Browse > Article

A WD40 Repeat Protein, Arabidopsis Sec13 Homolog 1, May Play a Role in Vacuolar Trafficking by Controlling the Membrane Association of AtDRP2A  

Lee, Myoung Hui (Center for Plant Intracellular Trafficking and Division of Molecular and Life Sciences, Pohang University of Science and Technology)
Lee, Sung Hoon (Center for Plant Intracellular Trafficking and Division of Molecular and Life Sciences, Pohang University of Science and Technology)
Kim, Heyran (Center for Plant Intracellular Trafficking and Division of Molecular and Life Sciences, Pohang University of Science and Technology)
Jin, Jing Bo (Center for Plant Intracellular Trafficking and Division of Molecular and Life Sciences, Pohang University of Science and Technology)
Kim, Dae Heon (Center for Plant Intracellular Trafficking and Division of Molecular and Life Sciences, Pohang University of Science and Technology)
Hwang, Inhwan (Center for Plant Intracellular Trafficking and Division of Molecular and Life Sciences, Pohang University of Science and Technology)
Abstract
Dynamin-related protein 2A (AtDRP2A, formally ADL6), a member of the dynamin family, is critical for protein trafficking from the TGN to the central vacuole. However, the mechanism controlling its activity is not well understood in plant cells. We isolated Arabidopsis sec13 homolog1 (AtSeh1) that interacts with AtDRP2A by a yeast two-hybrid screening. AtSeh1 has four WD40 motifs and amino acid sequence homology to Sec13, a component of COPII vesicles. Coimmunoprecipitation and protein pull-down experiments demonstrated specific interaction between AtSeh1 and AtDRP2A. AtSeh1 bound to the pleckstrin homology domain of AtDRP2A in competition with the C-terminal domain of the latter, and this resulted in inhibition of the interaction between AtDRP2A and PtdIns3P in vitro. AtSeh1 localized to multiple locations: the nucleus, the prevacuolar compartment and the Golgi complex. Based on these results we propose that AtSeh1 plays a role in regulating cycling of AtDRP2A between membrane-bound and soluble forms.
Keywords
Arabidopsis Sec13 Homolog; Dynamin-related Protein 2A; Phospholipid Binding; Protein-Protein Interaction;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
Times Cited By Web Of Science : 9  (Related Records In Web of Science)
연도 인용수 순위
1 Babst, M. (2005) A protein's final ESCRT. Traffic 6, 2-9
2 Burd, C. G., Mustol, P. A., Schu, P. V., and Emr, S. D. (1996) A yeast protein related to a mammalian Ras-binding protein, Vps9p, is required for localization of vacuolar proteins. Mol. Cell Biol. 16, 2369-2377   DOI
3 Corvera, S., D'Arrigo, A., and Stenmark, H. (1999) Phosphoinositides in membrane traffic. Curr. Opin. Cell Biol. 11, 460-465   DOI   ScienceOn
4 daSilva, L. L., Taylor, J. P., Hadlington, J. L., Hanton, S. L., Snowden, C. J., et al. (2005) Receptor salvage from the prevacuolar compartment is essential for efficient vacuolar protein targeting. Plant Cell 17, 132-148   DOI   ScienceOn
5 Schekman, R. and Orci, L. (1996) Coat proteins and vesicle budding. Science 271, 1526-1533   DOI
6 Schmid, S. L. (1997) Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu. Rev. Biochem. 66, 511-548   DOI   ScienceOn
7 Shimada, T., Kuroyanagi, M., Nishimura, M., Hara-Nishimura, I. (1997) A pumpkin 72-kDa membrane protein of precursoraccumulating vesicles has characteristics of a vacuolar sorting receptor. Plant Cell Physiol. 38, 1414-420   DOI   ScienceOn
8 Siniossoglou, S., Wimmer, C., Rieger, M., Doye, V., Tekotte, H., et al. (1996) A novel complex of nucleoporins, which includes Sec13p and a Sec13p homolog, is essential for normal nuclear pores. Cell 84, 265-275   DOI   ScienceOn
9 Fields, S. and Song, O. (1989) A novel genetic system to detect protein-protein interactions. Nature 340, 245-256   DOI   ScienceOn
10 Harlow, E. and Lane, D. (1988) Antibodies: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
11 Ghosh, P. and Kornfeld, S. (2004) The GGA proteins: key players in protein sorting at the trans-Golgi network. Eur. J. Cell Biol. 83, 257-262   DOI   ScienceOn
12 Zerial, M. and McBride, H. (2001) Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-117   DOI   ScienceOn
13 Kirsch, T., Paris, N., Butler, J. M., Beevers, L., and Rogers, J. C. (1994) Purification and initial characterization of a potential plant vacuolar targeting receptor. Proc. Natl. Acad. Sci. USA 91, 3403-3407
14 Wang, L. H., Sudhof, T. C., and Anderson, R. G. (1995) The appendage domain of alpha-adaptin is a high affinity binding site for dynamin. J. Biol. Chem. 270, 10079-10083   DOI
15 Eitzen, G. (2003) Actin remodeling to facilitate membrane fusion. Biochim. Biophys. Acta 1641, 175-181   DOI   ScienceOn
16 Marks, B., Stowell, M. H., Vallis, Y., Mills, I. G., Gibson, A., et al. (2001) GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410, 231-235   DOI   ScienceOn
17 Modregger, J., Ritter, B., Witter, B., Paulsson, M., and Plomann, M. (2000) All three PACSIN isoforms bind to endocytic proteins and inhibit endocytosis. J. Cell Sci. 113, 4511-4521
18 Patki, V., Virbasius, J., Lane, W. S., Toh, B. H., Shpetner, H. S., et al. (1997) Identification of an early endosomal protein regulated by phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 94, 7326-7330
19 Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant 15, 473-497   DOI
20 Tse, Y. C., Mo, B., Hillmer, S., Zhao, M., Lo, S. W., et al. (2004) Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell 16, 672-693   DOI   ScienceOn
21 Obar, R. A., Collins, C. A., Hammarback, J. A., Shpetner, H. S., and Vallee, R. B. (1990) Molecular cloning of the microtubule- associated mechanochemical enzyme dynamin reveals homology with a new family of GTP-binding proteins. Nature 347, 256-261   DOI   ScienceOn
22 Fontoura, B. M., Blobel, G., and Matunis, M. J. (1999) A conserved biogenesis pathway for nucleoporins: proteolytic processing of a 186-Kilodalton precursor generates Nup98 and the novel nucleoporin, Nup96. J. Cell Biol. 144, 1097-1112   DOI   ScienceOn
23 Jurgens, G. (2004) Membrane trafficking in plants. Annu. Rev. Cell Dev. Biol. 20, 481-504   DOI   ScienceOn
24 Pryer, N. K., Salama, N. R., Schekman, R., and Kaiser, C. A. (1993) Cytosolic Sec13p complex is required for vesicle formation from the endoplasmic reticulum in vitro. J. Cell Biol. 120, 865-875   DOI   ScienceOn
25 Robinson, M. S. and Bonifacino, J. S. (2001) Adaptor-related proteins. Curr. Opin. Cell Biol. 13, 444-453   DOI   ScienceOn
26 Stepp, J. D., Huang, K., and Lemmon, S. K. (1997) The yeast adaptor protein complex, AP-3, is essential for the efficient delivery of alkaline phosphatase by the alternate pathway to the vacuole. J. Cell Biol. 139, 1761-1774   DOI   ScienceOn
27 Paris, N. and Neuhaus, J. M. (2002) BP-80 as a vacuolar sorting receptor. Plant Mol. Biol. 50, 903-914   DOI   ScienceOn
28 Schmidt, A., Wolde, M., Thiele, C., Fest, W., Kratzin, H., et al. (1999) Endophilin I mediates synaptic vesicle formation by transfer of arachidonate to lysophosphatidic acid. Nature 401, 133-141   DOI   ScienceOn
29 Shim, J. and Lee, J. (2005) The AP-3 clathrin-associated complex is essential for embryonic and larval development in Caenorhabditis elegans. Mol. Cells 19, 452-457
30 Lam, B. C., Sage, T. L., Bianchi, F., and Blumwald, E. (2002) Regulation of ADL6 activity by its associated molecular network. Plant J. 31, 565-576   DOI   ScienceOn
31 Sengar, A. S., Wang, W., Bishay, J., Cohen, S., and Egan, S. E. (1999) The EH and SH3 domain Ese proteins regulate endocytosis by linking to dynamin and Eps15. EMBO J. 18, 1159- 1171   DOI   ScienceOn
32 Barlowe, C., Orci, L., Yeung, T., Hosobuchi, M., Hamamoto, S., et al. (1994) COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77, 895-907   DOI   ScienceOn
33 Foster-Barber, A. and Bishop, J. M. (1998) Src interacts with dynamin and synapsin in neuronal cells. Proc. Natl. Acad. Sci. USA 95, 4673-4677
34 Denisenko, O., Shnyreva, M., Suzuki, H., and Bomsztyk, K. (1998) Point mutations in the WD40 domain of Eed block its interaction with Ezh2. Mol. Cell Biol. 18, 5634-5642   DOI
35 Bassham, D. C. and Raikhel, N. V. (1999) The pre-vacuolar t- SNARE AtPEP12p forms a 20S complex that dissociates in the presence of ATP. Plant J. 19, 599-603   DOI   ScienceOn
36 Kim, H., Park, M., Kim, S. J., and Hwang, I. (2005) Actin filaments play a critical role in vacuolar trafficking at the Golgi complex in plant cells. Plant Cell 17, 888-902   DOI   ScienceOn
37 Ferguson, K. M., Lemmon, M. A., Schlessinger, J., and Sigler, P. B. (1994) Crystal structure at 2.2 A resolution of the pleckstrin homology domain from human dynamin. Cell 79, 199- 209   DOI   ScienceOn
38 Piper, R. C. and Luzio, J. P. (2001) Late endosomes: sorting and partitioning in multivesicular bodies. Traffic 2, 612-621   DOI   ScienceOn
39 Herskovits, J. S., Burgess, C. C., Obar, R. A., and Vallee, R. B. (1993) Effects of mutant rat dynamin on endocytosis. J. Cell Biol. 122, 565-578   DOI   ScienceOn
40 Sweitzer, S. M. and Hinshaw, J. E. (1998) Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93, 1021-1029   DOI   ScienceOn
41 Fischer von Mollard, G. and Stevens, T. H. (1999) The Saccharomyces cerevisiae v-SNARE Vti1p is required for multiple membrane transport pathways to the vacuole. Mol. Biol. Cell 10, 1719-1732   DOI
42 Traub, L. M. (2005) Common principles in clathrin-mediated sorting at the Golgi and the plasma membrane. Biochim. Biophys. Acta 1744, 415-437   DOI   ScienceOn
43 Gout, I., Dhand, R., Hiles, I. D., Fry, M. J., Panayotou, G., et al. (1993) The GTPase dynamin binds to and is activated by a subset of SH3 domains. Cell 75, 25-36   DOI
44 Jin, J. B., Kim, Y. A, Kim, S. J., Lee, S. H., Kim, D. H., et al. (2001) 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   DOI   ScienceOn
45 Kim, D. H., Eu, Y.-J., Yoo, C. M., Kim, Y. W., Pih, K. T., et al. (2001) Trafficking of phosphatidylinositol 3-phosphate from the trans-Golgi network to the lumen of the central vacuole in plant cells. Plant Cell 13, 287-301   DOI   ScienceOn
46 Seedorf, K., Kostka, G., Lammers, R., Bashkin, P., Daly, R., et al. (1994) Dynamin binds to SH3 domains of phospholipase C gamma and GRB-2. J. Biol. Chem. 269, 16009-16014
47 Bassham, D. C. and Raikhel, N. V. (2000) Unique features of the plant vacuolar sorting machinery. Curr. Opin. Cell Biol. 12, 491-495   DOI   ScienceOn
48 Carter, C. J., Bednarek, S. Y., and Raikhel, N. V. (2004) Membrane trafficking in plants: new discoveries and approaches. Curr. Opin. Plant Biol. 7, 701-707   DOI   ScienceOn
49 Park, M., Lee, D., Lee, G. J., and Hwang, I. (2005) AtRMR1 functions as a cargo receptor for protein trafficking to the protein storage vacuole. J. Cell Biol. 170, 757-767   DOI   ScienceOn
50 Zheng, H., von Mollard, G. F., Kovaleva, V., Stevens, T. H., and Raikhel, N. V. (1999) The plant vesicle-associated SNARE AtVTI1a likely mediates vesicle transport from the trans- Golgi network to the prevacuolar compartment. Mol. Biol. Cell 10, 2251-2264   DOI
51 Park, M., Kim, S. J., Vitale, A., and Hwang, I. (2004) Identification of the protein storage vacuole and protein targeting to the vacuole in leaf cells of three plant species. Plant Physiol. 134, 625-639   DOI   ScienceOn
52 Sever, S., Muhlberg, A. B., and Schmid, S. L. (1999) Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature 398, 481-486   DOI   ScienceOn
53 Conibear, E. and Stevens, T. H. (1998) Multiple sorting pathways between the late Golgi and the vacuole in yeast. Biochim. Biophys. Acta 1404, 211-230   DOI
54 Gu, F., Crump, C. M., and Thomas, G. (2001) Trans-Golgi network sorting. Cell Mol. Life Sci. 58, 1067-1084   DOI   ScienceOn
55 Hohl, I., Robinson, D. G., Chrispeels, M. J., and Hinz, G. (1996) Transport of storage proteins to the vacuole is mediated by vesicles without a clathrin coat. J. Cell Sci. 109, 2539-2550
56 Takei, K., Slepnev, V. I., Haucke, V., and De Camilli, P. (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat. Cell Biol. 1, 33-39   DOI   ScienceOn
57 Okamoto, M., Schoch, S., and Sudhof, T. C. (1999) EHSH1/ intersectin, a protein that contains EH and SH3 domains and binds to dynamin and SNAP-25. A protein connection between exocytosis and endocytosis? J. Biol. Chem. 274, 18446- 18454   DOI
58 Schroder, S. and Ungewickell, E. (1991) Subunit interaction and function of clathrin-coated vesicle adaptors from the Golgi and the plasma membrane. J. Biol. Chem. 266, 7910-7908
59 Bassham, D. C., Sanderfoot, A. A., Kovaleva, V., Zheng, H., and Raikhel, N. V. (2000) AtVPS45 complex formation at the trans-Golgi network. Mol. Biol. Cell 11, 2251-2265   DOI
60 Ahmed, S. U., Rojo, E., Kovaleva, V., Venkataraman, S., Dombrowski, J. E., et al. (2000) The plant vacuolar sorting receptor AtELP is involved in transport of NH(2)-terminal propeptide- containing vacuolar proteins in Arabidopsis thaliana. J. Cell Biol. 149, 1335-1344   DOI   ScienceOn
61 Hinshaw, J. E. (2000) Dynamin and its role in membrane fission. Annu. Rev. Cell Dev. Biol. 16, 483-519   DOI   ScienceOn
62 Hinshaw, J. E. and Schmid, S. L. (1995) Dynamin selfassembles into rings suggesting a mechanism for coated vesicle budding. Nature 374, 190-192   DOI   ScienceOn
63 Rapoport, T. A. (1986) Protein translocation across and integration into membranes. CRC Crit. Rev. Biochem. 20, 73-137   DOI
64 James, P., Halladay, J., and Craig, E. A. (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144, 1425-1436
65 Lai, M. M., Hong, J. J., Ruggiero, A. M., Burnett, P. E., Slepnev, V. I., et al. (1999) The calcineurin-dynamin 1 complex as a calcium sensor for synaptic vesicle endocytosis. J. Biol. Chem. 274, 25963-25966   DOI
66 Miki, H., Miura, K., Matuoka, K., Nakata, T., Hirokawa, N., et al. (1994) Association of Ash/Grb-2 with dynamin through the Src homology 3 domain. J. Biol. Chem. 269, 5489-5492