Two microtubule-associated proteins of Arabidopsis MAP65s promote antiparallel microtubule bundling

Molecular Biology of the Cell

Volumn 19, Issue 10, 2008, Pages 4534-4544

  Gaillard, Jérémie ^a   Neumann, Emmanuelle ^b   Van Damme, Daniel ^c,d   Stoppin Mellet, Virginie ^a   Ebel, Christine ^b   Barbier, Elodie ^a   Geelen, Danny ^d   Vantard, Marylin ^a  

^a UNIV GRENOBLE ALPES   (France)

^b INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO TERMINAL SEQUENCE; ARABIDOPSIS; ARTICLE; IN VITRO STUDY; IN VIVO STUDY; MICROTUBULE; MITOSIS; NONHUMAN; PHRAGMOPLAST; PRIORITY JOURNAL; PROTEIN BINDING; SPINDLE CELL;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYTOSKELETON; DIMERIZATION; GENE EXPRESSION REGULATION, PLANT; GREEN FLUORESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY;

ARABIDOPSIS; MAMMALIA;

EID: 56349118579     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-04-0341     Document Type: Article

References (45)

1. Ambrose, J., Li, W., Marcus, A., Ma, H., and Cyr, R. (2005). A minus-end-directed kinesin with plus-end tracking protein activity is involved in spindle morphogenesis. Mol. Biol. Cell 16, 1584-1592.
2. Ambrose, J., and Cyr, R. (2007). The kinesin ATK5 functions in early spindle assembly in Arabidopsis. Plant Cell 19, 226-236.
3. Caillaud, M. C. et al. (2008). MAP65-3 microtubule-associated protein is essential for nematode-induced giant cell ontogenesis in Arabidopsis. Plant Cell. Advanced online publication 8 February 2008; doi: 10.1105/tpc.107.057422.
4. Chan, J., Jensen, C. G., Jensen, L. C., Bush, M., and Lloyd, C. W. (1999). The 65-kDa carrot microtubule-associated protein forms regularly arranged filamentous cross-bridges between microtubules. Proc. Natl. Acad. Sci. USA 96, 14931-14936.
5. Chan, J., Calder, G. M., Doonan, J. H., and Lloyd, C. W. (2003). EB1 reveals mobile microtubule nucleation sites in Arabidopsis. Nat. Cell Biol. 5, 967-971.
6. Chan, J., Calder, G., Fox, S., and Lloyd, C. W. (2007). Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells. Nat. Cell Biol. 9, 171-175.
7. Chrétien, D., Kenney, J., Fuller, S., and Wade, R. (1996). Determination of microtubule polarity by cryo-electron microscopy. Structure 4, 1031-1040.
8. Dixit, R., and Cyr, R. (2004). Encounters between dynamic cortical microtubules promote ordering of the cortical array through angle-dependent modifications of microtubule behaviour. Plant Cell 16, 3274-3284.
9. Dixit, R., Chang, E., and Cyr, R. (2006). Establishment of polarity during organization of the acentrosomal plant cortical microtubule array. Mol. Biol. Cell 17, 1298-1305.
10. Dubochet, J., Adrian, M., Chand, J. J., Homo, J. C., Lepault, J., McDowall, A. W., and Schultz, P. (1988). Cryo-electron microscopy of vitrified specimens. Rev. Biophys. 21, 129-228.
11. Ebel, C. (2007). Analytical ultracentrifugation. State of the art and perspectives. In: Methods in Protein Structure and Stability Analysis: Conformational Stability, Size, Shape and Surface of Protein Molecules, ed. V. Uversky and E. A. Permyakov, New York: Nova Science Publishers.
12. Ehrhardt, D. W., and Shaw, S. L. (2006). Microtubule dynamics and organization in the plant cortex. Annu. Rev. Plant Biol. 57, 859-875.
13. Geelen, D. N., and Inzé, D. G. (2001). A bright future for the bright yellow-2 cell culture. Plant Physiol. 127, 1375-1379.
14. Gunasekaran, K., Tsai, C., Kumar, S., Zanuy, D., and Nussinov, R. (2003). Extended disordered proteins: targeting function with less scaffold. Trends Biochem. Sci. 28, 81-85.
15. Hardham, A. R., and Gunning, B. (1978). Structure of cortical microtubules in plant cells. J. Cell Biol. 77, 14-34.
16. Hussey, P., Hawkins, T. J., Igarashi, H., Kaloriti, D., and Smertenko, A. (2002). The plant cytoskeleton: recent advances in the study of the plant microtubuleassociated proteins MAP-65, MAP-190 and the Xenopus MAP215-like protein, MOR1. Plant Mol. Biol. 50, 915-924.
17. Hyman, A., Dreschel, D., Kellog, D., Salser, S., Sawin, K., Steffen, P., Wordeman, L., and Mitchison, T. (1991). Preparation of modified tubulins. Methods Enzymol. 196, 478-485.
18. Janson, M., Loughlin, R., Loïodice, I., Brunner, C., Nédelec, F., and Tran, P. T. (2007). Crosslinkers and motors organize dynamic microtubules to form stable bipolar arrays in fission yeast. Cell 128, 357-368.
19. Li, H., Mao, T., Zhang, Z., and Yuan, M. (2007a). The AtMAP65-1 cross-bridge between microtubules is formed by one dimer. Plant Cell Physiol. 48, 866-874.
20. Li, H., Yuan, M., and Mao, T. (2007b). AtMAP65-1 binds to tubulin dimers to promote tubulin assembly. J. Biochem. Mol. Biol. 40, 218-225.
21. Linding, R., Jensen, L. J., Diella, F., Bork, P., Gibson, T. J., and Russell, R. B. (2003). Protein disorder prediction: implications for structural proteomics. Structure 11, 1453-1459.
22. Lloyd, C. W. (1994). Why should stationary plants cells have such dynamic microtubules? Mol. Biol. Cell 5, 1277-1280.
23. Loïdice, I., Staub, J., Getty, T. G., Hguyen, N. T., Paoletti, A., and Tran, P. T. (2005). Ase1p organizes antiparallel microtubule arrays during interphase and mitosis in fission yeast. Mol. Biol. Cell 16, 1756-1768.
24. Mao, G., Chan, J., Calder, G., Doonan, J. H., and Lloyd, C. W. (2005a). Modulated targeting of GFP-AtMAP65-1 to central spindle microtubules during division. Plant Cell 43, 469-478.
25. Mao, T., Jin, L., Liu, B., and Yuan, M. (2005b). Two microtubule- associated proteins of the Arabidopsis MAP65 family function differently on microtubules. Plant Physiol. 138, 654-662.
26. Mollinari, C., Kleman, J. P., Jiang, W., Schoehn, G., Hunter, T., and Margolis, B. (2002). PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J. Cell Biol. 157, 1175-1186.
27. Murata, M., Sonobe, S., Baskin, T. I., Hyodo, S., Hasezawa, S., Nagata, T., Horio, T., and Hasebe, M. (2005). Microtubule-dependent microtubule nucleation based on recruitment of gamma-tubulin in higher plants. Nat. Cell Biol. 7, 961-968.
28. Pastuglia, M., Azimzadeh, J., Goussot, M., Camilleri, C., Evrard, J. L., Schmit, A. C., Guerche, P., and Bouchez, D. (2006). Gamma-tubulin is essential for microtubule organization and development in Arabidopsis. Plant Cell 18, 1412-1425.
29. Receveur-Bréchot, V., Bourhis, J. M., Uversky, V., Canard, B., and Longhi, S. (2006). Assessing protein disorder and induced folding. Proteins 62, 24-45.
30. Schuck, P. (2000). Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619.
31. Schuyler, S., Liu, J. Y., and Pellman, D. (2003). The molecular function of Ase1p: evidence for a MAP-dependent midzone-specific spindle matrix. J. Cell Biol. 160, 517-528.
32. Shaw, S. L., Kamyar, R., and Ehrhardt, D. W. (2003). Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300, 1715-1718.
33. Smertenko, A., Chang, H., Wagner, V., Kaloriti, D., Fenyk, S., Sonobe, S., Lloyd, C. W., Hauser, M., and Hussey, P. (2004). The Arabidopsis microtubule-associated protein AtMAP65-1, molecular analysis of its microtubule bundling activity. Plant Cell 16, 2035-2047.
34. Smertenko, A. P., Chang, H. Y., Sonobe, S., Fenyk, S. I., Weingartner, M., Bogre, L., and Hussey, P. (2006). Control of the AtMAP65-1 interaction with microtubules through the cell cycle. J. Cell Sci. 119, 3227-3237.
35. Stoppin, V., Lambert, A. M., and Vantard, M. (1996). Plant microtubule-associated proteins (MAPs) affect microtubule nucleation and growth at plant nuclei and mammalian centrosomes. Eur. J. Cell Biol. 69, 11-23.
36. Tian, G. W., Smith, D., Gluck, S., and Baskin, T. I. (2004). Higher plant cortical microtubule array analyzed in vitro in the presence of the cell wall. Cell Motil. Cytoskelet. 57, 26-36.
37. Uversky, V. N. (2002). What does it mean to be natively unfolded? Eur. J. Biochem. 269, 2-12.
38. Van Damme, D., Van Poucke, K., Boutant, E., Ritzenthaler, C., Inzé, D., and Geelen, D. (2004a). In vivo dynamics and differential microtubule-binding activities of MAP65 proteins. Plant Physiol. 136, 3956-3967.
39. Van Damme, D., Bouget, F. Y., Van Poucke, K., Inzé, D., Geelen, D. (2004b). Molecular dissection of plant cytokinesis and phragmoplast structure: a survey of GFP-tagged proteins. Plant J. 40, 386-398.
40. Vantard, M., Peter, C., Fellous, A., Schellenbaum, P., and Lambert, A. M. (1994). Characterization of a 100-kDa heat-stable microtubule-associated protein from higher plants. Eur. J. Biochem. 220, 847-853.
41. Verni, F., Somma, M. P., Gunsalus, C. K., Bonaccorsi, S., Belloni, G., Goldberg, M. L., and Gatti, M. (2004). Feo, the Drosophila homolog of PRC1, is required for central-spindle formation and cytokinesis. Curr. Biol. 14, 1569-1575.
42. Vos, J. W., Dogterom, M., and Emons, A. M. (2004). Microtubules become more dynamic but not shorter during preprophase band formation: a possible "search-and-capture" mechanism for microtubule translocation. Cell Motil. Cytoskelet. 57, 246-258.
43. Wasteneys, G. O., and Fujita, M. (2006). Establishing and maintaining axial growth: wall mechanical properties and the cytoskeleton. J. Plant Res. 119, 5-10.
44. Wicker-Planquart, C., Stoppin-Mellet, V., Blanchoin, L., and Vantard, M. (2004). Interactions of tobacco microtubule-associated protein MAP651b with microtubules. Plant J. 39, 126-134.
45. Zhu, C., Lau, E., Schwarzenbacher, R., Bossy-Wetzel, E., and Jiang, W. (2006). Spatiotemporal control of spindle midzone formation by PRC1 in human cells. Proc. Natl. Acad. Sci. USA 18, 6196-6201.