Cell cycle regulation of the microtubular cytoskeleton

  • Marylin Vantard
  • Rachel Cowling
  • Catherine Delichère

Abstract

The microtubular element of the plant cytoskeleton undergoes dramatic architectural changes in the course of the cell cycle, specifically at the entry into and exit from mitosis. These changes underlie the acquisition of specialized properties and functions involved, for example, in the equal segregation of chromosomes and the correct positioning and formation of the new cell wall. Here we review some of the molecular mechanisms by which the dynamics and the organization of microtubules are regulated and suggest how these mechanisms may be under the control of cell cycle events.

Key words

cell cycle cytoskeleton microtubules microtubule-associated proteins plants tubulin 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Andersen, S.S.L. and Karsenti, E. 1997. XMAP310: a Xenopus rescue-promoting factor localized to the mitotic spindle. J. Cell. Biol. 139: 975–983.PubMedCrossRefGoogle Scholar
  2. Andersen, S.S.L., Buendia, B., Dominguez, J.E., Sawyer, A. and Karsenti, E. 1994. Effects on microtubule dynamics of XMAP230, a microtubule-associated protein present in Xenopus laevis eggs and dividing cells. J. Cell. Biol. 127: 1289–1299.PubMedCrossRefGoogle Scholar
  3. Arundhati, A., Feiler, H., Traas, J., Zhang, H., Lunness, P.A. and Doonan, J.H. 1995. A novel Arabidopsis type 1 protein phosphatase is highly expressed in male and female tissues and functionally complements a conditional cell cycle mutant of Aspergillus. Plant J. 7: 823–834.PubMedCrossRefGoogle Scholar
  4. Asada, T. and Collings, D. 1997. Molecular motors in higher plants. Trends Plant Sci. 2: 29–37.CrossRefGoogle Scholar
  5. Asada, T., Sonobe, S. and Shibaoka, H. 1991. Microtubule translocation in the cytokinetic apparatus of cultured tobacco cells. Nature 350: 238–241.CrossRefGoogle Scholar
  6. Asada, T., Kuriyama, R. and Shibaoka, H. 1997. TKRP125, a kinesin-related protein involved in the centrosome-independent Organization of the cytokinetic apparatus in tobacco BY-2 cells. J. Cell Sci. 110: 179–189.PubMedGoogle Scholar
  7. Balczon, R. 1996. The centrosome in animal cells and its functional homologues in plant and yeast cells. Int. Rev. Cytol. 169: 25–82.PubMedCrossRefGoogle Scholar
  8. Belmont, L. and Mitchison, T. 1996. Identification of a protein that interacts with tubulin dimers and increases the catastrophe rates of microtubules. Cell 84: 623–631.PubMedCrossRefGoogle Scholar
  9. Binarova, P., Hause, B., Dolezel, J., Draber, P. 1998a. Association of γ-tubulin with kinetochore/centromeric region of plant chromosomes. Plant J. 14: 751–757.CrossRefGoogle Scholar
  10. Binarova, P., Dolezel, J., Draber, P., Heberle-Bors, E., Strnad, M., Bogre, L. 1998b. Treatment of Vicia faba root tip cells with specific inhibitors to cyclin-dependent kinases leads to abnormal spindle formation. Plant J. 16: 697–707.PubMedCrossRefGoogle Scholar
  11. Bögre, L., Calderini, O., Binarova, P., Mattauch, M., Till, S., Kiegerl, S., Jonak, C., Pollaschek, C., Barker, P., Huskisson, N.S., Hirt, H. and Heberle-Bors, E. 1999. A MAP kinase is activated late in plant mitosis and becomes localized to the plane of cell division. Plant Cell 11: 101–114.PubMedGoogle Scholar
  12. Calderini, O, Bogre, L., Vicente, O., Binarova, P., Heberle-Bors, E. and Wilson, C. 1998. A cell cycle regulated MAP kinase with a possible role in cytokinesis in tobacco cells. J. Cell Sci. 111: 3091–3100.PubMedGoogle Scholar
  13. Cassimeris, L. 1999. Accessory protein regulation of microtubule dynamics throughout the cell cycle. Curr. Opin. Cell Biol. 11: 134–141.PubMedCrossRefGoogle Scholar
  14. Chan, J., Rutten, T. and Lloyd, C.W. 1996. Isolation of microtubule-associated proteins from carrot cytoskeletons: a 120 kDa MAP decorates all four microtubule arrays and the nucleus. Plant J. 10: 251–259.PubMedCrossRefGoogle Scholar
  15. Chang-Jie, J. and Sonobe, S. 1993. Identification and preliminary characterization of a 65 kDa higher-plant microtubule-associated protein. J. Cell Sci. 105: 891–901.PubMedGoogle Scholar
  16. Chevrier, V., Komesli, S., Schmit, A.C., Vantard, M., Lambert, A.M. and Job, D. 1992. A monoclonal antibody, raised against mammalian centrosomes and screened by recognition of plant microtubule organizing centres, identifies a pericentriolar component in different cell types. J. Cell Sci. 101: 823–835.PubMedGoogle Scholar
  17. Clayton, L., Black, C.M. and Lloyd, C. 1985. Microtubule nucleating sites in higher plant identified by an autoantibody against pericentriolar material. Cell 35: 621–629.Google Scholar
  18. Cleary, A.L. and Smith, L.G. 1998. The Tangledl gene is required for spatial control of cytoskeletal arrays associated with cell division during maize leaf development. Plant Cell 10: 1875–1888.PubMedGoogle Scholar
  19. Cleary, A.L., Gunning, B.E.S., Wasteneys, G.O. and Hepler, P.K. 1992. Microtubule and F-actin dynamics at the division site in living Tradescantia stamen hairs. J. Cell Sci. 103: 977–988.Google Scholar
  20. Colasanti, J., Cho, S.O., Wick, S. and Sundaresan, V. 1993. Localization of the functional p34cdc2 homologue of maize in root tip and stomatal complex cells: association with predicted division sites. Plant Cell 5: 1101–1111.PubMedGoogle Scholar
  21. Cyr, R.J. and Palevitz, B.A. 1995. Organization of cortical microtubules in plant cells. Curr. Opin. Cell Biol. 7: 65–71.PubMedCrossRefGoogle Scholar
  22. Deavours, B.E., Reddy, A.S.N. and Walker, R.A. 1998. Cal-cium/calmodulin regulation of the Arabidopsis kinesin-like calmodulin-binding protein. Cell Motil. Cytoskel. 40: 408–416.CrossRefGoogle Scholar
  23. Del Vecchio, A.J., Harper, J.D., Vaughn, K.C., Baron, A.T., Salisbury, J.L. and Overall, R.L. 1997. Centrin homologues in higher plant cells are prominently associated with the developing cell plate. Protoplasma 196: 224–234.CrossRefGoogle Scholar
  24. Dictenberg, J.B., Zimmerman, W., Sparks, C.A., Young, A., Vidair, C., Zheng, Y., Carrington, W., Fay, F.S. and Doxsey, S.J. 1998. Pericentrin and γ-tubulin form a protein complex and are organized into a novel lattice at the centrosome. J. Cell Biol. 141: 163–174.PubMedCrossRefGoogle Scholar
  25. Durso, N.A. and Cyr, R.J. 1994. A calmodulin-sensitive interaction between microtubules and a higher plant homologue of protein translation elongation factor EF-α. Plant Cell 6: 893–905.PubMedGoogle Scholar
  26. Fanara, P., Oback, B., Ashman, K., Podtelejnikov, A. and Brandt, R. 1999. Identification of MINUS, a small polypeptide that functions as a microtubule nucleation suppressor. EMBO J. 18: 565–577.PubMedCrossRefGoogle Scholar
  27. Flurkey, W.H., Prentice, D.A., Fox, M.T. and Hughes, J.R 1993. Stathmin in mung bean leaves and rat brain. Biochem. Biophys. Res. Commun. 196: 589–595.PubMedCrossRefGoogle Scholar
  28. Hazezawa, S. and Nagata, T. 1993. Microtubule organizing centers in plant cells: localization of a 49 kDa protein that is immunologically cross-reactive to 51 kDa protein from sea urchin centrosomes in synchronized BY-2 cells. Protoplasma 176: 64–74.CrossRefGoogle Scholar
  29. Hepler, P.K. and Hush, J.M. 1996. Behaviour of microtubules in living plant cells. Plant Physiol. 112: 455–461.PubMedGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. Hush, J.M., Wadsworth, P., Callahan, D.A. and Hepler, P.K. 1994. Quantification of microtubule dynamics in living plant cells. J. Cell Sci. 107: 775–784.PubMedGoogle Scholar
  32. Hush, J.M., Wu, L., John, P.C.L., Hepler, L.H. and Hepler, P.K. 1996. Plant mitosis promoting factors disassembles the microtubule preprophase band and accelerates prophase progression in Tradescantia. Cell Biol. Int. 20: 275–287.PubMedCrossRefGoogle Scholar
  33. Kellog, D.R., Moritz, M. and Alberts, B.M. 1994. The centrosome and cellular organization. Annu. Rev. Biochem. 63: 639–674.CrossRefGoogle Scholar
  34. Kumagai, F., Hazezawa, 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 Gl phase in tobacco BY-2 cells. Bot. Acta 108: 467–473.Google Scholar
  35. Lajoie-Mazenc, I., Tollon, Y., Detraves, C., Julian, M., Moisand, A., Gueth-Hallonet, C., Debec, A., Salles-Passador, I., Puget, A. and Mazarguil, H. 1994. Recruitment of antigenic gamma-tubulin during mitosis in animal cells: presence of gamma-tubulin in the mitotic spindle. J. Cell Sci. 107: 2825–2837.PubMedGoogle Scholar
  36. Lambert, A.M. 1993. Microtubule-organizing centres in higher plants. Curr. Opin. Cell Biol. 5: 116–122.PubMedCrossRefGoogle Scholar
  37. Liu, B., Joshi, H.C, Wilson, T.J., Silflow, C.D., Palevitz, B.A. and Snustad, D.P. 1994. Gamma-tubulin in Arabidopsis: gene sequence, immunoblot, and immunofluorescence studies. Plant Cell 6: 303–314.PubMedGoogle Scholar
  38. Liu, B., Cyr, R. and Palevitz, B.A. 1996. A kinesin-like protein, KatAp, in the cells of Arabidopsis and other plants. Plant Cell 8: 119–132.PubMedGoogle Scholar
  39. Lopez, I., Khan, S.S., Cande, W.Z. and Hussey, P.J. 1995. Isolation of a full-length cDNA encoding Zea mays gamma-tubulin. Plant Physiol. 107: 309–310.PubMedCrossRefGoogle Scholar
  40. McNally, F.J. and Thomas, S. 1998. Katanin is responsible for the M-phase microtubule severing activity in Xenopus eggs. Mol. Biol. Cell 9: 1847–1861.PubMedGoogle Scholar
  41. Marc, J. 1997. Microtubule-organizing centres in plants. Trends Plant Sci. 2: 223–230.CrossRefGoogle Scholar
  42. Marc, J., Mineyuki, Y. and Palevitz, B.A. 1989. The generation and consolidation of a radical array of cortical microtubules in developing guard cells of Allium cepa L. Planta 179: 516–529.CrossRefGoogle Scholar
  43. Marc, J., Sharkey, D.E., Durso, N.A., Zhang, M. and Cyr, R. 1996. Isolation of a 90 kDa microtubule-associated protein from tobacco membranes. Plant Cell 8: 2127–2138.PubMedGoogle Scholar
  44. Marc, J., Granger, C.L., Brincat, J., Fisher, D.D., Kao, T., Mc-Cubbin, A.G. and Cyr, R.J. 1998. A GFP-MAP4 reporter gene for vizualizing cortical microtubule rearrangements in living epidermal cells. Plant Cell 10: 1927–1939.PubMedGoogle Scholar
  45. Mayer, U., Herzog, U., Berger, F., Inzé, D. and Jürgens, G. 1999. Mutations in the PILZ group genes disrupt the microtubule cytoskeleton and uncouple cell cycle progression from cell division in Arabidopsis embryo and endosperm. Euro. J. Cell Biol. 78: 100–108.CrossRefGoogle Scholar
  46. Mineyuki, Y. 1999. The preprophase band of microtubules: its function as a cytokinetic apparatus in higher plants. Int. Rev. Cytol. 187: 1–49.CrossRefGoogle Scholar
  47. Mitsui, H., Yamaguchi-Shinozaki, K., Nishikawa, K. and Takahashi, H. 1993. Identification of a gene family (kat) encoding kinesin-like proteins in Arabidopsis thaliana and the characterization of secondary structure of KatA. Mol. Gen. Genet. 238: 362–368.PubMedCrossRefGoogle Scholar
  48. 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.PubMedCrossRefGoogle Scholar
  49. Mitsui, H., Hasezawa, S., Nagata, T. and Takahashi, H. 1996. Cell cycle-dependent accumulation of a kinesin-like protein, KatB/C, in synchronised tobacco BY-2 cells. Plant Mol. Biol. 30: 177–181.PubMedCrossRefGoogle Scholar
  50. Moore, J.D. and Endow, S.A. 1996. Kinesins proteins: a phylum of motors for microtubule-based motility. Bioessays 18: 207–219.PubMedCrossRefGoogle Scholar
  51. Moore, R.C., Zhang, M., Cassimeris, L. and Cyr, R. 1997. In vitro assembled plant microtubules exhibit a high state of dynamic instability. Cell Motil. Cytoskel. 38: 278–286.CrossRefGoogle Scholar
  52. Moore, R.C., Durso, N. and Cyr, R. 1998. Elongation factor-1α stabilizes microtubules in a calcium/calmodulin-dependent manner. Cell Motil. Cytoskel. 41: 168–180.CrossRefGoogle Scholar
  53. Morgensen, M., Mackie, J.B., Doxsey, S.J., Stearns, T. and Tucker, J.B. 1997. Centrosomal deployment of gamma-tubulin and pericentrin: evidence for a microtubule-nucleating domain and a minus-end docking domain in certain mouse epithelial cells. Cell Motil. Cytoskel. 36: 276–290.CrossRefGoogle Scholar
  54. Moudjou, M., Bordes, N., Paintrand, M. and Bornens, M. 1996. Gamma-tubulin in mammalian cells: the centrosomal and the cytosolic forms. J. Cell Sci. 4: 875–887.Google Scholar
  55. Nguyen, H.L., Chari, S., Gruber, D., Lue, C.M., Chapin, S.J. and Bulinski, J.C. 1997. Overexpression of full-or partial-length MAP4 stabilizes microtubules and alters cell growth. J. Cell Sci. 110: 281–294.PubMedGoogle Scholar
  56. Nick, P., Lambert, A.M. and Vantard, M. 1991. A microtubule-associated protein in maize is expressed during phytochrome-induced cell elongation. Plant J. 8: 835–844.CrossRefGoogle Scholar
  57. Ookata, K., Hisanaga, S., Bulinski, J.C., Murofushi, H., Aizawa, H.T., Itoh, J., Hotani, H., Okumura, E., Tachibana, K., Kishimoto, T. 1995. Cyclin B interaction with microtubule-associated protein 4 (MAP4) targets p34cdc2 kinase to microtubules and is a potential regulator of M-phase microtubule dynamics. J. Cell Biol. 128: 849–862.PubMedCrossRefGoogle Scholar
  58. Paoletti, A., Moudjou, M., Paintrand, M., Salisbury, J.L. and Bornens, M. 1996. Most of centrin in animal cells is not centrosome-associated and centrosomal centrin is confined to the distal lumen of centrioles. J. Cell Biol. 109: 3089–3102.Google Scholar
  59. Reddy, A.S.N., Narasimhulu, S.B., Safadi, F., Golovkin, M. and Hu, X. 1996a. A plant kinesin heavy chain-like protein is a calmodulin-binding protein. Plant J. 10: 9–21.PubMedCrossRefGoogle Scholar
  60. Reddy, A.S.N., Safadi, F., Narasimhulu, S.B., Golovkin, M. and Hu, X. 1996b. A novel plant calmodulin-binding protein with kinesin heavy motor domain. J. Biol. Chem. 271: 7052–7060.PubMedCrossRefGoogle Scholar
  61. Rodriguez, P.L., Leube, M.P and Grill, E. 1998. Molecular cloning in Arabidopsis thaliana of a new protein phosphatase 2C (PP2C) with homology to ABI1 and ABI2. Plant Mol. Biol. 38: 879–883.PubMedCrossRefGoogle Scholar
  62. Rutten, T., Chan, J. and Lloyd, C.W. 1997. A 60 kDa plant microtubule-associated protein promotes the growth and stabilization of neurotubules in vitro. Proc. Natl. Acad. Sci. USA 94: 4469–4474.PubMedCrossRefGoogle Scholar
  63. Schmit, A.C., Stoppin, V., Chevrier, V., Job, D. and Lambert, A.M. 1994. Cell cycle dependent distribution of a centrosomal antigen at the perinuclear MTOC or at the kinetochores of higher plant cells. Chromosoma 103: 343–351.PubMedCrossRefGoogle Scholar
  64. Smirnova, E., Cox, E.A., Bajer, A.S. 1995. Antibody against phosphorylated proteins (MPM-2) recognizes mitotic microtubules in endosperm cells of higher plant Haemanthus. Cell Motil. Cytoskel. 31:34–44.CrossRefGoogle Scholar
  65. Smirnova, E., Reddy, A.S.N., Bowser, J. and Bajer, A.S. 1998. Minus end-directed kinesin-like motor protein, KCBP, localizes to anaphase spindle poles in Haemanthus endosperm. Cell Motil. Cytoskel. 41:271–280.CrossRefGoogle Scholar
  66. Staiger, C. and Cande, W.Z. 1990. Microtubule distribution in dv, a maize meiotic mutant defective in the prophase to metaphase transition. Dev. Biol. 138: 231–242.PubMedCrossRefGoogle Scholar
  67. Stals, H., Bauwens, S., Traas, J., Van Montagu, M., Engler, G. and Inzé, D. 1997. Plant CDC2 is not only targeted to the pre-prophase band, but also co-localizes with the spindle, phragmoplast, and chromosomes. FEBS Lett. 418: 229–234.PubMedCrossRefGoogle Scholar
  68. Stoppin, V., Vantard, M., Schmit, A.C. and Lambert, A.M. 1994. Isolated plant nuclei nucleate microtubule assembly: the nuclear surface in higher plants has centrosome-like activity. Plant Cell 6: 1099–1106.PubMedGoogle Scholar
  69. Stoppin, V., Lambert, A.M. and Vantard, M. 1996. Plant microtubule-associated proteins (MAPs) affect microtubule nu-cleation and growth at plant nuclei and mammalian centrosomes. Eur. J. Cell Biol. 69: 11–23.PubMedGoogle Scholar
  70. Stoppin-Mellet, V., Peter, C., Buendia, B., Karsenti, E. and Lambert, A.M. 1999. Tobacco BY-2 cell-free extracts induce the recovery of microtubule nucleating activity of inactivated mammalian centrosomes. Biochim. Biophys. Acta 1449: 101–106.PubMedCrossRefGoogle Scholar
  71. Tassin, A.M., Celati, C., Moudjou, M. and Bornens, M. 1998. Characterization of the human homologue of the yeast spc98p and its association with gamma-tubulin. J. Cell Biol. 4: 689–701.CrossRefGoogle Scholar
  72. Tournebize, R., Andersen, S.S., Verde, F., Doree, M., Karsenti, E., Hyman, A.A. 1997. Distinct roles of PP1 and PPA-like phosphatase in control of microtubule dynamics during mitosis. EMBOJ. 16: 5537–5549.CrossRefGoogle Scholar
  73. Torres-Ruiz, R.A. and Jürgens, G. 1994. Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development 120: 2967–2978.PubMedGoogle Scholar
  74. Traas, J., Bellini, C., Nacry, P., Kronenberger, J., Bouchez, D. and Caboche, M. 1995. Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375: 676–677.CrossRefGoogle Scholar
  75. Vasquez, R.J., Gard, D.L. and Cassimeris, L. 1994. XMAP from Xenopus rescue-promoting factor localized to the mitotic spindle. J. Cell Biol. 139: 1289–1299.Google Scholar
  76. Vantard, M., Schellenbaum, P., Fellous, A. and Lambert, A.M. 1991. Characterization of maize microtubule-associated proteins, one of which is immunologically related to tau. Biochemistry 24: 9334–9340.CrossRefGoogle Scholar
  77. Vantard, M., Stoppin, V. and Lambert, A.M. 1998. Cell-cycle dependent nucleation and assembly of plant microtubular proteins. In: D. Francis, D. Dudits and D. Inzé (Eds.) Plant Cell Division, Portland Press, London, pp. 301–315.Google Scholar
  78. Vaughn, K. and Harper, J. 1998. Microtubule-organizing centres and nucleating sites in land plants. Int. Rev. Cytol. 181: 75–1149.PubMedCrossRefGoogle Scholar
  79. Wang, W., Takesawa, D., Narasimhulu, S.B., Reddy, A.S.N, and Poovaiah, B.W. 1996. A novel kinesin-like protein with calmodulin-binding domain. Plant Mol. Biol. 31: 87–100.PubMedCrossRefGoogle Scholar
  80. Wasteneys, G.O., Gunning, B.E.S. and Hepler, P.K. 1993. Microinjection of fluorescent brain tubulin reveals dynamic properties of cortical microtubules in living plant cells. Cell Motil. Cytoskel. 24:205–213.CrossRefGoogle Scholar
  81. Waterman-Store, CM. and Salmon, E.D. 1997. Microtubule dynamics: treadmilling comes around again. Curr. Biol. 7: 369–372.CrossRefGoogle Scholar
  82. Wheatley, S.P., Hinchcliff, E.H., Glotzer, M., Hyman, A.A., Sluder, G. and Wang, Y.I. 1997. CDK1 inactivation regulates anaphase spindle dynamics and cytokinesis in vivo. J. Cell Biol. 138: 385–393.PubMedCrossRefGoogle Scholar
  83. Wymer, C. and Lloyd, C.W. 1996. Dynamic microtubules: implications for cell-wall patterns. Trends Plant Sci. 1: 222–228.Google Scholar
  84. Yuan, M., Shaw, P.J., Warm, R.M. and Lloyd, C.W. 1994. Dynamic reorientation of cortical microtubules, from transverse to longitudinal, in living plant cells. Proc. Natl. Acad. Sci. USA. 91: 6050–6053.PubMedCrossRefGoogle Scholar
  85. Yuan, M., Warm, R.M., Shaw, P.J. and Lloyd, C.W. 1995. Dynamic microtubules under the radial and outer tangential walls of microinjected pea epidermal cells observed by computer reconstruction. Plant. J. 7: 17–23.PubMedCrossRefGoogle Scholar
  86. Zhang, D.H., Wadsworth, P. and Hepler, P.K. 1990. Microtubule dynamics in living dividing plant cells: confocal imaging of fluorescent brain tubulin. Proc. Natl. Acad. Sci. USA 87: 8820–8824.PubMedCrossRefGoogle Scholar
  87. Zimmerman, W., Sparks, C. and Doxsey, S.J. 1999. Amorphous no longer: the centrosome comes into focus. Curr. Opin. Cell Biol. 11: 122–128.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2000

Authors and Affiliations

  • Marylin Vantard
    • 1
  • Rachel Cowling
    • 1
  • Catherine Delichère
    • 1
  1. 1.Laboratoire de Physiologie Cellulaire VégétaleURA 576, DBMS-CEA/GrenobleGrenoble cedex 9France

Personalised recommendations