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Auxin Transport Inhibitors Impair Vesicle Motility and Actin Cytoskeleton Dynamics in Diverse Eukaryotes

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Auxin Transport Inhibitors Impair Vesicle Motility and Actin Cytoskeleton Dynamics in Diverse Eukaryotes Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes Pankaj Dhonukshea,b,c, Ilya Grigorievd, Rainer Fischere, Motoki Tominagaf,g, David G. Robinsonh, Jirˇı´Hasˇeki, Tomasz Pacioreka,j, Jan Petra´ sˇekk, Daniela Seifertova´ k, Ricardo Tejosl,m, Lee A. Meiselm, Eva Zazˇı´malova´ k, Theodorus W. J. Gadella, Jr.b, York-Dieter Stierhofa, Takashi Uedan, Kazuhiro Oiwaf, Anna Akhmanovad, Roland Brocke,o, Anne Spangp,q, and Jirˇı´Frimla,l,r,s aZentrum fu¨r Molekularbiologie der Pflanzen (ZMBP), Universita¨t Tu¨ bingen, Auf der Morgenstelle 3, D-72076 Tu¨bingen, Germany; dDepartment of Cell Biology and Genetics, Erasmus Medical Centre, P.O. Box 1738, 3000 DR Rotterdam, The Netherlands; eInstitute for Cell Biology, University of Tu¨bingen, D-72076 Tu¨bingen, Germany; fKansai Advanced Research Centre, National Institute of Information and Communications Technology, Kobe 651-2492, Japan; hCell Biology, Heidelberg Institute for Plant Sciences, University of Heidelberg, D-69120 Heidelberg, Germany; iInstitute of Microbiology, Academy of Sciences of the Czech Republic, Vı´denˇska´1083, 142 20 Prague 4, Czech Republic; bSection of Molecular Cytology, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098 SM Amsterdam, The Netherlands; kInstitute of Experimental Botany, Academy of Sciences of the Czech Republic, Rozvojova´ 263, 165 02 Praha 6, Czech Republic; nDepartment of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan; pFriedrich Miescher Laboratory of the Max Planck Society, Spemannstrasse 39, D-72076 Tu¨bingen, Germany; rDepartment of Functional Genomics, Masaryk University, Kamenice 25, C2-62500 Brno, Czech Republic; lDepartment of Plant Systems Biology, Flanders Institute for Biotechnology and Department of Molecular Genetics, Ghent University, Technologiepark 927, 9052 Gent, Belgium; and mMillennium Nucleus in Plant Cell Biology and Center of Plant Biotechnology, Andre´s Bello University, Avenue Repu´blica 217, 837-0146, Santiago, Chile Edited by Joanne Chory, Salk Institute for Biological Studies, La Jolla, CA, and approved January 22, 2008 (received for review December 6, 2007) Many aspects of plant development, including patterning and (12). Inhibition of ADP-ribosylation factor (ARF) guanine nucle- tropisms, are largely dependent on the asymmetric distribution of otide exchange factor (GEF)-dependent vesicle trafficking by the plant signaling molecule auxin. Auxin transport inhibitors brefeldin A also has suggested that both PIN and AUX1 auxin (ATIs), which interfere with directional auxin transport, have been carriers undergo constitutive cycling between the plasma mem- essential tools in formulating this concept. However, despite the brane (PM) and endosomes (13–15). Unexpectedly, ATIs such as use of ATIs in plant research for many decades, the mechanism of TIBA or PBA interfere with this trafficking (13, 15), but the PLANT BIOLOGY ATI action has remained largely elusive. Using real-time live-cell underlying cellular mechanism and functional significance of this microscopy, we show here that prominent ATIs such as 2,3,5- effect is unclear. Here, we demonstrate that TIBA and PBA triiodobenzoic acid (TIBA) and 2-(1-pyrenoyl) benzoic acid (PBA) interfere with actin dynamics in plants and also in yeast and inhibit vesicle trafficking in plant, yeast, and mammalian cells. mammalian cells providing a mechanism by which these drugs Effects on micropinocytosis, rab5-labeled endosomal motility at disrupt vesicle subcellular trafficking, including that of PIN auxin the periphery of HeLa cells and on fibroblast mobility indicate that efflux carriers. ATIs influence actin cytoskeleton. Visualization of actin cytoskel- eton dynamics in plants, yeast, and mammalian cells show that Results ATIs stabilize actin. Conversely, stabilizing actin by chemical or Supporting Information (SI). For further information on the results genetic means interferes with endocytosis, vesicle motility, auxin discussed below, see SI Figs. 5–15, SI Movies 1–14, and SI Results. transport, and plant development, including auxin transport-de- pendent processes. Our results show that a class of ATIs act as actin ATIs Interfere with Multiple Vesicle Trafficking Processes in Plant stabilizers and advocate that actin-dependent trafficking of auxin Cells. To address the mechanism of ATIs effect on auxin carrier transport components participates in the mechanism of auxin trafficking, we explored their effects on various vesicle trafficking transport. These studies also provide an example of how the processes by real-time live-cell microscopy. First we tested the effect common eukaryotic process of actin-based vesicle motility can of ATIs on endocytic, endosomal, and Golgi dynamics in suspen- fulfill a plant-specific physiological role. sion-cultured tobacco BY-2 cells and in Arabidopsis root cells. FM4–64 was used as an endocytic tracer (16), GFP-Ara7 (the plant ͉ ͉ ͉ PIN proteins plant development vesicle traffic auxin efflux inhibitors ortholog of mammalian Rab5) (17) was used as an endosomal he signaling molecule auxin plays a pivotal role in regulating Tplant development; however, auxin is unique among plant Author contributions: P.D., L.A.M., E.Z., T.W.J.G., K.O., A.A., R.B., A.S., and J.F. designed hormones because it is transported in a directional (polar) manner research; P.D., I.G., R.F., M.T., J.H., T.P., J.P., D.S., R.T., Y.-D.S., T.U., A.A., and A.S. performed research; D.G.R. contributed new reagents/analytic tools; P.D., I.G., R.F., M.T., J.H., J.P., E.Z., through plant tissues (1). This polar transport mediates an asym- Y.-D.S., T.U., A.A., R.B., and A.S. analyzed data; and P.D. and J.F. wrote the paper. metric distribution of auxin between cells that triggers a plethora of The authors declare no conflict of interest. growth and developmental processes, such as embryo and organ This article is a PNAS Direct Submission. development, vascular patterning, apical dominance, and tropisms cPresent address: Molecular Genetics Group, Department of Biology, Utrecht University, (2–6). Our knowledge of the mechanism of polar auxin transport Padualaan 8, 3584 CH, Utrecht, The Netherlands. and its role in plant development has largely been based on gPresent address: Discovery Research Institute, RIKEN, 2-1, Hirosawa, Wako, Saitama 351- pharmacological tools: auxin transport inhibitors (ATIs) that have 0198, Japan. been in use for more than half a century. ATIs such as 1-naphth- jPresent address: Stanford University, 371 Serra Mall, Stanford, CA 94305-5020. ylphthalamic acid (NPA), 2,3,5-triiodobenzoic acid (TIBA), and oPresent address: Department of Biochemistry, Nijmegen Centre for Molecular Life Sci- 2-(1-pyrenoyl) benzoic acid (PBA) inhibit auxin efflux and thus ences, Radboud University Nijmegen Medical Centre, Geert Grooteplein 28, 6525 GA, block polar auxin movement between cells (7, 8). Exogenously Nijmegen, The Netherlands. applied ATIs interfere with auxin distribution and thus perturb qPresent address: Biozentrum, University of Basel, Klingelbergstrasse 50/70, CH-4056 Basel, plant development (1). Similar developmental defects identified in Switzerland. some Arabidopsis mutants have led to the identification of the auxin sTo whom correspondence should be addressed. E-mail: [email protected]. efflux and influx components PIN (5, 9) and AUX1/LAX (10, 11) This article contains supporting information online at www.pnas.org/cgi/content/full/ proteins, respectively. PIN proteins have been shown, on account of 0711414105/DC1. their polar, subcellular localization, to direct the polar flow of auxin © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0711414105 PNAS ͉ March 18, 2008 ͉ vol. 105 ͉ no. 11 ͉ 4489–4494 Downloaded by guest on September 26, 2021 Fig. 1. Effects of ATIs on endocytosis and vesicle motility in plant cells. (A–F) Endocytosis and endosomal and trans-Golgi motility in tobacco BY-2 cells as visualized by FM4-64 (red), ST-YFP (green), and GFP-Ara7 (green). Solvent control, FM4-64 (2 ␮M, 30 min): FM4-64/ST-YFP overlay (A), FM4-64 overlay of frame 1 (red) on frame 2 (ϩ3 s, green) (B), ST-YFP overlay of frame 1 (green) on frame 2 (ϩ3 s, red) (C). (D) TIBA (25 ␮M, 30 min) followed by TIBA/FM4–64 (90 min): FM4–64 (red), ST-YFP overlay of frame 1 (green) on frame 10 (ϩ30 s, red). (E) Solvent control (30 min), GFP-Ara7 overlay of frame 1 (green) on frame 2 (ϩ1.5 s, red). (F) Treatment with TIBA (25 ␮M, 30 min), GFP-Ara7 overlay of frame 1 (green) on frame 10 (ϩ15 s, red). Note the Insets for better visualization of vesicles. (Scale bars: 5 ␮m.) (G–L) Endocytosis and endosomal motility in Arabidopsis root cells as visualized by FM4-64 (red) and GFP-Ara7 (green). Solvent control, FM4-64 (2 ␮M, 30 min): FM4-64/GFP-Ara7 overlay (G). GFP-Ara7 overlay of frame 1 (green) on frame 2 (ϩ6 s, red) (H), FM4-64 overlay of frame 1 (red) on frame 2 (ϩ6 s, green) (I). FM4-64 (2 ␮M, 30 min) followed by PBA (15 ␮M)/FM4-64 (30 min): FM4-64/GFP-Ara7 overlay (J), GFP-Ara7 overlay of frame 1 (green) on frame 5 (ϩ30 s, red) (K), FM4-64 overlay of frame 1 (red) on frame 5 (ϩ30 s, green) (L). (Scale bars: 5 ␮m.) marker, and sialyl transferase-yellow fluorescent protein (ST-YFP) FM4–64 uptake was reduced and FM4–64 persisted to large extent (18) was used as a Golgi marker. In BY-2 cells, FM4–64 was at the PM (Fig. 2B). We also tested the effects of ATIs on internalized within 5–10 min, and labeled endosomes, which were mammalian cells. Three main types of endocytosis can be distin- largely distinct from the ST-YFP-labeled Golgi (Fig. 1A). Both guished in HeLa cells: macropinocytosis, which is strongly depen- endosomes and Golgi displayed a highly dynamic behavior, which dent on actin cytoskeleton dynamics; clathrin-mediated endocyto- was visualized through superimposition of two successive frames sis; and lipid raft/caveolar-dependent endocytosis (20).
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