Arabidopsis dynamin-related proteins DRP2B and DRP1A participate together in clathrin-coated vesicle formation during endocytosis
10.1073/pnas.0913562107
Crossref journal-article
Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences (341)
Abstract

Endocytosis performs a wide range of functions in animals and plants. Clathrin-coated vesicle (CCV) formation is an initial step of endocytosis, and in animal cells is largely achieved by dynamins. However, little is known of its molecular mechanisms in plant cells. To identify dynamin-related proteins (DRPs) involved in endocytic CCV formation in plant cells, we compared the behaviors of two structurally different Arabidopsis DRPs, DRP2B and DRP1A, with those of the clathrin light chain (CLC), a marker of CCVs, at the plasma membrane by variable incidence angle fluorescent microscopy (VIAFM). DRP2B shares domain organization with animal dynamins whereas DRP1A is plant-specific. We show that green fluorescent protein (GFP)-tagged DRP2B and DRP1A colocalized with CLC tagged with monomeric Kusabira Orange (mKO) in Arabidopsis cultured cells. Time-lapse VIAFM observations suggested that both GFP-DRP2B and GFP-DRP1A appeared and accumulated on the existing mKO-CLC foci and disappeared at the same time as or immediately after the disappearance of mKO-CLC. Moreover, DRP2B and DRP1A colocalized and assembled/disassembled together at the plasma membrane in Arabidopsis cells. A yeast two-hybrid assay showed that DRP2B and DRP1A interacted with each other. An inhibitor of clathrin-mediated endocytosis, tyrphostin A23, disturbed the localization of DRP1A, but had little effect on the localization of DRP2B, indicating that DRP1A and DRP2B have different molecular properties. These results suggest that DRP2B and DRP1A participate together in endocytic CCV formation in Arabidopsis cells despite the difference of their molecular properties.

Bibliography

Fujimoto, M., Arimura, S., Ueda, T., Takanashi, H., Hayashi, Y., Nakano, A., & Tsutsumi, N. (2010). Arabidopsis dynamin-related proteins DRP2B and DRP1A participate together in clathrin-coated vesicle formation during endocytosis. Proceedings of the National Academy of Sciences, 107(13), 6094–6099.

Authors 7
  1. Masaru Fujimoto (first)
  2. Shin-ichi Arimura (additional)
  3. Takashi Ueda (additional)
  4. Hideki Takanashi (additional)
  5. Yoshikazu Hayashi (additional)
  6. Akihiko Nakano (additional)
  7. Nobuhiro Tsutsumi (additional)
References 35 Referenced 118
  1. I Mellman, Endocytosis and molecular sorting. Annu Rev Cell Dev Biol 12, 575–625 (1996). (10.1146/annurev.cellbio.12.1.575) / Annu Rev Cell Dev Biol / Endocytosis and molecular sorting by Mellman I (1996)
  2. AS Murphy, A Bandyopadhyay, SE Holstein, WA Peer, Endocytotic cycling of PM proteins. Annu Rev Plant Biol 56, 221–251 (2005). (10.1146/annurev.arplant.56.032604.144150) / Annu Rev Plant Biol / Endocytotic cycling of PM proteins by Murphy AS (2005)
  3. FM Brodsky, C-Y Chen, C Knuehl, MC Towler, DE Wakeham, Biological basket weaving: Formation and function of clathrin-coated vesicles. Annu Rev Cell Dev Biol 17, 517–568 (2001). (10.1146/annurev.cellbio.17.1.517) / Annu Rev Cell Dev Biol / Biological basket weaving: Formation and function of clathrin-coated vesicles by Brodsky FM (2001)
  4. CJ Merrifield, ME Feldman, L Wan, W Almers, Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4, 691–698 (2002). (10.1038/ncb837) / Nat Cell Biol / Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits by Merrifield CJ (2002)
  5. M Kaksonen, CP Toret, DG Drubin, A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123, 305–320 (2005). (10.1016/j.cell.2005.09.024) / Cell / A modular design for the clathrin- and actin-mediated endocytosis machinery by Kaksonen M (2005)
  6. P Dhonukshe, et al., Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr Biol 17, 520–527 (2007). (10.1016/j.cub.2007.01.052) / Curr Biol / Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis by Dhonukshe P (2007)
  7. CA Konopka, SY Bednarek, Comparison of the dynamics and functional redundancy of the Arabidopsis dynamin-related isoforms DRP1A and DRP1C during plant development. Plant Physiol 147, 1590–1602 (2008). (10.1104/pp.108.116863) / Plant Physiol / Comparison of the dynamics and functional redundancy of the Arabidopsis dynamin-related isoforms DRP1A and DRP1C during plant development by Konopka CA (2008)
  8. CA Konopka, SY Bednarek, Variable-angle epifluorescence microscopy: A new way to look at protein dynamics in the plant cell cortex. Plant J 53, 186–196 (2008). (10.1111/j.1365-313X.2007.03306.x) / Plant J / Variable-angle epifluorescence microscopy: A new way to look at protein dynamics in the plant cell cortex by Konopka CA (2008)
  9. CA Konopka, SK Backues, SY Bednarek, Dynamics of Arabidopsis dynamin-related protein 1C and a clathrin light chain at the plasma membrane. Plant Cell 20, 1363–1380 (2008). (10.1105/tpc.108.059428) / Plant Cell / Dynamics of Arabidopsis dynamin-related protein 1C and a clathrin light chain at the plasma membrane by Konopka CA (2008)
  10. M Fujimoto, S Arimura, M Nakazono, N Tsutsumi, Imaging of plant dynamin-related proteins and clathrin around the plasma membrane by variable incidence angle fluorescence microscopy. Plant Biotechnol 24, 449–455 (2007). (10.5511/plantbiotechnology.24.449) / Plant Biotechnol / Imaging of plant dynamin-related proteins and clathrin around the plasma membrane by variable incidence angle fluorescence microscopy by Fujimoto M (2007)
  11. D Danino, JE Hinshaw, Dynamin family of mechanoenzymes. Curr Opin Cell Biol 13, 454–460 (2001). (10.1016/S0955-0674(00)00236-2) / Curr Opin Cell Biol / Dynamin family of mechanoenzymes by Danino D (2001)
  12. GJ Praefcke, HT McMahon, The dynamin superfamily: Universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5, 133–147 (2004). (10.1038/nrm1313) / Nat Rev Mol Cell Biol / The dynamin superfamily: Universal membrane tubulation and fission molecules? by Praefcke GJ (2004)
  13. S Sever, Dynamin and endocytosis. Curr Opin Cell Biol 14, 463–467 (2002). (10.1016/S0955-0674(02)00347-2) / Curr Opin Cell Biol / Dynamin and endocytosis by Sever S (2002)
  14. K Takei, PS McPherson, SL Schmid, P De Camilli, Tubular membrane invaginations coated by dynamin rings are induced by GTP-γS in nerve terminals. Nature 374, 186–190 (1995). (10.1038/374186a0) / Nature / Tubular membrane invaginations coated by dynamin rings are induced by GTP-γS in nerve terminals by Takei K (1995)
  15. SM Sweitzer, JE Hinshaw, Dynamin undergoes a GTP-dependent confor-mational change causing vesiculation. Cell 93, 1021–1029 (1998). (10.1016/S0092-8674(00)81207-6) / Cell / Dynamin undergoes a GTP-dependent confor-mational change causing vesiculation by Sweitzer SM (1998)
  16. MA Puthenveedu, M von Zastrow, Cargo regulates clathrin-coated pit dynamics. Cell 127, 113–124 (2006). (10.1016/j.cell.2006.08.035) / Cell / Cargo regulates clathrin-coated pit dynamics by Puthenveedu MA (2006)
  17. Z Hong, et al., A unified nomenclature for Arabidopsis dynamin-related large GTPases based on homology and possible functions. Plant Mol Biol 53, 261–265 (2003). (10.1023/B:PLAN.0000007000.29697.81) / Plant Mol Biol / A unified nomenclature for Arabidopsis dynamin-related large GTPases based on homology and possible functions by Hong Z (2003)
  18. J Samaj, et al., Endocytosis, actin cytoskeleton, and signaling. Plant Physiol 135, 1150–1161 (2004). (10.1104/pp.104.040683) / Plant Physiol / Endocytosis, actin cytoskeleton, and signaling by Samaj J (2004)
  19. Y Vallis, P Wigge, B Marks, PR Evans, HT McMahon, Importance of the pleckstrin homology domain of dynamin in clathrin-mediated endocytosis. Curr Biol 9, 257–260 (1999). (10.1016/S0960-9822(99)80114-6) / Curr Biol / Importance of the pleckstrin homology domain of dynamin in clathrin-mediated endocytosis by Vallis Y (1999)
  20. HS Shpetner, JS Herskovits, RB Vallee, A binding site for SH3 domains targets dynamin to coated pits. J Biol Chem 271, 13–16 (1996). (10.1074/jbc.271.1.13) / J Biol Chem / A binding site for SH3 domains targets dynamin to coated pits by Shpetner HS (1996)
  21. B-H Kang, JS Busse, SY Bednarek, Members of the Arabidopsis dynamin-like gene family, ADL1, are essential for plant cytokinesis and polarized cell growth. Plant Cell 15, 899–913 (2003). (10.1105/tpc.009670) / Plant Cell / Members of the Arabidopsis dynamin-like gene family, ADL1, are essential for plant cytokinesis and polarized cell growth by Kang B-H (2003)
  22. B-H Kang, JS Busse, C Dickey, DM Rancour, SY Bednarek, The Arabidopsis cell plate-associated dynamin-like protein, ADL1Ap, is required for multiple stages of plant growth and development. Plant Physiol 126, 47–68 (2001). (10.1104/pp.126.1.47) / Plant Physiol / The Arabidopsis cell plate-associated dynamin-like protein, ADL1Ap, is required for multiple stages of plant growth and development by Kang B-H (2001)
  23. B-H Kang, DM Rancour, SY Bednarek, The dynamin-like protein ADL1C is essential for plasma membrane maintenance during pollen maturation. Plant J 35, 1–15 (2003). (10.1046/j.1365-313X.2003.01775.x) / Plant J / The dynamin-like protein ADL1C is essential for plasma membrane maintenance during pollen maturation by Kang B-H (2003)
  24. DA Collings, et al., Arabidopsis dynamin-like protein DRP1A: A null mutant with widespread defects in endocytosis, cellulose synthesis, cytokinesis, and cell expansion. J Exp Bot 59, 361–376 (2008). (10.1093/jxb/erm324) / J Exp Bot / Arabidopsis dynamin-like protein DRP1A: A null mutant with widespread defects in endocytosis, cellulose synthesis, cytokinesis, and cell expansion by Collings DA (2008)
  25. JB Jin, et al., A new dynamin-like protein, ADL6, is involved in trafficking from the trans-Golgi network to the central vacuole in Arabidopsis. Plant Cell 13, 1511–1526 (2001). (10.1105/TPC.000534) / Plant Cell / A new dynamin-like protein, ADL6, is involved in trafficking from the trans-Golgi network to the central vacuole in Arabidopsis by Jin JB (2001)
  26. BC-H Lam, TL Sage, F Bianchi, E Blumwald, Regulation of ADL6 activity by its associated molecular network. Plant J 31, 565–576 (2002). (10.1046/j.1365-313X.2002.01377.x) / Plant J / Regulation of ADL6 activity by its associated molecular network by Lam BC-H (2002)
  27. E Alexandersson, G Saalbach, C Larsson, P Kjellbom, Arabidopsis plasma membrane proteomics identifies components of transport, signal transduction and membrane trafficking. Plant Cell Physiol 45, 1543–1556 (2004). (10.1093/pcp/pch209) / Plant Cell Physiol / Arabidopsis plasma membrane proteomics identifies components of transport, signal transduction and membrane trafficking by Alexandersson E (2004)
  28. S Arimura, GP Aida, M Fujimoto, M Nakazono, N Tsutsumi, Arabidopsis dynamin-like protein 2a (ADL2a), like ADL2b, is involved in plant mitochondrial division. Plant Cell Physiol 45, 236–242 (2004). (10.1093/pcp/pch024) / Plant Cell Physiol / Arabidopsis dynamin-like protein 2a (ADL2a), like ADL2b, is involved in plant mitochondrial division by Arimura S (2004)
  29. S Mano, C Nakamori, M Kondo, M Hayashi, M Nishimura, An Arabidopsis dynamin-related protein, DRP3A, controls both peroxisomal and mitochondrial division. Plant J 38, 487–498 (2004). (10.1111/j.1365-313X.2004.02063.x) / Plant J / An Arabidopsis dynamin-related protein, DRP3A, controls both peroxisomal and mitochondrial division by Mano S (2004)
  30. M Fujimoto, et al., Arabidopsis dynamin-related proteins DRP3A and DRP3B are functionally redundant in mitochondrial fission, but have distinct roles in peroxisomal fission. Plant J 58, 388–400 (2009). (10.1111/j.1365-313X.2009.03786.x) / Plant J / Arabidopsis dynamin-related proteins DRP3A and DRP3B are functionally redundant in mitochondrial fission, but have distinct roles in peroxisomal fission by Fujimoto M (2009)
  31. DG Robinson, L Jiang, K Schumacher, The endosomal system of plants: Charting new and familiar territories. Plant Physiol 147, 1482–1492 (2008). (10.1104/pp.108.120105) / Plant Physiol / The endosomal system of plants: Charting new and familiar territories by Robinson DG (2008)
  32. K Takei, Y Yoshida, H Yamada, Regulatory mechanisms of dynamin-dependent endocytosis. J Biochem 137, 243–247 (2005). (10.1093/jb/mvi052) / J Biochem / Regulatory mechanisms of dynamin-dependent endocytosis by Takei K (2005)
  33. SEH Holstein, Clathrin and plant endocytosis. Traffic 3, 614–620 (2002). (10.1034/j.1600-0854.2002.30903.x) / Traffic / Clathrin and plant endocytosis by Holstein SEH (2002)
  34. TJ Pucadyil, SL Schmid, Conserved functions of membrane active GTPases in coated vesicle formation. Science 325, 1217–1220 (2009). (10.1126/science.1171004) / Science / Conserved functions of membrane active GTPases in coated vesicle formation by Pucadyil TJ (2009)
  35. D Loerke, et al., Cargo and dynamin regulate clathrin-coated pit maturation. PLoS Biol 7, e57 (2009). (10.1371/journal.pbio.1000057) / PLoS Biol / Cargo and dynamin regulate clathrin-coated pit maturation by Loerke D (2009)
Dates
Type When
Created 15 years, 5 months ago (March 15, 2010, 11:59 p.m.)
Deposited 3 years, 2 months ago (June 7, 2022, 2:33 a.m.)
Indexed 4 weeks, 1 day ago (July 30, 2025, 8:28 p.m.)
Issued 15 years, 5 months ago (March 15, 2010)
Published 15 years, 5 months ago (March 15, 2010)
Published Online 15 years, 5 months ago (March 15, 2010)
Published Print 15 years, 4 months ago (March 30, 2010)
Funders 0

None

@article{Fujimoto_2010, title={Arabidopsis dynamin-related proteins DRP2B and DRP1A participate together in clathrin-coated vesicle formation during endocytosis}, volume={107}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.0913562107}, DOI={10.1073/pnas.0913562107}, number={13}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Fujimoto, Masaru and Arimura, Shin-ichi and Ueda, Takashi and Takanashi, Hideki and Hayashi, Yoshikazu and Nakano, Akihiko and Tsutsumi, Nobuhiro}, year={2010}, month=mar, pages={6094–6099} }