A novel endosomal sorting complex required for transport (ESCRT) component in arabidopsis thaliana controls cell expansion and development

Journal of Biological Chemistry

Volumn 289, Issue 8, 2014, Pages 4980-4988

  Reyes, Francisca C ^a,b   Buono, Rafael A ^a   Roschzttardtz, Hannetz ^a   Di Rubbo, Simone ^c   Yeun, Li Huey ^a   Russinova, Eugenia ^c   Otegui, Marisa S ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSIDAD ANDRÉS BELLO   (Chile)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

ARABIDOPSIS THALIANA; ATP-ASE ACTIVITY; CELL EXPANSION; CELLULAR PROCESS; ENDOSOMAL SORTING COMPLEX REQUIRED FOR TRANSPORTS; MEMBRANE REMODELING; REGULATORY MECHANISM;

PLANTS (BOTANY);

CARRIER PROTEINS AND BINDING PROTEINS; ESCRT PROTEIN; LIP5 PROTEIN; PROTEIN PROS; REGULATOR PROTEIN; SUPPRESSOR OF K+ TRANSPORT GROWTH DEFECT; UNCLASSIFIED DRUG; VACUOLAR PROTEIN SORTING 4;

ARABIDOPSIS THALIANA; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL EXPANSION; CELL MUTANT; CELL SELECTION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE SILENCING; HETEROLOGOUS EXPRESSION; IN VITRO STUDY; MICROTUBULE INTERACTING AND TRANSPORT; MIT INTERACTING MOTIF; NONHUMAN; PLANT DEVELOPMENT; PLANT GENE; PRIORITY JOURNAL; PROS GENE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION;

CELL BIOLOGY; CELL GROWTH; ENDOSOMES; ENZYME PURIFICATION; GENE SILENCING; MEMBRANE TRAFFICKING; PLANT; PROTEIN MOTIFS; PROTEIN PURIFICATION;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; CELL PROLIFERATION; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; MOLECULAR SEQUENCE DATA; MULTIVESICULAR BODIES; MUTATION; PLANT DEVELOPMENT; PLANT LEAVES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPECIES SPECIFICITY;

EID: 84894453335     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.529685     Document Type: Article

References (40)

1. Elia, N., Sougrat, R., Spurlin, T. A., Hurley, J. H., and Lippincott-Schwartz, J. (2011) Dynamics of endosomal sorting complex required for transport (ESCRT) machinery during cytokinesis and its role in abscission. Proc. Natl. Acad. Sci. U.S.A. 108, 4846-4851
2. Guizetti, J., Schermelleh, L., Mäntler, J., Maar, S., Poser, I., Leonhardt, H., Müller-Reichert, T., and Gerlich, D. W. (2011) Cortical constriction during abscission involves helices of ESCRT-III-dependent filaments. Science 331, 1616-1620
3. Wollert, T., Wunder, C., Lippincott-Schwartz, J., and Hurley, J. H. (2009) Membrane scission by the ESCRT-III complex. Nature 458, 172-177
4. Fyfe, I., Schuh, A. L., Edwardson, J. M., and Audhya, A. (2011) Association of ESCRT-II with VPS20 generates a curvature sensitive protein complex capable of nucleating filaments of ESCRT-III. J. Biol. Chem. 286, 34262-34270
5. Henne, W. M., Buchkovich, N. J., Zhao, Y., and Emr, S. D. (2012) The endosomal sorting complex ESCRT-II mediates the assembly and architecture of ESCRT-III Helices. Cell 151, 356-371
6. Babst, M., Davies, B. A., and Katzmann, D. J. (2011) Regulation of Vps4 during MVB sorting and cytokinesis. Traffic 12, 1298-1305
7. Nickerson, D. P., West, M., and Odorizzi, G. (2006) Did2 coordinates Vps4-mediated dissociation of ESCRT-III from endosomes. J. Cell Biol. 175, 715-720
8. Stauffer, D. R., Howard, T. L., Nyun, T., and Hollenberg, S. M. (2001) CHMP1 is a novel nuclear matrix protein affecting chromatin structure and cell-cycle progression. J. Cell Sci. 114, 2383-2393
9. Shim, J. H., Xiao, C., Hayden, M. S., Lee, K. Y., Trombetta, E. S., Pypaert, M., Nara, A., Yoshimori, T., Wilm, B., Erdjument-Bromage, H., Tempst, P., Hogan, B. L., Mellman, I., and Ghosh, S. (2006) CHMP5 is essential for late endosome function and down-regulation of receptor signaling during mouse embryogenesis. J. Cell Biol. 172, 1045-1056
10. Xiao, J. (2008) Structural basis of Vta1 function in the multivesicular body sorting pathway. Dev. Cell 14, 37-49
11. Yang, Z., Vild, C., Ju, J., Zhang, X., Liu, J., Shen, J., Zhao, B., Lan, W., Gong, F., Liu, M., Cao, C., and Xu, Z. (2012) Structural basis of molecular recognition between ESCRT-III like protein Vps60 and AAA-ATPase regulator Vta1 in the multi-vesicular body pathway. J. Biol. Chem. 287, 43899-43908
12. Dimaano, C., Jones, C. B., Hanono, A., Curtiss, M., and Babst, M. (2008) Ist1 regulates Vps4 localization and assembly. Mol. Biol. Cell 19, 465-474
13. Rue, S. M., Mattei, S., Saksena, S., and Emr, S. D. (2008) Novel ist1-did2 complex functions at a late step in multivesicular body sorting. Mol. Biol. Cell 19, 475-484
14. Ghazi-Tabatabai, S., Saksena, S., Short, J. M., Pobbati, A. V., Veprintsev, D. B., Crowther, R. A., Emr, S. D., Egelman, E. H., and Williams, R. L. (2008) Structure and disassembly of filaments formed by the ESCRT-III subunit Vps24. Structure 16, 1345-1356
15. Leung, K. F., Dacks, J. B., and Field, M. C. (2008) Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic 9, 1698-1716
16. Winter, V., and Hauser, M.-T. (2006) Exploring the ESCRTing machinery in eukaryotes. Trends Plant Sci. 11, 115-123
17. Shahriari, M., Richter, K., Keshavaiah, C., Sabovljevic, A., Huelskamp, M., and Schellmann, S. (2011) The Arabidopsis ESCRT protein-protein interaction network. Plant Mol. Biol. 76, 85-96
18. Shahriari, M., Keshavaiah, C., Scheuring, D., Sabovljevic, A., Pimpl, P., Häusler, R. E., Hülskamp, M., and Schellmann, S. (2010) The AAA-type ATPase AtSKD1 contributes to vacuolar maintenance of Arabidopsis thaliana. Plant J. 64, 71-85
19. Spitzer, C., Reyes, F. C., Buono, R., Sliwinski, M. K., Haas, T. J., and Otegui, M. S. (2009) The ESCRT-related CHMP1A and B proteins mediate multivesicular body sorting of auxin carriers in Arabidopsis and are required for plant development. Plant Cell 21, 749-766
20. Haas, T. J., Sliwinski, M. K., Martínez, 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
21. Spitzer, C., Schellmann, S., Sabovljevic, A., Shahriari, M., Keshavaiah, C., Bechtold, N., Herzog, M., Müller, S., Hanisch, F. G., and Hulskamp, M. (2006) The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis. Development 133, 4679-4689
22. Richardson, L. G. L., Howard, A. S. M., Khuu, N., Gidda, S. K., McCartney, A., Morphy, B. J., and Mullen, R. T. (2011) Protein-protein interaction network and subcellular localization of the Arabidopsis thaliana ESCRT machinery. Frontiers Plant Sci. 2, 20
23. Azmi, I., Davies, B., Dimaano, C., Payne, J., Eckert, D., Babst, M., and Katzmann, D. J. (2006) Recycling of ESCRTs by the AAA-ATPase Vps4 is regulated by a conserved VSL region in Vta1. J. Cell Biol. 172, 705-717
24. Babst, M., Sato, T. K., Banta, L. M., and Emr, S. D. (1997) Endosomal transport function in yeast requires a novel AAA-type ATPase, Vps4p. EMBO J. 16, 1820-1831
25. Bracha-Drori, K., Shichrur, K., Katz, A., Oliva, M., Angelovici, R., Yalovsky, S., and Ohad, N. (2004) Detection of protein-protein interactions in plants using bimolecular fluorescence complementation. Plant J. 40, 419-427
26. Yoo, S.-D., Cho, Y.-H., and Sheen, J. (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protocols 2, 1565-1572
27. von Arnim, A. G., Deng, X. W., and Stacey, M. G. (1998) Cloning vectors for the expression of green fluorescent protein fusion proteins in transgenic plants. Gene 221, 35-43
28. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J. Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., and Cardona, A. (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9, 676-682
29. Schwab, R., Ossowski, S., Riester, M., Warthmann, N., and Weigel, D. (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18, 1121-1133
30. Shim, S., Kimpler, L. A., and Hanson, P. I. (2007) Structure/function analysis of four core ESCRT-III proteins reveals common regulatory role for extreme C-terminal domain. Traffic 8, 1068-1079
31. Lata, S., Roessle, M., Solomons, J., Jamin, M., Gottlinger, H. G., Svergun, D. I., and Weissenhorn, W. (2008) Structural basis for autoinhibition of ESCRT-III CHMP3. J. Mol. Biol. 378, 816-825
32. Skalicky, J. J., Arii, J., Wenzel, D. M., Stubblefield, W.-M. B., Katsuyama, A., Uter, N. T., Bajorek, M., Myszka, D. G., and Sundquist, W. I. (2012) Interactions of the human LIP5 regulatory protein with endosomal sorting complexes required for transport. J. Biol. Chem. 287, 43910-43926
33. Obita, T., Saksena, S., Ghazi-Tabatabai, S., Gill, D. J., Perisic, O., Emr, S. D., and Williams, R. L. (2007) Structural basis for selective recognition of ESCRT-III by the AAA ATPase Vps4. Nature 449, 735-739
34. Azmi, I. F., Davies, B. A., Xiao, J., Babst, M., Xu, Z., and Katzmann, D. J. (2008) ESCRT-III family members stimulate Vps4 ATPase activity directly or via Vta1. Dev. Cell 14, 50-61
35. Merrill, S. A., and Hanson, P. I. (2010) Activation of human VPS4A by ESCRT-III proteins reveals ability of substrates to relieve enzyme autoinhibition. J. Biol. Chem. 285, 35428-35438
36. Yang, D., and Hurley, J. H. (2010) Structural role of the Vps4-Vta1 interface in ESCRT-III recycling. Structure 18, 976-984
37. Nafisi, M., Goregaoker, S., Botanga, C. J., Glawischnig, E., Olsen, C. E., Halkier, B. A., and Glazebrook, J. (2007) Arabidopsis cytochrome P450 monooxygenase 71A13 catalyzes the conversion of indole-3-acetaldoxime in camalexin synthesis. Plant Cell 19, 2039-2052
38. Rusten, T. E., Vaccari, T., and Stenmark, H. (2012) Shaping development with ESCRTs. Nat. Cell Biol. 14, 38-45
39. Zamborlini, A., Usami, Y., Radoshitzky, S. R., Popova, E., Palu, G., and Göttlinger, H. (2006) Release of autoinhibition converts ESCRT-III components into potent inhibitors of HIV-1 budding. Proc. Natl. Acad. Sci. U.S.A. 103, 19140-19145
40. Katsiarimpa, A., Kalinowska, K., Anzenberger, F., Weis, C., Ostertag, M., Tsutsumi, C., Schwechheimer, C., Brunner, F., Hückelhoven, R., and Isono, E. (2013) The deubiquitinating enzyme AMSH1 and the ESCRT-III subunit VPS2.1 are required for autophagic degradation in Arabidopsis. Plant Cell 25, 2236-2252