HeLa cells and on fibroblast mobility indicate that ATIs influence actin cytoskeleton. Visualization of actin cytoskeleton dynamics in plants, yeast, and mammalian cells show that ATIs stabilize actin. Conversely, stabilizing actin by chemical or genetic means interferes with endocytosis, vesicle motility, auxin transport, and plant development, including auxin transport-dependent processes. 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| subjects | 2,3,5-triiodobenzoic acid 2-(1-pyrenoyl) benzoic acid Actins Actins - metabolism Arabidopsis - drug effects Arabidopsis - metabolism Arabidopsis thaliana auxin transport inhbitors Auxins Biological Sciences Biological Transport Botany cell biology Cell Line Cytoskeleton Cytoskeleton - metabolism Endocytosis Eukaryotes fibroblasts HeLa cells Indoleacetic Acids - antagonists & inhibitors Indoleacetic Acids - metabolism metabolic inhibitors Microfilaments neoplasms organelles Plant cells Plant development Plant growth Plants Proteins Saccharomyces cerevisiae Saccharomyces cerevisiae - drug effects Saccharomyces cerevisiae - metabolism Solvents Studies vesicles Yeasts |
| title | Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes |
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