Purification and characterization of novel microtubule-associated proteins from arabidopsis cell suspension cultures

Plant Physiology

Volumn 163, Issue 4, 2013, Pages 1804-1816

  Hamada, Takahiro ^a   Nagasaki Takeuchi, Nahoko ^a   Kato, Takehide ^a   Fujiwara, Masayuki ^a   Sonobe, Seiji ^b   Fukao, Yoichiro ^a   Hashimoto, Takashi ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b UNIVERSITY OF HYOGO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; KINESIN; MICROTUBULE ASSOCIATED PROTEIN; TUBULIN;

ARABIDOPSIS; ARTICLE; CELL CULTURE; CELL FRACTIONATION; CELL PROLIFERATION; CYTOLOGY; ISOLATION AND PURIFICATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; PROTEIN TRANSPORT; SUSPENSION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; CHROMATOGRAPHY, LIQUID; GREEN FLUORESCENT PROTEINS; KINESIN; MASS SPECTROMETRY; MICROTUBULE-ASSOCIATED PROTEINS; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SUBCELLULAR FRACTIONS; SUSPENSIONS; TUBULIN;

EID: 84888882481     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.225607     Document Type: Article

References (61)

1. Abe T, Hashimoto T (2005) Altered microtubule dynamics by expression of modified alpha-tubulin protein causes right-handed helical growth in transgenic Arabidopsis plants. Plant J 43: 191-204
2. Abel S, Savchenko T, Levy M (2005) Genome-wide comparative analysis of the IQD gene families in Arabidopsis thaliana and Oryza sativa. BMC Evol Biol 5: 72
3. Ambrose JC, Shoji T, Kotzer AM, Pighin JA, Wasteneys GO (2007) The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division. Plant Cell 19: 2763-2775
4. Bharti P, Schliebs W, Schievelbusch T, Neuhaus A, David C, Kock K, Herrmann C, Meyer HE, Wiese S, Warscheid B, et al (2011) PEX14 is required for microtubule-based peroxisome motility in human cells. J Cell Sci 124: 1759-1768
5. Bokros CL, Hugdahl JD, Kim HH, Hanesworth VR, van Heerden A, Browning KS, Morejohn LC (1995) Function of the p86 subunit of eukaryotic initiation factor (iso)4F as a microtubule-associated protein in plant cells. Proc Natl Acad Sci USA 92: 7120-7124
6. Buschmann H, Chan J, Sanchez-Pulido L, Andrade-Navarro MA, Doonan JH, Lloyd CW (2006) Microtubule-associated AIR9 recognizes the cortical division site at preprophase and cell-plate insertion. Curr Biol 16: 1938-1943
7. Chang-Jie J, Sonobe S (1993) Identification and preliminary characterization of a 65 kDa higher-plant microtubule-associated protein. J Cell Sci 105: 891-901
8. Chuong SD, Good AG, Taylor GJ, Freeman MC, Moorhead GB, Muench DG (2004) Large-scale identification of tubulin-binding proteins provides insight on subcellular trafficking, metabolic channeling, and signaling in plant cells. Mol Cell Proteomics 3: 970-983
9. Chuong SD, Park NI, Freeman MC, Mullen RT, Muench DG (2005) The peroxisomal multifunctional protein interacts with cortical microtubules in plant cells. BMC Cell Biol 6: 40
10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
11. Desai A, Mitchison TJ (1997) Microtubule polymerization dynamics. Annu Rev Cell Dev Biol 13: 83-117
12. Fujiwara M, Hamada S, Hiratsuka M, Fukao Y, Kawasaki T, Shimamoto K (2009) Proteome analysis of detergent-resistant membranes (DRMs) associated with OsRac1-mediated innate immunity in rice. Plant Cell Physiol 50: 1191-1200
13. Furutani I, Watanabe Y, Prieto R, Masukawa M, Suzuki K, Naoi K, Thitamadee S, Shikanai T, Hashimoto T (2000) The SPIRAL genes are required for directional control of cell elongation in Arabidopsis thaliana. Development 127: 4443-4453
14. Gache V, Waridel P, Winter C, Juhem A, Schroeder M, Shevchenko A, Popov AV (2010) Xenopus meiotic microtubule-associated interactome. PLoS ONE 5: e9248
15. Gardiner J, Marc J (2003) Putative microtubule-associated proteins from the Arabidopsis genome. Protoplasma 222: 61-74
16. Hamada T (2007) Microtubule-associated proteins in higher plants. J Plant Res 120: 79-98
17. Hamada T, Igarashi H, Itoh TJ, Shimmen T, Sonobe S (2004) Characterization of a 200 kDa microtubule-associated protein of tobacco BY-2 cells, a member of the XMAP215/MOR1 family. Plant Cell Physiol 45: 1233-1242
18. 2, is a microtubule-associated protein in tobacco. Plant Cell Physiol 50: 801-811
19. Hamada T, Igarashi H, YaoM, Hashimoto T, Shimmen T, Sonobe S (2006) Purification and characterization of plant dynamin from tobacco BY-2 cells. Plant Cell Physiol 47: 1175-1181
20. Hamada T, Tominaga M, Fukaya T, Nakamura M, Nakano A, Watanabe Y, Hashimoto T, Baskin TI (2012) RNA processing bodies, peroxisomes, Golgi bodies, mitochondria, and endoplasmic reticulum tubule junctions frequently pause at cortical microtubules. Plant Cell Physiol 53: 699-708
21. Hong Z, Bednarek SY, Blumwald E, Hwang I, Jurgens G, Menzel D, Osteryoung KW, Raikhel NV, Shinozaki K, Tsutsumi N, et al (2003a) A unified nomenclature for Arabidopsis dynamin-related large GTPases based on homology and possible functions. Plant Mol Biol 53: 261-265
22. Hong Z, Geisler-Lee CJ, Zhang Z, Verma DP (2003b) Phragmoplastin dynamics: multiple forms, microtubule association and their roles in cell plate formation in plants. Plant Mol Biol 53: 297-312
23. Hussey PJ, Hawkins TJ, Igarashi H, Kaloriti D, Smertenko A (2002) The plant cytoskeleton: recent advances in the study of the plant microtubule-associated proteins MAP-65, MAP-190 and the Xenopus MAP215-like protein, MOR1. Plant Mol Biol 50: 915-924
24. Igarashi H, Orii H, Mori H, Shimmen T, Sonobe S (2000) Isolation of a novel 190 kDa protein from tobacco BY-2 cells: possible involvement in the interaction between actin filaments and microtubules. Plant Cell Physiol 41: 920-931
25. Ishida T, Kaneko Y, Iwano M, Hashimoto T (2007a) Helical microtubule arrays in a collection of twisting tubulin mutants of Arabidopsis thaliana. Proc Natl Acad Sci USA 104: 8544-8549
26. Ishida T, Thitamadee S, Hashimoto T (2007b) Twisted growth and organization of cortical microtubules. J Plant Res 120: 61-70
27. Ketelaar T, Voss C, Dimmock SA, Thumm M, Hussey PJ (2004) Arabidopsis homologues of the autophagy protein Atg8 are a novel family of microtubule binding proteins. FEBS Lett 567: 302-306
28. Komaki S, Abe T, Coutuer S, Inzé D, Russinova E, Hashimoto T (2010) Nuclear-localized subtype of end-binding 1 protein regulates spindle organization in Arabidopsis. J Cell Sci 123: 451-459
29. Konopka CA, Schleede JB, Skop AR, Bednarek SY (2006) Dynamin and cytokinesis. Traffic 7: 239-247
30. Korolev AV, Chan J, Naldrett MJ, Doonan JH, Lloyd CW (2005) Identification of a novel family of 70 kDa microtubule-associated proteins in Arabidopsis cells. Plant J 42: 547-555
31. Korolev AV, Buschmann H, Doonan JH, Lloyd CW (2007) AtMAP70-5, a divergent member of the MAP70 family of microtubule-associated proteins, is required for anisotropic cell growth in Arabidopsis. J Cell Sci 120: 2241-2247
32. Krupnova T, Sasabe M, Ghebreghiorghis L, Gruber CW, Hamada T, Dehmel V, Strompen G, Stierhof YD, Lukowitz W, Kemmerling B, et al (2009) Microtubule-associated kinase-like protein RUNKEL needed [corrected] for cell plate expansion in Arabidopsis cytokinesis. Curr Biol 19: 518-523
33. Liska AJ, Popov AV, Sunyaev S, Coughlin P, Habermann B, Shevchenko A, Bork P, Karsenti E, Shevchenko A (2004) Homology-based functional proteomics by mass spectrometry: application to the Xenopus microtubule-associated proteome. Proteomics 4: 2707-2721
34. Lloyd C, Hussey P (2001) Microtubule-associated proteins in plants: why we need a MAP. Nat Rev Mol Cell Biol 2: 40-47
35. Maiato H, Sampaio P, Sunkel CE (2004) Microtubule-associated proteins and their essential roles during mitosis. Int Rev Cytol 241: 53-153
36. Mandelkow E, Mandelkow EM (1995) Microtubules and microtubuleassociated proteins. Curr Opin Cell Biol 7: 72-81
37. Martin KC, Ephrussi A (2009) mRNA localization: gene expression in the spatial dimension. Cell 136: 719-730
38. Menges M, Murray JA (2002) Synchronous Arabidopsis suspension cultures for analysis of cell-cycle gene activity. Plant J 30: 203-212
39. Moore RC, Cyr RJ (2000) Association between elongation factor-1alpha and microtubules in vivo is domain dependent and conditional. Cell Motil Cytoskeleton 45: 279-292
40. Motose H, Hamada T, Yoshimoto K, Murata T, Hasebe M, Watanabe Y, Hashimoto T, Sakai T, Takahashi T (2011) NIMA-related kinases 6, 4, and 5 interact with each other to regulate microtubule organization during epidermal cell expansion in Arabidopsis thaliana. Plant J 67: 993-1005
41. Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y, Toyooka K, Matsuoka K, Jinbo T, Kimura T (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 104: 34-41
42. Nakajima K, Kawamura T, Hashimoto T (2006) Role of the SPIRAL1 gene family in anisotropic growth of Arabidopsis thaliana. Plant Cell Physiol 47: 513-522
43. Nakamura M, Ehrhardt DW, Hashimoto T (2010) Microtubule and katanin-dependent dynamics of microtubule nucleation complexes in the acentrosomal Arabidopsis cortical array. Nat Cell Biol 12: 1064-1070
44. Nakamura M, Naoi K, Shoji T, Hashimoto T (2004) Low concentrations of propyzamide and oryzalin alter microtubule dynamics in Arabidopsis epidermal cells. Plant Cell Physiol 45: 1330-1334
45. Nakamura M, Yagi N, Kato T, Fujita S, Kawashima N, Ehrhardt DW, Hashimoto T (2012) Arabidopsis GCP3-interacting protein 1/MOZART 1 is an integral component of the γ-tubulin-containing microtubule nucleating complex. Plant J 71: 216-225
46. Obar RA, Collins CA, Hammarback JA, Shpetner HS, Vallee RB (1990) Molecular cloning of the microtubule-associated mechanochemical enzyme dynamin reveals homology with a new family of GTP-binding proteins. Nature 347: 256-261
47. Oda Y, Iida Y, Kondo Y, Fukuda H (2010) Wood cell-wall structure requires local 2D-microtubule disassembly by a novel plasma membraneanchored protein. Curr Biol 20: 1197-1202
48. Oh SA, Allen T, Kim GJ, Sidorova A, Borg M, Park SK, Twell D (2012) Arabidopsis Fused kinase and the Kinesin-12 subfamily constitute a signalling module required for phragmoplast expansion. Plant J 72: 308-319
49. Patel PC, Fisher KH, Yang EC, Deane CM, Harrison RE (2009) Proteomic analysis of microtubule-associated proteins during macrophage activation. Mol Cell Proteomics 8: 2500-2514
50. Perrin RM, Wang Y, Yuen CY, Will J, Masson PH (2007) WVD2 is a novel microtubule-associated protein in Arabidopsis thaliana. Plant J 49: 961-971
51. Ruggenthaler P, Fichtenbauer D, Krasensky J, Jonak C, Waigmann E (2009) Microtubule-associated protein AtMPB2C plays a role in organization of cortical microtubules, stomata patterning, and tobamovirus infectivity. Plant Physiol 149: 1354-1365
52. Sedbrook JC, Kaloriti D (2008) Microtubules, MAPs and plant directional cell expansion. Trends Plant Sci 13: 303-310
53. Sharp DJ, Ross JL (2012) Microtubule-severing enzymes at the cutting edge. J Cell Sci 125: 2561-2569
54. Sharp JA, Plant JJ, Ohsumi TK, Borowsky M, Blower MD (2011) Functional analysis of the microtubule-interacting transcriptome. Mol Biol Cell 22: 4312-4323
55. Shinoda K, Tomita M, Ishihama Y (2010) emPAI Calc: for the estimation of protein abundance from large-scale identification data by liquid chromatography-tandem mass spectrometry. Bioinformatics 26: 576-577
56. Shpetner HS, Vallee RB (1989) Identification of dynamin, a novel mechanochemical enzyme that mediates interactions between microtubules. Cell 59: 421-432
57. Toya M, Sato M, Haselmann U, Asakawa K, Brunner D, Antony C, Toda T (2007) Gamma-tubulin complex-mediated anchoring of spindle microtubules to spindle-pole bodies requires Msd1 in fission yeast. Nat Cell Biol 9: 646-653
58. Vineyard L, Elliott A, Dhingra S, Lucas JR, Shaw SL (2013) Progressive transverse microtubule array organization in hormone-induced Arabidopsis hypocotyl cells. Plant Cell 25: 662-676
59. Whittington AT, Vugrek O, Wei KJ, Hasenbein NG, Sugimoto K, Rashbrooke MC, Wasteneys GO (2001) MOR1 is essential for organizing cortical microtubules in plants. Nature 411: 610-613
60. Yao M, Wakamatsu Y, Itoh TJ, Shoji T, Hashimoto T (2008) Arabidopsis SPIRAL2 promotes uninterrupted microtubule growth by suppressing the pause state of microtubule dynamics. J Cell Sci 121: 2372-2381
61. Zhu C, Dixit R (2012) Functions of the Arabidopsis kinesin superfamily of microtubule-based motor proteins. Protoplasma 249: 887-899