The AP-1 μ adaptin is required for KNOLLE localization at the cell plate to mediate cytokinesis in arabidopsis

Plant and Cell Physiology

Volumn 54, Issue 6, 2013, Pages 838-847

  Teh, Ooi Kock ^a   Shimono, Yuki ^a   Shirakawa, Makoto ^a   Fukao, Yoichiro ^b   Tamura, Kentaro ^a   Shimada, Tomoo ^a   Hara Nishimura, Ikuko ^a  

^a KYOTO UNIVERSITY   (Japan)

^b NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

Adaptin; Adaptor protein complex; Arabidopsis thaliana; Cytokinesis; KNOLLE; Trans Golgi network

Indexed keywords

ADAPTIN; ADAPTOR PROTEIN; AP1M2 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; BREFELDIN A; CONCANAMYCIN A; DIMETHYL SULFOXIDE; GREEN FLUORESCENT PROTEIN; KNOLLE PROTEIN, ARABIDOPSIS; MACROLIDE; SYNTAXIN;

ADAPTOR PROTEIN COMPLEX; ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; CHEMISTRY; CYTOKINESIS; CYTOLOGY; DRUG EFFECT; ENDOCYTOSIS; GROWTH, DEVELOPMENT AND AGING; KNOLLE; MASS SPECTROMETRY; METABOLISM; MUTATION; PLANT DEVELOPMENT; PROTEIN TRANSPORT; SEEDLING; TRANS GOLGI NETWORK; ULTRASTRUCTURE;

ADAPTIN; ADAPTOR PROTEIN COMPLEX; ARABIDOPSIS THALIANA; CYTOKINESIS; KNOLLE; TRANS-GOLGI NETWORK;

ADAPTOR PROTEIN COMPLEX 1; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BREFELDIN A; CYTOKINESIS; DIMETHYL SULFOXIDE; ENDOCYTOSIS; GREEN FLUORESCENT PROTEINS; MACROLIDES; MASS SPECTROMETRY; MUTATION; PLANT DEVELOPMENT; PROTEIN TRANSPORT; QA-SNARE PROTEINS; SEEDLING; TRANS-GOLGI NETWORK;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

EID: 84878868384     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pct048     Document Type: Article

References (48)

1. Assaad, F.F., Huet, Y., Mayer, U. and Jurgens, G. (2001) The cytokinesis gene KEULE encodes a Sec1 protein that binds the syntaxin KNOLLE. J. Cell Biol. 152: 531-543.
2. Assaad, F.F., Mayer, U., Wanner, G. and Jurgens, G. (1996) The KEULE gene is involved in cytokinesis in Arabidopsis. Mol. Gen. Genet. 253: 267-277.
3. Bassham, D.C., Brandizzi, F., Otegui, M.S. and Sanderfoot, A.A. (2008) The secretory system of Arabidopsis. The Arabidopsis Book 6: e0116.
4. Boehm, M. and Bonifacino, J.S. (2002) Genetic analyses of adaptin function from yeast to mammals. Gene 286: 175-186.
5. Bolte, S., Talbot, C., Boutte, Y., Catrice, O., Read, N.D. and Satiat-Jeunemaitre, B. (2004) FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J. Microsc. 214: 159-173.
6. Bonifacino, J.S. and Traub, L.M. (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72: 395-447.
7. Chow, C.M., Neto, H., Foucart, C. and Moore, I. (2008) Rab-A2 and Rab-A3 GTPases define a trans-Golgi endosomal membrane domain in Arabidopsis that contributes substantially to the cell plate. Plant Cell 20: 101-123.
8. Dacks, J.B., Poon, P.P. and Field, M.C. (2008) Phylogeny of endocytic components yields insight into the process of nonendosymbiotic organelle evolution. Proc. Natl Acad. Sci. USA 105: 588-593.
9. Dettmer, J., Hong-Hermesdorf, A., Stierhof, Y.D. and Schumacher, K. (2006) Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18: 715-730.
10. Faso, C., Chen, Y.N., Tamura, K., Held, M., Zemelis, S., Marti, L. et al. (2009) A missense mutation in the Arabidopsis COPII coat protein Sec24A induces the formation of clusters of the endoplasmic reticulum and Golgi apparatus. Plant Cell 21: 3655-3671.
11. Feraru, E., Paciorek, T., Feraru, M.I., Zwiewka, M., De Groodt, R., De Rycke, R. et al. (2010) The AP-3 beta adaptin mediates the biogenesis and function of lytic vacuoles in Arabidopsis. Plant Cell 22: 2812-2824.
12. Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P. et al. (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112: 219-230.
13. Geldner, N., Denervaud-Tendon, V., Hyman, D.L., Mayer, U., Stierhof, Y.D. and Chory, J. (2009) Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J. 59: 169-178.
14. Green, R.A., Paluch, E. and Oegema, K. (2012) Cytokinesis in animal cells. Annu. Rev. Cell Dev. Biol. 28: 29-58.
15. Happel, N., Honing, S., Neuhaus, J.M., Paris, N., Robinson, D.G. and Holstein, S.E. (2004) Arabidopsis mu A-adaptin interacts with the tyrosine motif of the vacuolar sorting receptor VSR-PS1. Plant J. 37: 678-693.
16. Heese, M., Gansel, X., Sticher, L., Wick, P., Grebe, M., Granier, F. et al. (2001) Functional characterization of the KNOLLE-interacting t-SNARE AtSNAP33 and its role in plant cytokinesis. J. Cell Biol. 155: 239-249.
17. Hirst, J., Barlow, L.D., Francisco, G.C., Sahlender, D.A., Seaman, M.N., Dacks, J.B. et al. (2011) The fifth adaptor protein complex. PLoS Biol. 9: e1001170.
18. Jaillais, Y., Fobis-Loisy, I., Miege, C., Rollin, C. and Gaude, T. (2006) AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 443: 106-109.
19. Jurgens, G. (2005) Plant cytokinesis: fission by fusion. Trends Cell Biol. 15: 277-283.
20. Kita, A., Sugiura, R., Shoji, H., He, Y., Deng, L., Lu, Y. et al. (2004) Loss of Apm1, the micro1 subunit of the clathrin-associated adaptorprotein-1 complex, causes distinct phenotypes and synthetic lethality with calcineurin deletion in fission yeast. Mol. Biol. Cell 15: 2920-2931.
21. Lauber, M.H., Waizenegger, I., Steinmann, T., Schwarz, H., Mayer, U., Hwang, I. et al. (1997) The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J. Cell Biol. 139: 1485-1493.
22. Lukowitz, W., Mayer, U. and Jurgens, G. (1996) Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84: 61-71.
23. McMahon, H.T. and Boucrot, E. (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell. Biol. 12: 517-533.
24. Meyer, C., Zizioli, D., Lausmann, S., Eskelinen, E.L., Hamann, J., Saftig, P. et al. (2000) mu1A-adaptin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors. EMBO J. 19: 2193-2203.
25. Niihama, M., Takemoto, N., Hashiguchi, Y., Tasaka, M. and Morita, M.T. (2009) ZIP genes encode proteins involved in membrane trafficking of the TGN-PVC/vacuoles. Plant Cell Physiol. 50: 2057-2068.
26. Ohno, H., Stewart, J., Fournier, M.C., Bosshart, H., Rhee, I., Miyatake, S. et al. (1995) Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269: 1872-1875.
27. Park, M., Touihri, S., Muller, I., Mayer, U. and Jurgens, G. (2012) Sec1/Munc18 protein stabilizes fusion-competent syntaxin for membrane fusion in Arabidopsis cytokinesis. Dev. Cell 22: 989-1000.
28. Phan, H.L., Finlay, J.A., Chu, D.S., Tan, P.K., Kirchhausen, T. and Payne, G.S. (1994) The Saccharomyces cerevisiae APS1 gene encodes a homolog of the small subunit of the mammalian clathrin AP-1 complex: evidence for functional interaction with clathrin at the Golgi complex. EMBO J. 13: 1706-1717.
29. Prekeris, R. and Gould, G.W. (2008) Breaking up is hard to do-membrane traffic in cytokinesis. J. Cell Sci. 121: 1569-1576.
30. Reichardt, I., Stierhof, Y.D., Mayer, U., Richter, S., Schwarz, H., Schumacher, K. et al. (2007) Plant cytokinesis requires de novo secretory trafficking but not endocytosis. Curr. Biol. 17: 2047-2053.
31. Robinson, M.S. (2004) Adaptable adaptors for coated vesicles. Trends Cell Biol. 14: 167-174.
32. Robinson, M.S. and Bonifacino, J.S. (2001) Adaptor-related proteins. Curr Opin. Cell Biol. 13: 444-453.
33. Segui-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.
34. Shim, J., Sternberg, P.W. and Lee, J. (2000) Distinct and redundant functions of mu1 medium chains of the AP-1 clathrin-associated protein complex in the nematode Caenorhabditis elegans. Mol. Biol. Cell 11: 2743-2756.
35. Sollner, R., Glasser, G., Wanner, G., Somerville, C.R., Jurgens, G. and Assaad, F.F. (2002) Cytokinesis-defective mutants of Arabidopsis. Plant Physiol. 129: 678-690.
36. Sosa, R.T., Weber, M.M., Wen, Y. and O'Halloran, T.J. (2012) A single beta adaptin contributes to AP1 and AP2 complexes and clathrin function in Dictyostelium. Traffic 13: 305-316.
37. Stepp, J.D., Pellicena-Palle, A., Hamilton, S., Kirchhausen, T. and Lemmon, S.K. (1995) A late Golgi sorting function for Saccharomyces cerevisiae Apm1p, but not for Apm2p, a second yeast clathrin AP medium chain-related protein. Mol. Biol. Cell 6: 41-58.
38. Strompen, G., El Kasmi, F., Richter, S., Lukowitz, W., Assaad, F.F., Jurgens, G. et al. (2002) The Arabidopsis HINKEL gene encodes a kinesin-related protein involved in cytokinesis and is expressed in a cell cycle-dependent manner. Curr. Biol. 12: 153-158.
39. Tamura, K., Fukao, Y., Iwamoto, M., Haraguchi, T. and Hara-Nishimura, I. (2010) Identification and characterization of nuclear pore complex components in Arabidopsis thaliana. Plant Cell 22: 4084-4097.
40. Tebar, F., Sorkina, T., Sorkin, A., Ericsson, M. and Kirchhausen, T. (1996) Eps15 is a component of clathrin-coated pits and vesicles and is located at the rim of coated pits. J. Biol. Chem. 271: 28727-28730.
41. Ueda, T., Uemura, T., Sato, M.H. and Nakano, A. (2004) Functional differentiation of endosomes in Arabidopsis cells. Plant J. 40: 783-789.
42. Uemura, T., Kim, H., Saito, C., Ebine, K., Ueda, T., Schulze-Lefert, P. et al. (2012) Qa-SNAREs localized to the trans-Golgi network regulate multiple transport pathways and extracellular disease resistance in plants. Proc. Natl Acad. Sci. USA 109: 1784-1789.
43. Van Damme, D., Gadeyne, A., Vanstraelen, M., Inze, D., Van Montagu, M.C., De Jaeger, G. et al. (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.
44. Van Damme, D., Inze, D. and Russinova, E. (2008) Vesicle trafficking during somatic cytokinesis. Plant Physiol. 147: 1544-1552.
45. Waizenegger, I., Lukowitz, W., Assaad, F., Schwarz, H., Jurgens, G. and Mayer, U. (2000) The Arabidopsis KNOLLE and KEULE genes interact to promote vesicle fusion during cytokinesis. Curr. Biol. 10: 1371-1374.
46. Wolfenstetter, S., Wirsching, P., Dotzauer, D., Schneider, S. and Sauer, N. (2012) Routes to the tonoplast: the sorting of tonoplast transporters in Arabidopsis mesophyll protoplasts. Plant Cell 24: 215-232.
47. Zaremba, S. and Keen, J.H. (1983) Assembly polypeptides from coated vesicles mediate reassembly of unique clathrin coats. J. Cell Biol. 97: 1339-1347.
48. Zizioli, D., Meyer, C., Guhde, G., Saftig, P., von Figura, K. and Schu, P. (1999) Early embryonic death of mice deficient in gamma-adaptin. J. Biol. Chem. 274: 5385-5390.