Dynamics of Arabidopsis SUN proteins during mitosis and their involvement in nuclear shaping

Plant Journal

Volumn 66, Issue 4, 2011, Pages 629-641

  Oda, Yoshihisa ^a   Fukuda, Hiroo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

microtubule; mitosis; nuclear envelope; nuclear shape; phragmoplast; SUN domain

Indexed keywords

MICROTUBULES; MITOSIS; NUCLEAR ENVELOPE; NUCLEAR SHAPE; PHRAGMOPLAST;

BODY FLUIDS; DYNAMICS; GENES; MAINTENANCE; VISUALIZATION;

PROTEINS;

ARABIDOPSIS PROTEIN; HYBRID PROTEIN;

ARABIDOPSIS; ARTICLE; CELL CULTURE; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CONFOCAL MICROSCOPY; CYTOLOGY; CYTOPLASM; ENDOPLASMIC RETICULUM; GENE SILENCING; GENETICS; METABOLISM; MICROTUBULE; MITOSIS; PLANT ROOT; PROTEIN TRANSPORT; RHIZOBIUM RADIOBACTER;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL NUCLEUS; CELLS, CULTURED; CYTOPLASM; ENDOPLASMIC RETICULUM; GENE KNOCKDOWN TECHNIQUES; MICROSCOPY, CONFOCAL; MICROTUBULES; MITOSIS; NUCLEAR ENVELOPE; PLANT ROOTS; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; RHIZOBIUM RADIOBACTER;

ARABIDOPSIS; EUKARYOTA; METAZOA;

EID: 79954565013     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04523.x     Document Type: Article

References (62)

1. Anderson, D.J., and, Hetzer, M.W., (2007) Nuclear envelope formation by chromatin-mediated reorganization of the endoplasmic reticulum. Nat. Cell Biol. 9, 1160-1166. (Pubitemid 47500492)
2. Anderson, D.J., and, Hetzer, M.W., (2008) Reshaping of the endoplasmic reticulum limits the rate for nuclear envelope formation. J. Cell Biol. 182, 911-924.
3. Andrés, V., and, González, J.M., (2009) Role of A-type lamins in signaling, transcription, and chromatin organization. J. Cell Biol. 187, 945-957.
4. Austin, J.R. II, Seguí-Simarro, J.M., and, Staehelin, L.A., (2005) Quantitative analysis of changes in spatial distribution and plus-end geometry of microtubules involved in plant-cell cytokinesis. J. Cell Sci. 118, 3895-3903. (Pubitemid 41410273)
5. Barr, F.A., and, Gruneberg, U., (2007) Cytokinesis: placing and making the final cut. Cell, 131, 847-860. (Pubitemid 350138092)
6. Beaudouin, J., Gerlich, D., Daigle, N., Eils, R., and, Ellenberg, J., (2002) Nuclear envelope breakdown proceeds by microtubule-induced tearing of the lamina. Cell, 108, 83-96. (Pubitemid 34137014)
7. Bobinnec, Y., Marcaillou, C., Morin, X., and, Debec, A., (2003) Dynamics of the endoplasmic reticulum during early development of Drosophila melanogaster. Cell Motil. Cytoskeleton, 54, 217-225. (Pubitemid 36258704)
8. Crisp, M., Liu, Q., Roux, K., Rattner, J.B., Shanahan, C., Burke, B., Stahl, P.D., and, Hodzic, D., (2006) Coupling of the nucleus and cytoplasm: role of the LINC complex. J. Cell Biol. 172, 41-53. (Pubitemid 43042628)
9. Dhonukshe, P., Vischer, N., and, Gadella, T.W.J. Jr, (2006) Contribution of microtubule growth polarity and flux to spindle assembly and functioning in plant cells. J. Cell Sci. 119, 3193-3205. (Pubitemid 44322133)
10. Dittmer, T.A., Stacey, N.J., Sugimoto-Shirasu, K., and, Richards, E.J., (2007) LITTLE NUCLEI genes affecting nuclear morphology in Arabidopsis thaliana. Plant Cell, 19, 2793-2803. (Pubitemid 350046229)
11. Dultz, E., Zanin, E., Wurzenberger, C., Braun, M., Rabut, G., Sironi, L., and, Ellenberg, J., (2008) Systematic kinetic analysis of mitotic dis- and reassembly of the nuclear pore in living cells. J. Cell Biol. 180, 857-865. (Pubitemid 351398413)
12. Ellenberg, J., Siggia, E.D., Moreira, J.E., Smith, C.L., Presley, J.F., Worman, H.J., and, Lippincott-Schwartz, J., (1997) Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis. J. Cell Biol. 138, 1193-1206. (Pubitemid 27415047)
13. Georgatos, S.D., Pyrpasopoulou, A., and, Theodoropoulos, P.A., (1997) Nuclear envelope breakdown in mammalian cells involves stepwise lamina disassembly and microtubule-drive deformation of the nuclear membrane. J. Cell Sci. 110, 2129-2140. (Pubitemid 27440436)
14. Graumann, K., and, Evans, D.E., (2010) The plant nuclear envelope in focus. Biochem. Soc. Trans. 38, 307-311.
15. Graumann, K., Runions, J., and, Evans, D.E., (2009) Characterization of SUN-domain proteins at the higher plant nuclear envelope. Plant J. 61, 134-144.
16. Gruenbaum, Y., Margalit, A., Goldman, R.D., Shumaker, D.K., and, Wilson, K.L., (2005) The nuclear lamina comes of age. Nat. Rev. Mol. Cell Biol. 6, 21-31. (Pubitemid 40064896)
17. Gupton, S.L., Collings, D.A., and, Allen, N.S., (2006) Endoplasmic reticulum targeted GFP reveals ER organization in tobacco NT-1 cells during cell division. Plant Physiol. Biochem. 44, 95-105. (Pubitemid 43816302)
18. Güttinger, S., Laurell, E., and, Kutay, U., (2009) Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat. Rev. Mol. Cell Biol. 10, 178-191.
19. Hallberg, E., Wozniak, R.W., and, Blobel, G., (1993) An integral membrane protein of the pore membrane domain of the nuclear envelope contains a nucleoporin-like region. J. Cell Biol. 122, 513-521. (Pubitemid 23226669)
20. Haraguchi, T., Kojidani, T., Koujin, T., Shimi, T., Osakada, H., Mori, C., Yamamoto, A., and, Hiraoka, Y., (2008) Live cell imaging and electron microscopy reveal dynamic processes of BAF-directed nuclear envelope assembly. J. Cell Sci. 121, 2540-2554.
21. Harel, A., Orjalo, A.V., Vincent, T., Lachish-Zalait, A., Vasu, S., Shah, S., Zimmerman, E., Elbaum, M., and, Forbes, D.J., (2003) Removal of a single pore subcomplex results in vertebrate nuclei devoid of nuclear pores. Mol. Cell, 11, 853-864. (Pubitemid 36566309)
22. Hetzer, M.W., and, Wente, S.R., (2009) Border control at the nucleus: biogenesis and organization of the nuclear membrane and pore complexes. Dev. Cell, 17, 606-616.
23. Irons, S.L., Evans, D.E., and, Brandizzi, F., (2003) The first 238 amino acids of the human lamin B receptor are targeted to the nuclear envelope in plants. J. Exp. Bot. 54, 943-950. (Pubitemid 36317408)
24. Jeong, S.Y., Rose, A., Joseph, J., Dasso, M., and, Meier, I., (2005) Plant-specific mitotic targeting of RanGAP requires a functional WPP domain. Plant J. 42, 270-282. (Pubitemid 40589388)
25. Katsani, K.R., Karess, R.E., Dostatni, N., and, Doye, V., (2008) In vivo dynamics of Drosophila nuclear envelope components. Mol. Biol. Cell, 19, 3652-3666.
26. Kimura, Y., Kuroda, C., and, Masuda, K., (2009) Differential nuclear envelope assembly at the end of mitosis in suspension-cultured Apium graveolens cells. Chromosoma, 119, 195-204.
27. Kiseleva, E., Rutherford, S., Cotter, L.M., Allen, T.D., and, Goldberg, M.W., (2001) Steps of nuclear pore complex disassembly and reassembly during mitosis in early Drosophila embryos. J. Cell Sci. 114, 3607-3618. (Pubitemid 33041043)
28. Lee, K.K., Gruenbaum, Y., Spann, P., Liu, J., and, Wilson, K.L., (2000) C. elegans nuclear envelope proteins emerin, MAN1, lamin, and nucleoporins reveal unique timing of nuclear envelope breakdown during mitosis. Mol. Biol. Cell, 11, 3089-3099. (Pubitemid 32107085)
29. Lénárt, P., Rabut, G., Daigle, N., Hand, A.R., Terasaki, M., and, Ellenberg, J., (2003) Nuclear envelope breakdown in starfish oocytes proceeds by partial NPC disassembly followed by a rapidly spreading fenestration of nuclear membranes. J. Cell Biol. 160, 1055-1068. (Pubitemid 36443874)
30. Liu, Q., Pante, N., Misteli, T., Elsagga, M., Crisp, M., Hodzic, D., Burke, B., and, Roux, K.J., (2007) Functional association of Sun1 with nuclear pore complexes. J. Cell Biol. 178, 785-798. (Pubitemid 47347364)
31. Macaulay, C., and, Forbes, D.J., (1996) Assembly of the nuclear pore: biochemically distinct steps revealed with NEM, GTP gamma S and BAPTA. J. Cell Biol. 132, 5-20. (Pubitemid 26035071)
32. Mansfeld, J., Güttinger, S., Hawryluk-Gara, L.A., et al. (2006) The conserved transmembrane nucleoporin NDC1 is required for nuclear pore complex assembly in vertebrate cells. Mol. Cell, 22, 93-103.
33. Masuda, K., Haruyama, S., and, Fujino, K., (1999) Assembly and disassembly of the peripheral architecture of the plant cell nucleus during mitosis. Planta, 210, 165-167. (Pubitemid 30000928)
34. Meier, I., and, Brkljacic, J., (2009) The nuclear pore and plant development. Curr. Opin. Plant Biol. 12, 87-95.
35. Mora-Bermudez, F., Gerlich, D., and, Ellenberg, J., (2007) Maximal chromosome compaction occurs by axial shortening in anaphase and depends on Aurora kinase. Nat. Cell Biol. 9, 822-831. (Pubitemid 47019469)
36. Mühlhäusser, P., and, Kutay, U., (2007) An in vitro nuclear disassembly system reveals a role for the RanGTPase system and microtubule-dependent steps in nuclear envelope breakdown. J. Cell Biol. 178, 595-610. (Pubitemid 47267272)
37. Nakagawa, T., Suzuki, T., Murata, S., et al. (2007) Improved Gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci. Biotechnol. Biochem. 71, 2095-2100. (Pubitemid 350113146)
38. Oda, Y., Iida, Y., Kondo, Y., and, Fukuda, H., (2010) Wood cell-wall structure requires local 2D-microtubule disassembly by a novel plasma membrane-anchored protein. Curr. Biol. 20, 1197-1202.
39. Padmakumar, V.C., Libotte, T., Lu, W., Zaim, H., Abraham, S., Noegel, A.A., Gotzmann, J., Foisner, R., and, Karakesisoglou, I., (2005) The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope. J. Cell Sci. 118, 3419-3430. (Pubitemid 41246097)
40. Patel, S., Rose, A., Meulia, T., Dixit, R., Cyr, R.J., and, Meier, I., (2004) Arabidopsis WPP-domain proteins are developmentally associated with the nuclear envelope and promote cell division. Plant Cell, 16, 3260-3273. (Pubitemid 41096005)
41. Pay, A., Resch, K., Frohnmeyer, H., Fejes, E., Nagy, F., and, Nick, P., (2002) Plant RanGAPs are localized at the nuclear envelope in interphase and associated with microtubules in mitotic cells. Plant J. 30, 699-709. (Pubitemid 34696062)
42. Puhka, M., Vihinen, H., Joensuu, M., and, Jokitalo, E., (2007) Endoplasmic reticulum remains continuous and undergoes sheet-to-tubule transformation during cell division in mammalian cells. J. Cell Biol. 179, 895-909. (Pubitemid 350223487)
43. Razafsky, D., and, Hodzic, D., (2009) Bringing KASH under the SUN: the many faces of nucleo-cytoskeletal connections. J. Cell Biol. 186, 461-472.
44. Salina, D., Bodoor, K., Eckley, D.M., Schroer, T.A., Rattner, J.B., and, Burke, B., (2002) Cytoplasmic dynein as a facilitator of nuclear envelope breakdown. Cell, 108, 97-107. (Pubitemid 34137015)
45. Schneider, M., Noegel, A.A., and, Karakesisoglou, I., (2008) KASH-domain proteins and the cytoskeletal landscapes of the nuclear envelope. Biochem. Soc. Trans. 36, 1368-1372.
46. Starr, D.A., (2009) A nuclear-envelope bridge positions nuclei and moves chromosomes. J. Cell Sci. 122, 577-586.
47. Stavru, F., Hülsmann, B.B., Spang, A., Hartmann, E., Cordes, V.C., and, Görlich, D., (2006) NDC1: a crucial membrane-integral nucleoporin of metazoan nuclear pore complexes. J. Cell Biol. 173, 509-519. (Pubitemid 43765198)
48. Stick, R., Angres, B., Lehner, C.F., and, Nigg, E.A., (1988) The fates of chicken nuclear lamin proteins during mitosis: evidence for a reversible redistribution of lamin B2 between inner nuclear membrane and elements of the endoplasmic reticulum. J. Cell Biol. 107, 397-406.
49. Terasaki, M., Campagnola, P., Rolls, M.M., Stein, P.A., Ellenberg, J., Hinkle, B., and, Slepchenko, B., (2001) A new model for nuclear envelope breakdown. Mol. Biol. Cell, 12, 503-510. (Pubitemid 33051591)
50. Ulbert, S., Platani, M., Boue, S., and, Mattaj, I.W., (2006) Direct membrane protein-DNA interactions required early in nuclear envelope assembly. J. Cell Biol. 173, 469-476. (Pubitemid 43765194)
51. Vagnarelli, P., Hudson, D.F., Ribeiro, S.A., Trinkle-Mulcahy, L., Spence, J.M., Lai, F., Farr, C.J., Lamond, A.I., and, Earnshaw, W.C., (2006) Condensin and Repo-Man-PP1 co-operate in the regulation of chromosome architecture during mitosis. Nat. Cell Biol. 8, 1133-1142. (Pubitemid 44473609)
52. Van Bruaene, N., Joss, G., Thas, O., and, Van Oostveldt, P., (2003) Four-dimensional imaging and computer-assisted track analysis of nuclear migration in root hairs of Arabidopsis thaliana. J. Microsc. 211, 167-178. (Pubitemid 36960550)
53. Van Damme, D., Bouget, F.-Y., Van Poucke, K., Inzé, D., and, Geelen, D., (2004) Molecular dissection of plant cytokinesis and phragmoplast structure: a survey of GFP-tagged proteins. Plant J. 40, 386-398. (Pubitemid 39415620)
54. Vos, J.W., Pieuchot, L., Evrard, J.-L., Janski, N., Bergdoll, M., de Ronde, D., Perez, L.H., Sardon, T., Vernos, I., and, Schmit, A.-C., (2008) The plant TPX2 protein regulates prospindle assembly before nuclear envelope breakdown. Plant Cell, 20, 2783-2797. (Pubitemid 352844590)
55. Wagner, N., and, Krohne, G., (2007) LEM-Domain proteins: new insights into lamin-interacting proteins. Int. Rev. Cytol. 261, 1-46. (Pubitemid 46856616)
56. Walther, T.C., Alves, A., Pickersgill, H., et al. (2003) The conserved Nup107-160 complex is critical for nuclear pore complex assembly. Cell, 113, 195-206. (Pubitemid 36514971)
57. Wilhelmsen, K., Ketema, M., Truong, H., and, Sonnenberg, A., (2006) KASH-domain proteins in nuclear migration, anchorage and other processes. J. Cell Sci. 119, 5021-5029. (Pubitemid 46085182)
58. Xu, X.M., and, Meier, I., (2008) The nuclear pore comes to the fore. Trends Plant Sci. 13, 20-27.
59. Xu, X.M., Meulia, T., and, Meier, I., (2007) Anchorage of plant RanGAP to the nuclear envelope involves novel nuclear-pore-associated proteins. Curr. Biol. 17, 1157-1163. (Pubitemid 46990889)
60. Xu, X.M., Zhao, Q., Rodrigo-Peiris, T., Brkljacic, J., He, C.S., Müller, S., and, Meier, I., (2008) RanGAP1 is a continuous marker of the Arabidopsis cell division plane. Proc. Natl Acad. Sci. USA, 105, 18637-18642.
61. Yang, L., Guan, T., and, Gerace, L., (1997) Integral membrane proteins of the nuclear envelope are dispersed throughout the endoplasmic reticulum during mitosis. J. Cell Biol. 137, 1199-1210. (Pubitemid 27265936)
62. Zhao, Q., Brkljacic, J., and, Meier, I., (2008) Two distinct interacting classes of nuclear envelope-associated coiled-coil proteins are required for the tissue-specific nuclear envelope targeting of Arabidopsis RanGAP. Plant Cell, 20, 1639-1651. (Pubitemid 352844168)