Isolation of a 90-kD microtubule-associated protein from tobacco membranes

Plant Cell

Volumn 8, Issue 11, 1996, Pages 2127-2138

  Marc, Jan ^a   Sharkey, Deirdre E ^a   Durso, Neil A ^b   Zhang, Min ^b   Cyr, Richard J ^b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTIANA TABACUM;

EID: 0030452396     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.8.11.2127     Document Type: Article

References (83)

1. Aizawa, H., Kawasaki, H., Murofushi, H., Kotani, S., Suzuki, K., and Sakai, H. (1988). Microtubule-binding domain of tau proteins. J. Biol. Chem. 263, 7703-7707.
2. Barnes, G., Louie, K.A., and Botstein, O. (1992). Yeast proteins associated with microtubules in vitro and in vivo. Mol. Biol. Cell 3, 29-47.
3. Bokros, C.L., Hugdahl, J.D., Kim, H.-H., Hanesworth, V.R., Heerden, A.V., Browning, K.S., and Morejohn, L.C. (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.
4. Butner, K.A., and Kirschner, M.W. (1991). Tau protein binds to microtubules through a flexible array of distributed weak sites. J. Cell Biol 115, 717-730
5. Cassimeris, L. (1993). Regulation of microtubule dynamic instability. Cell Motil. Cytoskeleton 26, 275-281.
6. Chapin, S.J., and Bulinski, J.C. (1992). Microtubule stabilization by assembly-promoting microtubule-associated proteins: A repeat performance. Cell Motil. Cytoskeleton 23, 236-243.
7. Cleveland, D.W. (1990). Microtubule MAPping. Cell 60, 701-702.
8. Cole, N.B., and Lippincott-Schwartz, J. (1995). Organization of organelles and membrane traffic by microtubules. Curr. Opin. Cell Biol. 7, 55-64.
9. Cyr, R.J. (1991a). Microtubule-associated proteins in higher plants. In The Cytoskeletal Basis of Plant Growth and Form, C.W. Lloyd, ed (San Diego, CA: Academic Press), pp. 57-67.
10. Cyr, R.J. (1991b). Calcium/calmodulin affects microtubule stability in lysed protoplasts. J. Cell Sci. 100, 311-317.
11. Cyr, R.J. (1994). Microtubules in plant morphogenesis: Role of the cortical array. Annu. Rev. Cell Biol. 10, 153-180.
12. Cyr, R.J., and Palevitz, B.A. (1989). Microtubule-binding proteins from carrot. I. Initial characterization and microtubule bundling. Planta 177, 245-260.
13. Cyr, R.J., and Palevitz, B.A. (1995). Organization of cortical microtubules in plant cells. Curr. Opin. Cell Biol. 7, 65-71.
14. Cyr, R.J., Bustos, M.M., Guiltinan, M.J., and Fosket, D.E. (1987). Developmental modulation of tubulin protein and mRNA levels during somatic embryogenesis in cultured carrot cells. Planta 171, 365-376.
15. Dhamodharan, R., and Wadsworth, P. (1995). Modulation of microtubule dynamic instability in vivo by brain microtubule associated proteins. J. Cell Sci. 108, 1679-1689.
16. Dibbayawan, T.P., Harper, J.D.I., Elliott, J.E., Gunning, B.E.S., and Marc, J. (1995). A γ-tubulin that associates specifically with centrioles in HeLa cells and the basal body complex in Chlamydomonas. Cell Biol. Int. 19, 559-567.
17. Drechsel, D.N., Hyman, A.A., Cobb, M.H., and Kirschner, M.W. (1992). Modulation of the dynamic instability of tubulin assembly by the microtubule-asscciated protein tau. Mol. Biol. Cell 3, 1141-1154.
18. Durso, N.A., and Cyr, R.J. (1994a). A calmodulin-sensitive interaction between microtubules and a higher plant homolog of elongation factor-1α. Plant Cell 6, 893-905.
19. Durso, N.A., and Cyr, R.J. (1994b). Beyond translation: Elongation factor-1α and the cytoskeleton. Protoplasma 180, 99-105.
20. Durso, N.A., and Cyr, R.J. (1995). Reply: A MAP by any other name would still bind to microtubules. Plant Cell 6, 1699-1702.
21. Durso, N.A., Leslie, J.D., and Cyr, R.J. (1996). In situ immunocytochemical evidence that a homolog of protein translation elongation factor EF-1α is associated with microtubules in carrot cells. Protoplasma 190, 141-150.
22. Fosket, D.E., and Morejohn, L.C. (1992). Structural and functional organization of tubulin. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43, 201-240.
23. Gelfand, V.I., and Bershadsky, A.D. (1991). Microtubule dynamics: Mechanism, regulation and function. Annu. Rev. Cell Biol. 7, 93-116.
24. Goddard, R.H., Wick, S.M., Silflow, C.D., and Snustad, D.P. (1994). Microtubule components of the plant cell cytoskeleton. Plant Physiol. 104, 1-6.
25. Gonzalez, M., Cambiazo, V., and Maccioni, R.B. (1935) Identification of a new microtubule-interacting protein Mip-90 Eur. J. Cell Biol. 67, 158-169.
26. Hall, J.L. (1983). Plasma membranes. In Isolation of Membranes and Organelles from Plant Cells, J.L. Hall and A.L. Moore, eds (London: Academic Press), pp. 55-81.
27. Harlow, E., and Lane, D. (1988). Antibodies. A Laboratory Manual (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory).
28. Heinlein, M., Epel, B.L., Padgett, H.S., and Beachy, R.N. (1995). Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science 270, 1983-1985.
29. Hirokawa, N., (1994). Microtubule organization and dynamics dependent on microtubule-associated proteins. Curr. Opin. Cell Biol. 6, 74-81.
30. Hjelmeland, L.M. (1980). A nondenaturing zwitterionic detergent for membrane biochemistry: Design and synthesis. Proc. Natl. Acad. Sci USA 77, 6368-6370.
31. Hoffman, J.C., Vaughn, K.C., and Joshi, H.C. (1994). Structural and immunocytochemical characterization of microtubule organizing centers in pteridophyte spermatogenous cells. Protoplasma 179, 46-60.
32. Hugdahl, J.D., Bokros, C.L., Hanesworth, V.R., Aalund, G.R., and Morejohn, L.C. (1993). Unique functional characteristics of the polymerization and MAP binding regulatory domains of plant tubulin. Plant Cell 5, 1063-1080.
33. Hussey, P.J., Snustad, D.P., and Silflow, C.D. (1991). Tubulin gene expression in higher plants. In The Cytosketetal Basis of Plant Growth and Form, C.W. Lloyd, ed (San Diego, CA: Academic Press), pp. 15-27.
34. Itoh, T., and Hotani, H. (1994) Microtubule-stabilizing activity of microtubule-associated proteins (MAPs) is due to increase in frequency of rescue in dynamic instability: Shortening length decreases with binding of MAPs onto microtubules. Cell Struct. Funct. 19, 279-290.
35. Jablonski, P.P., Elliott, J., and Williamson, R.E. (1993). Purification of a mung bean protein binding to microtubules through two defined sites in the carboxyl-terminal domain of β-tubulin. Plant Sci. 94, 35-45.
36. Jiang, C.-J., and Sonobe, S. (1993). Identification and preliminary characterization of a 55 kD higher-plant microtubule-associated protein J. Cell Sci. 105, 891-901.
37. Joshi, H.C. (1994). Microtubule organizing centers and γ-tubulin. Curr. Opin. Cell Biol. 6, 55-62.
38. Kellogg, D.R., Field, C.M., and Alberts, B.M. (1989). Identification of microtubule-associated proteins in the centrosome, spindle, and kinetochore of the early Drosophila embryo. J Cell Biol. 109, 2977-2991.
39. Kellogg, D.R., Moritz, M., and Alberts, B.M. (1994). The centrosome and cellular organization. Annu. Rev. Biochem. 63, 639-674.
40. Kirschner, M., and Mitchison, T. (1986). Beyond self-assembly: From microtubules to morphogenesis. Cell 45, 329-342.
41. Kumagai, F., Hasezawa, S., Takahashi, Y., and Nagata, T. (1995). The involvement of protein synthesis elongation factor 1α in the organization of microtubules on the perinuclear region during the cell cycle transition from M phase to G1 phase in tobacco BY-2 cells. Bot. Acta 108, 467-473.
42. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
43. Lambert, A.-M. (1993). Microtubule-organizing centers in higher plants. Curr. Opin. Cell Biol. 5, 116-122.
44. Lancelle, S.A., and Hepler, P.K. (1992). Ultrastructure of freeze-substituted pollen tubes of Lilium longiflorum. Protoplasma 167, 215-230.
45. Liu, B., Marc, J., Joshi, H.C., and Palevitz, B.A. (1993). A γ-tubulin-related protein associated with the microtubule arrays of higher plants in a cell cycle-dependent manner. J. Cell Sci. 104, 1217-1228.
46. Liu, B., Joshi, H.C., Wilson, T.J., Silflow, C.D., Palevitz, B.A., and Snustad, D.P. (1994). γ-Tubulin in Arabidopsis: Gene sequence, immunoblot, and immunofluorescence studies. Plant Cell 6, 303-314.
47. Liu, B., Cyr, R.J., and Palevitz, B.A. (1996). A kinesin-like protein, KatAp, in the cells of Arabidopsis and other plants. Plant Cell 8, 119-132
48. Maekawa, T., Ogihata, S., Murofushi, H., and Nagai, R. (1990). Green algal microtubule-associated protein with a molecular weight of 90 kD which bundles microtubules. Protoplasma 158, 10-18.
49. Mandelkow, E., and Mandelkow, E.-M. (1995). Microtubules and microtubule-associated proteins. Curr. Opin. Cell Biol. 7, 72-81.
50. Marc, J. (1991). Protein components of plasma membrane-associated cytoskeleton. Plant Physiol. 96 (suppl.), 128 (abstr.).
51. Marc, J., and Palevitz, B.A. (1990). Regulation of the spatial order of cortical microtubules in developing guard cells of Allium. Planta 182, 626-634.
52. Marc, J., Mineyuki, Y., and Palevitz, B.A. (1989). The generation and consolidation of a radial array of cortical microtubules in developing guard cells of Allium cepa L. Planta 179, 516-529.
53. Marc, J., Durso, N., Zhang, M., and Cyr, R. (1994). Microtubule-binding proteins from tobacco membranes. Mol. Biol. Cell 5 (suppl.), 289 (abstr.).
54. Marc, J., Sharkey, D.E., and Cyr, R.J. (1995). A 90 kD microtubule-binding protein from tobacco membranes. J. Cell. Biochem. 21A (suppl.), 446 (abstr.).
55. Masson, D., and Kreiss, T.E. (1993). Identification and molecular characterization of E-MAP-115, a novel microtubule-associated protein predominantly expressed in epithelial cells. J. Cell Biol. 123, 357-371.
56. Mays, R.W., Beck, K.A., and Nelson, W.J. (1994). Organization and function of the cytoskeleton in polarized epithelial cells: A component of the protein sorting machinery. Curr. Opin. Cell Biol. 6, 16-24.
57. Michalik, L., Vanier, M.-T., and Launay, J.-F. (1991). Microtubule affinity chromatography: A new technique for isolating microtubule-binding proteins from rat pancreas. Cell Mol. Biol. 37, 805-811.
58. Mitsui, H., Nakatani, K., Yamaguchi-Shinozaki, K., Shinozaki, K., Nishikawa, K., and Takahashi, H. (1994). Sequencing and characterization of the kinesin-related genes katB and katC of Arabidopsis thaliana. Plant Mol. Biol. 25, 865-876.
59. Moritz, M., Braunfeld, M.B., Sedat, J.W., Alberts, B., and Agard, D.A. (1995). Microtubule nucleation by γ-tubulin-containing rings in the centrosome. Nature 378, 638-640.
60. Morrissey, J.H. (1981). Silver stain for proteins in polyacrylamide gels: A modified procedure with enhanced uniform sensitivity. Anal. Biochem. 117, 307-310.
61. Nagata, T., Okada, K., Takebe, I., and Matsui, C. (1981). Delivery of tobacco mosaic virus RNA into plant protoplasts mediated by reverse-phase evaporation vesicles (liposomes). Mol. Gen. Genet. 184, 161-165.
62. Nick, P., Lambert, A.-M., and Vantard, M. (1995). A microtubule associated protein in maize is expressed during phytochrome-induced cell elongation. Plant J. 8, 835-844
63. Oakley, B.R. (1992) γ-Tubulin: The microtubule organizer? Trends Cell Biol. 2, 1-5.
64. Olmsted, J.B. (1986). Microtubule-associated proteins. Annu Rev. Cell Biol. 2, 421-457.
65. Pedrotti, B., Colombo, R., and Islam, K. (1994). Microtubule associated protein MAP1A is an actin-binding and crosslinking protein. Cell Motil. Cytoskeleton 29, 110-116.
66. Pierre, P., Scheel, J., Rickard, J.E., and Kreis, T.E. (1992). CLIP-170 links endocytic vesicles to microtubules Cell 70, 887-900.
67. Preuss, U., Doring, F., Illenberger, S., and Mandelkow, E.-M. (1995). Cell cycle-dependent phosphorylation and microtubule binding of tau protein stably transfected into Chinese hamster ovary cells. Mol. Biol. Cell 6, 1397-1410.
68. Pryer, U.K., Walker, R.A., Skeen, V.P., Bourns, B.D., Soboeiro, V.F., and Salmon, E.D. (1992). Brain microtubule-associated proteins modulate microtubule dynamic instability in vitro. Real-time observations using video microscopy. J. Cell Sci. 103, 965-976.
69. Sandelius, A.S., and Morre, D.J. (1990). Plasma membrane isolation. In The Plant Plasma Membrane, C. Larsson and I.M. Moller, eds (Berlin: Springer-Verlag), pp. 45-75.
70. Schellenbaum, P., Vantard, M., and Lambert, A.-M. (1992). Higher plant microtubule-associated proteins (MAPs): A survey. Biol. Cell 76, 359-364.
71. Schellenbaum, P., Vantard, M., Peter, C., Fellous, A., and Lambert, A.-M. (1993). Co-assembly properties of higher plant microtubule-associated proteins with purified brain and plant tubulins. Plant J 3, 253-260.
72. Sokal, R.R., and Bohlf, F.J. (1995). Biometry: The Principles and Practice of Statistics in Biological Research, 3rd ed. (New York: Freeman and Co)
73. 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.
74. Tiezzi, A., Moscatelli, A., Cai, A, Bartalesi, A., and Cresti, M. (1992). An immunoreactive homolog of mammalian kinesin in Nicotiana tabacum pollen tubes. Cell Motil. Cytoskeleton 21, 132-137.
75. Towbin, H., Staehelin, T., and Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedures and some applications. Proc. Natl. Acad. Sci. USA 76, 4350-4354.
76. Traas, J.A. (1990). The plasma membrane associated cytoskeleton. In The Plant Plasma Membrane, C. Larsson and I.M. Moller, eds (Berlin: Springer-Verlag), pp. 269-292.
77. Vallee, R.B. (1982). A taxol-dependent procedure for the isolation of microtubules and microtubule-associated proteins (MAPs). J. Cell Biol. 92, 435-442.
78. Vandecandelaere, A., Martin, S.R., and Bayley, P.M. (1995). Regulation of microtubule dynamic instability by tubulin-GDP. Biochemistry 34, 1332-1343
79. Vantard, M., Schellenbaum, P., Fellous, A., and Lambert, A.-E. (1991). Characterization of maize microtubule-associated proteins, one of which is immunologically related to tau. Biochemistry 30, 9334-9340.
80. Vasquez, R.J., Gard, D.L., and Cassimeris, L. (1994). XMAP from Xenopus eggs promotes rapid plus end assembly of microtubules and rapid microtubule polymer turnover. J. Cell Biol. 127, 985-993.
81. Wiche, G., Oberkanins, C., and Himmler, A. (1991). Molecular structure and function of microtubule-associated proteins. Int. Rev. Cytol. 124, 217-273.
82. Williamson, R.E. (1991). Orientation of cortical microtubules in interphase plant cells. Int. Rev. Cytol. 129, 135-206.
83. Zheng, Y., Wong, M.L., Alberts, B., and Mitchison, T. (1995). Nucleation of microtubule assembly by a γ-tubulin-containing ring complex. Nature 378, 578-583.