Dynamic behavior of clathrin in Arabidopsis thaliana unveiled by live imaging

Plant Journal

Volumn 69, Issue 2, 2012, Pages 204-216

  Ito, Emi ^a   Fujimoto, Masaru ^a   Ebine, Kazuo ^a,c   Uemura, Tomohiro ^a   Ueda, Takashi ^a   Nakano, Akihiko ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b RIKEN   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

Arabidopsis thaliana; brefeldin A; cell plate; clathrin; live imaging; plasma membrane; wortmannin

Indexed keywords

ARABIDOPSIS THALIANA; BREFELDIN A; CELL PLATE; CLATHRINS; PLASMA MEMBRANE; WORTMANNIN;

CELL MEMBRANES; DYNAMICS; MEMBRANES; MOLECULAR BIOLOGY; PLANTS (BOTANY); PLASMAS;

PROTEINS;

ANDROSTANE DERIVATIVE; ARABIDOPSIS PROTEIN; BREFELDIN A; CLATHRIN LIGHT CHAIN; DYNAMIN; HYBRID PROTEIN; PHOTOPROTEIN; PROTEIN KINASE INHIBITOR; PROTEIN SYNTHESIS INHIBITOR; WORTMANNIN;

ARABIDOPSIS; ARTICLE; CELL MEMBRANE; COATED VESICLE; CONFOCAL MICROSCOPY; DRUG EFFECT; ENDOCYTOSIS; ENDOSOME; GENETICS; METABOLISM; PLANT ROOT; SEEDLING; TIME LAPSE IMAGING; TRANS GOLGI NETWORK; TRANSGENIC PLANT; TRANSPORT AT THE CELLULAR LEVEL; ULTRASTRUCTURE;

ANDROSTADIENES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; BREFELDIN A; CELL MEMBRANE; CLATHRIN LIGHT CHAINS; CLATHRIN-COATED VESICLES; DYNAMINS; ENDOCYTOSIS; ENDOSOMES; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROTEIN KINASE INHIBITORS; PROTEIN SYNTHESIS INHIBITORS; RECOMBINANT FUSION PROTEINS; SEEDLING; TIME-LAPSE IMAGING; TRANS-GOLGI NETWORK;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84855671917     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04782.x     Document Type: Article

References (78)

1. Anuntalabhochai, S., Terryn, N., Van Montagu, M., and, Inzé, D., (1991) Molecular characterization of an Arabidopsis thaliana cDNA encoding a small GTP-binding protein, Rha1. Plant J. 1, 167-174. (Pubitemid 121001058)
2. Backues, S.K., and, Bednarek, S.Y., (2010) Arabidopsis dynamin-related protein 1A polymers bind, but do not tubulate, liposomes. Biochem. Biophys. Res. Commun. 393, 734-739.
3. Barth, M., and, Holstein, S.E., (2004) Identification and functional characterization of Arabidopsis AP180, a binding partner of plant alphaC-adaptin. J. Cell Sci. 117, 2051-2062. (Pubitemid 38745138)
4. Boevink, P., Oparka, K., Santa Cruz, S., Martin, B., Betteridge, A., and, Hawes, C., (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J. 15, 441-447.
5. Boutté, Y., Crosnier, M.T., Carraro, N., Traas, J., and, Satiat-Jeunemaitre, B., (2006) The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteins. J. Cell Sci. 119, 1255-1265.
6. Boutté, Y., Frescatada-Rosa, M., Men, S., et al. (2010) Endocytosis restricts Arabidopsis KNOLLE syntaxin to the cell division plane during late cytokinesis. EMBO J. 29, 546-558.
7. Brodsky, F.M., Chen, C.Y., Knuehl, C., Towler, M.C., and, Wakeham, D.E., (2001) Biological basket weaving: formation and function of clathrin-coated vesicles. Annu. Rev. Cell. Dev. Biol. 17, 517-568. (Pubitemid 33096185)
8. Chardin, P., and, McCormick, F., (1999) Brefeldin A: the advantage of being uncompetitive. Cell, 97, 153-155. (Pubitemid 29194265)
9. Coleman, J., Evans, D.E., Hawes, C.R., Horsley, D., and, Cole, L., (1987) Structure and molecular organization of higher plant coated vesicles. J. Cell Sci. 88, 35-45.
10. Collings, D.A., Gebbie, L.K., Howles, P.A., Hurley, U.A., Birch, R.J., Cork, A.H., Hocart, C.H., Arioli, T., and, Williamson, R.E., (2008) 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. (Pubitemid 351651372)
11. Danino, D., and, Hinshaw, J.E., (2001) Dynamin family of mechanoenzymes. Curr. Opin. Cell Biol. 13, 454-460. (Pubitemid 32709769)
12. Depta, H., and, Robinson, D.G., (1986) The isolation and enrichment of coated vesicles from suspension-cultured carrot cells. Protoplasma, 130, 162.
13. Depta, H., Freundt, H., Hartmann, D., and, Robinson, D.G., (1987) Preparation of a homogenous coated vesicle fraction from bean leaves. Protoplasma, 136, 154-160.
14. +-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell, 18, 715-730. (Pubitemid 43956173)
15. Dhonukshe, P., Aniento, F., Hwang, I., Robinson, D.G., Mravec, J., Stierhof, Y.D., and, Friml, J., (2007) Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 17, 520-527. (Pubitemid 46420535)
16. Di Paolo, G., and, De Camilli, P., (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature, 443, 651-657. (Pubitemid 44564702)
17. Ebine, K., and, Ueda, T., (2009) Unique mechanism of plant endocytic/vacuolar transport pathways. J. Plant. Res. 122, 21-30.
18. Ebine, K., Okatani, Y., Uemura, T., et al. (2008) A SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana. Plant Cell, 20, 3006-3021.
19. Ebine, K., Fujimoto, M., Okatani, Y., et al. (2011) A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6. Nat. Cell Biol. 13, 853-859.
20. Emans, N., Zimmermann, S., and, Fischer, R., (2002) Uptake of a fluorescent marker in plant cells is sensitive to brefeldin A and wortmannin. Plant Cell, 14, 71-86. (Pubitemid 34140399)
21. Fotin, A., Cheng, Y., Sliz, P., Grigorieff, N., Harrison, S.C., Kirchhausen, T., and, Walz, T., (2004) Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature, 432, 573-579. (Pubitemid 39626257)
22. Fujimoto, M., Arimura, S., Nakazono, M., and, Tsutsumi, N., (2008) Arabidopsis dynamin-related protein DRP2B is co-localized with DRP1A on the leading edge of the forming cell plate. Plant Cell Rep. 27, 1581-1586.
23. Fujimoto, M., Arimura, S., Ueda, T., Takanashi, H., Hayashi, Y., Nakano, A., and, Tsutsumi, N., (2010) Arabidopsis dynamin-related proteins DRP2B and DRP1A participate together in clathrin-coated vesicle formation during endocytosis. Proc. Natl Acad. Sci. USA, 107, 6094-6099.
24. Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P., Delbarre, A., Ueda, T., Nakano, A., and, Jürgens, G., (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell, 112, 219-230. (Pubitemid 36144111)
25. Grebe, M., Xu, J., Mobius, W., Ueda, T., Nakano, A., Geuze, H.J., Rook, M.B., and, Scheres, B., (2003) Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr. Biol. 13, 1378-1387. (Pubitemid 37029427)
26. Gürkan, C., Stagg, S.M., Lapointe, P., and, Balch, W.E., (2006) The COPII cage: unifying principles of vesicle coat assembly. Nat. Rev. Mol. Cell Biol. 7, 727-738. (Pubitemid 44450457)
27. Haas, T.J., Sliwinski, M.K., Martinez, D.E., Preuss, M., Ebine, K., Ueda, T., Nielsen, E., Odorizzi, G., and, Otegui, M.S., (2007) The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. Plant Cell, 19, 1295-1312. (Pubitemid 46941655)
28. Hillmer, S., Depta, H., and, Robinson, D.G., (1986) Confirmation of endocytosis in higher plant protoplasts using lectin-gold conjugates. Eur. J. Cell Biol. 41, 142-149.
29. Holstein, S.E., (2002) Clathrin and plant endocytosis. Traffic, 3, 614-620.
30. Holstein, S.E., and, Oliviusson, P., (2005) Sequence analysis of Arabidopsis thaliana E/ANTH-domain-containing proteins: membrane tethers of the clathrin-dependent vesicle budding machinery. Protoplasma, 226, 13-21. (Pubitemid 41464531)
31. Hong, Z., Bednarek, S.Y., Blumwald, E., et al. (2003) A unified nomenclature for Arabidopsis dynamin-related large GTPases based on homology and possible functions. Plant Mol. Biol. 53, 261-265. (Pubitemid 38097958)
32. Jaillais, Y., Fobis-Loisy, I., Miege, C., and, Gaude, T., (2008) Evidence for a sorting endosome in Arabidopsis root cells. Plant J. 53, 237-247.
33. Joachim, S., and, Robinson, D.G., (1984) Endocytosis of cationic ferritin by bean leaf protoplasts. Eur. J. Cell Biol. 34, 212-216.
34. Jung, J.Y., Kim, Y.W., Kwak, J.M., Hwang, J.U., Young, J., Schroeder, J.I., Hwang, I., and, Lee, Y., (2002) Phosphatidylinositol 3- and 4-phosphate are required for normal stomatal movements. Plant Cell, 14, 2399-2412. (Pubitemid 35224840)
35. Jürgens, G., (2005) Cytokinesis in higher plants. Annu. Rev. Plant Biol. 56, 281-299. (Pubitemid 40802411)
36. Kaksonen, M., Toret, C.P., and, Drubin, D.G., (2006) Harnessing actin dynamics for clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 7, 404-414. (Pubitemid 44050094)
37. Kang, B.H., Nielsen, E., Preuss, M.L., Mastronarde, D., and, Staehelin, L.A., (2011) Electron tomography of RabA4b- and PI-4Kbeta1-labeled trans Golgi network compartments in Arabidopsis. Traffic, 12, 313-329.
38. Karasawa, S., Araki, T., Nagai, T., Mizuno, H., and, Miyawaki, A., (2004) Cyan-emitting and orange-emitting fluorescent proteins as a donor/acceptor pair for fluorescence resonance energy transfer. Biochem. J. 381, 307-312. (Pubitemid 38932237)
39. Kitakura, S., Vanneste, S., Robert, S., Löfke, C., Teichmann, T., Tanaka, H., and, Friml, J., (2011) Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell, 21, 1055-1060.
40. Konopka, C.A., Backues, S.K., and, Bednarek, S.Y., (2008) Dynamics of Arabidopsis dynamin-related protein 1C and a clathrin light chain at the plasma membrane. Plant Cell, 20, 1363-1380. (Pubitemid 352844188)
41. Lam, S.K., Siu, C.L., Hillmer, S., Jang, S., An, G., Robinson, D.G., and, Jiang, L., (2007) Rice SCAMP1 defines clathrin-coated, trans-Golgi-located tubular-vesicular structures as an early endosome in tobacco BY-2 cells. Plant Cell, 19, 296-319. (Pubitemid 46852718)
42. Lee, S.H., Jin, J.B., Song, J., Min, M.K., Park, D.S., Kim, Y.W., and, Hwang, I., (2002) The intermolecular interaction between the PH domain and the C-terminal domain of Arabidopsis dynamin-like 6 determines lipid binding specificity. J. Biol. Chem. 277, 31842-31849. (Pubitemid 34968991)
43. Liu, S.H., Wong, M.L., Craik, C.S., and, Brodsky, F.M., (1995) Regulation of clathrin assembly and trimerization defined using recombinant triskelion hubs. Cell, 83, 257-267.
44. Mersey, B.G., Griffing, L.R., Rennie, P.J., and, Fowke, L.C., (1985) The isolation of coated vesicles from protoplasts of soybean. Planta, 163, 317.
45. Murashige, T., and, Skoog, F., (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
46. Naramoto, S., Kleine-Vehn, J., Robert, S., et al. (2010) ADP-ribosylation factor machinery mediates endocytosis in plant cells. Proc. Natl Acad. Sci. USA, 107, 21890-21895.
47. Newcomb, E.H., (1980) Coated vesicles: their occurrence in different plant cell types. In Coated Vesicles (, Ockleford, C.Y., and, Whyte, A., eds). Cambridge: Cambridge University Press, pp. 55-68.
48. Nielsen, E., Cheung, A.Y., and, Ueda, T., (2008) The regulatory RAB and ARF GTPases for vesicular trafficking. Plant Physiol. 147, 1516-1526. (Pubitemid 352844198)
49. Otegui, M.S., Mastronarde, D.N., Kang, B.H., Bednarek, S.Y., and, Staehelin, L.A., (2001) Three-dimensional analysis of syncytial-type cell plates during endosperm cellularization visualized by high resolution electron tomography. Plant Cell, 13, 2033-2051. (Pubitemid 32919019)
50. Owen, D.J., Collins, B.M., and, Evans, P.R., (2004) Adaptors for clathrin coats: structure and function. Annu. Rev. Cell. Dev. Biol. 20, 153-191. (Pubitemid 39488636)
51. Reichardt, I., Stierhof, Y.D., Mayer, U., Richter, S., Schwarz, H., Schumacher, K., and, Jurgens, G., (2007) Plant cytokinesis requires de novo secretory trafficking but not endocytosis. Curr. Biol. 17, 2047-2053. (Pubitemid 350180466)
52. Richter, S., Geldner, N., Schrader, J., Wolters, H., Stierhof, Y.D., Rios, G., Koncz, C., Robinson, D.G., and, Jurgens, G., (2007) Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature, 448, 488-492. (Pubitemid 47123513)
53. Robatzek, S., Chinchilla, D., and, Boller, T., (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20, 537-542. (Pubitemid 43345320)
54. Robert, S., Kleine-Vehn, J., Barbez, E., et al. (2010) ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell, 143, 111-121.
55. Robinson, D.G., Langhans, M., Saint-Jore-Dupas, C., and, Hawes, C., (2008) BFA effects are tissue and not just plant specific. Trends Plant Sci. 13, 405-408.
56. Robinson, D.G., Scheuring, D., Naramoto, S., and, Friml, J., (2011) ARF1 localizes to the Golgi and the trans-Golgi network. Plant Cell, 23, 846-849 author reply 849-850.
57. Roth, T.F., and, Porter, K.R., (1964) Yolk protein uptake in the oocyte of the mosquito Aedes aegypti. L. J. Cell Biol. 20, 313-332.
58. Sachse, M., Urbé, S., Oorschot, V., Strous, G.J., and, Klumperman, J., (2002) Bilayered clathrin coats on endosomal vacuoles are involved in protein sorting toward lysosomes. Mol. Biol. Cell, 13, 1313-1328. (Pubitemid 34309625)
59. Saint-Jore, C.M., Evins, J., Batoko, H., Brandizzi, F., Moore, I., and, Hawes, C., (2002) Redistribution of membrane proteins between the Golgi apparatus and endoplasmic reticulum in plants is reversible and not dependent on cytoskeletal networks. Plant J. 29, 661-678. (Pubitemid 34248756)
60. Samuels, A.L., Giddings, T.H. Jr, and, Staehelin, L.A., (1995) Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J. Cell Biol. 130, 1345-1357.
61. Satiat-Jeunemaitre, B., Cole, L., Bourett, T., Howard, R., and, Hawes, C., (1996) Brefeldin A effects in plant and fungal cells: something new about vesicle trafficking? J. Microsc. 181, 162-177. (Pubitemid 26099980)
62. Scheele, U., and, Holstein, S.E., (2002) Functional evidence for the identification of an Arabidopsis clathrin light chain polypeptide. FEBS Lett. 514, 355-360. (Pubitemid 34273969)
63. Sciaky, N., Presley, J., Smith, C., Zaal, K.J., Cole, N., Moreira, J.E., Terasaki, M., Siggia, E., and, Lippincott-Schwartz, J., (1997) Golgi tubule traffic and the effects of brefeldin A visualized in living cells. J. Cell Biol. 139, 1137-1155. (Pubitemid 27523203)
64. Seguí-Simarro, J.M., Austin, J.R. II, White, E.A., and, Staehelin, L.A., (2004) Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell, 16, 836-856. (Pubitemid 38459206)
65. Staehelin, L.A., and, Moore, I., (1995) The plant Golgi apparatus: structure, functional organization and trafficking mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 261-288.
66. Stierhof, Y.D., and, El Kasmi, F., (2010) Strategies to improve the antigenicity, ultrastructure preservation and visibility of trafficking compartments in Arabidopsis tissue. Eur. J. Cell Biol. 89, 285-297.
67. Tahara, H., Yokota, E., Igarashi, H., Orii, H., Yao, M., Sonobe, S., Hashimoto, T., Hussey, P.J., and, Shimmen, T., (2007) Clathrin is involved in organization of mitotic spindle and phragmoplast as well as in endocytosis in tobacco cell cultures. Protoplasma, 230, 1-11. (Pubitemid 46391115)
68. Takano, J., Miwa, K., Yuan, L., von Wiren, N., and, Fujiwara, T., (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc. Natl Acad. Sci. USA, 102, 12276-12281. (Pubitemid 41291165)
69. Tanchak, M.A., Griffing, L.R., Mersey, B.G., and, Fowke, L.C., (1984) Endocytosis of cationized ferritin by coated vesicles of soybean protoplasts. Planta, 162, 481-486.
70. Teh, O.K., and, Moore, I., (2007) An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature, 448, 493-496. (Pubitemid 47123523)
71. Traub, L.M., (2009) Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat. Rev. Mol. Cell Biol. 10, 583-596.
72. Uemura, T., Ueda, T., Ohniwa, R.L., Nakano, A., Takeyasu, K., and, Sato, M.H., (2004) Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct. Funct. 29, 49-65. (Pubitemid 39206720)
73. Van Damme, D., Gadeyne, A., Vanstraelen, M., Inzé, D., Van Montagu, M.C., De Jaeger, G., Russinova, E., and, Geelen, D., (2011) Adaptin-like protein TPLATE and clathrin recruitment during plant somatic cytokinesis occurs via two distinct pathways. Proc. Natl Acad. Sci. USA, 108, 615-620.
74. Vernoud, V., Horton, A.C., Yang, Z., and, Nielsen, E., (2003) Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol. 131, 1191-1208. (Pubitemid 36405305)
75. Viotti, C., Bubeck, J., Stierhof, Y.D., et al. (2010) Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell, 22, 1344-1357.
76. Wang, Y.J., Wang, J., Sun, H.Q., Martinez, M., Sun, Y.X., Macia, E., Kirchhausen, T., Albanesi, J.P., Roth, M.G., and, Yin, H.L., (2003) Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell, 114, 299-310. (Pubitemid 36962929)
77. Wang, J., Cai, Y., Miao, Y., Lam, S.K., and, Jiang, L., (2009) Wortmannin induces homotypic fusion of plant prevacuolar compartments. J Exp Bot. 60, 3075-3083.
78. Yamada, K., Fuji, K., Shimada, T., Nishimura, M., and, Hara-Nishimura, I., (2005) Endosomal proteases facilitate the fusion of endosomes with vacuoles at the final step of the endocytotic pathway. Plant J. 41, 888-898. (Pubitemid 40398717)