Skip to main content
SpringerLink
Log in

Heat-shock protein 90 is associated with microtubules in tobacco cells

  • Original Papers
  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

The localization of HSP90 (heat-shock protein 90) was analyzed with respect to the microtubular cytoskeleton by double immunofluorescence and confocal laser microscopy in tobacco VBI-O cells during axial cell division and elongation. HSP90 was observed to be colocalized with cortical and radial microtubules and the nuclear envelope in premitotic cells, with the preprophase band, and with the phragmoplast. The HSP90 epitope could not be detected in mature division spindles. The association of the HSP90 epitope with radial and cortical microtubules was not continuous in space. HSP90 was organized in discrete foci that were found to be aligned with microtubules, and the distance between these foci increased, when the cells entered the elongation phase. Elimination of microtubules by drugs resulted in a loss of cell axiality and alignment of the HSP90 epitope. Together with biochemical data demonstrating binding of tobacco HSP90 to tubulin dimers these data indicate a possible role of HSP90 in the organization of microtubules.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

EPC:

ethyl-N-phenylcarbamate

FITC:

fluorescein isothiocyanate

HSP90:

heat-shock protein 90

MAP:

microtubuleassociated protein

TRITC:

tetramethylrhodamine B isothiocyanate

References

  • Ansorge W (1982) Fast visualization of protein bands by impregnation in potassium permanganate and silver nitrate. Electrophoresis 82: 235–242

    Google Scholar 

  • Biancaflor EB, Hasenstein KH (1993) Organization of cortical microtubules in graviresponding maize roots. Planta 191: 230–237

    Google Scholar 

  • Brown CR, Doxsey SJ, Hong-Brown LQ, Martin RL, Welch WJ (1996) Molecular chaperones and the centrosome. J Biol Chem 271: 824–832

    Google Scholar 

  • Burns RG, Surridge CD (1994) Tubulin: conservation and structure. In: Hyams JS, Lloyd CW (eds) Microtubules. Wiley, New York, pp 3–31

    Google Scholar 

  • Cleveland DW (1987) The multitubulin hypothesis revisited: what have we learned? J Cell Biol 104: 361–383

    Google Scholar 

  • Czar MJ, Welsh MJ, Pratt WB (1996) Immunofluorescence localization of the 90-kDa heat-shock protein to the cytoskeleton. Eur J Cell Biol 70: 322–330

    Google Scholar 

  • Duckett CM, Lloyd CW (1994) Gibberellic acid-induced microtubule reorientation in dwarf peas is accompanied by rapid modification of an α-tubulin isotype. Plant J 5: 363–372

    Google Scholar 

  • Freudenreich A, Nick P (1998) Microtubular organization in tobacco cells: heat shock protein 90 can bind to tubulin in vitro. Bot Acta 111: 1–7

    Google Scholar 

  • Giddings TH, Staehelin A (1991) Microtubule-mediated control of microfibril deposition: a re-examination of the hypothesis. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 85–99

    Google Scholar 

  • Goddard RH, Wick SM, Silflow CD, Snustad DP (1994) Microtubule components of the plant cell cytoskeleton. Plant Physiol 104: 1–6

    Google Scholar 

  • Goldman GH, Temmerman W, Jacobs D, Contreras R, van Montagu M, Herrera-Estrella A (1993) A nucleotide substitution in one of the β-tubulin genes ofTrichoderma viridis confers resistance to the antimitotic drug methylbenzimidazole-2-yl-carbamate. Mol Gen Genet 240: 73–80

    Google Scholar 

  • Green PB (1980) Organogenesis: a biophysical view. Annu Rev Plant Physiol 31: 51–82

    Google Scholar 

  • Heller R (1953) Studies on the mineral nutrition of in vitro plant tissue cultures (in French). Ann Sci Nat Bot Biol Veg 14: 1–223

    Google Scholar 

  • Himmelspach R, Nick P, Schäfer E, Ehmann B (1997) Developmental and light-dependent changes of the cytosolic chaperonin containing TCP-1 (CCT) subunits in maize seedlings, and the localization in coleoptiles. Plant J 12: 1299–1310

    Google Scholar 

  • Katsuta J, Shibaoka H (1988) The roles of the cytoskeleton and the cell wall in nuclear positioning in tobacco BY-2 cells. Plant Cell Physiol 29: 403–413

    Google Scholar 

  • Kimura Y, Yahara I, Lindquist S (1995) Role of the protein chaperone YDJI in establishing Hsp90-mediated signal transduction pathways. Science 268: 1362–1365

    Google Scholar 

  • Koyasu S, Nishida E, Kadowaki T, Matsuzaki F, lida K, Harada F, Kasuga M, Sakai H, Yahara I (1986) Two mammalian heat shock proteins, HSP90 and HSP100, are actin-binding proteins. Proc Natl Acad Sci USA 83: 8054–8058

    Google Scholar 

  • Lambert AM (1993) Microtubule-organizing centers in higher plants. Curr Opin Cell Biol 5: 116–122

    Google Scholar 

  • Laskowski MJ (1990) Microtubule orientation in pea stem cells: a change in orientation follows the initiation of growth rate decline. Planta 181: 44–52

    Google Scholar 

  • Liang P, MacRae TH (1997) Molecular chaperones and the cytoskeleton. J Cell Sci 110: 1431–1440

    Google Scholar 

  • Lloyd CW (1991) Cytoskeletal elements of the phragmosome establish the division plane in vacuolated plant cells. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 245–257

    Google Scholar 

  • —, Seagull RW (1985) A new spring for plant cell biology: microtubules as dynamic helices. Trends Biochem Sci 10: 476–478

    Google Scholar 

  • Malus A (1990) Microtubule-associated proteins. Curr Opin Cell Biol 2: 10–14

    Google Scholar 

  • Mitchison T, Kirschner M (1984) Microtubule assembly nucleated by isolated centrosomes. Nature 312: 232–237

    Google Scholar 

  • Mizuno K (1994) Inhibition of gibberellin-induced elongation, reorientation of cortical microtubules and change of isoform of tubulin in epicotyl segments of azuki bean by protein kinase inhibitors. Plant Cell Physiol 35: 1149–1157

    Google Scholar 

  • —, Suzaki T (1990) Effects of anti-microtubule drugs on in vitro polymerization of tubulin from mung bean. Bot Mag Tokyo 103: 435–448

    Google Scholar 

  • Morejohn LC (1991) The molecular pharmacology of plant tubulin and microtubules. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 29–43

    Google Scholar 

  • Nick P, Bergfeld R, Schäfer E, Schopfer P (1990) Unilateral reorientation of microtubules at the outer epidermal wall during photo- and gravitropic curvature of maize coleoptiles and sunflower hypocotyls. Planta 181: 162–168

    Google Scholar 

  • —, Lambert AM, Vantard M (1995) A microtubule-associated protein in maize is induced during phytochrome-dependent cell elongation. Plant J 8: 835–844

    Google Scholar 

  • Opatrný Z, Opatrná A (1976) The specificity of the effect of 2,4-D and NAA on the growth, micromorphology and the occurrence of starch in long-termNicotiana tabacum cell strains. Biol Plant 18: 381–400

    Google Scholar 

  • Panteris E, Apostolakos P, Galatis B (1995) The effect of taxol onTriticum preprophase root cells: preprophase microtubule band organization seems to depend on new microtubule assembly. Protoplasma 186: 72–78

    Google Scholar 

  • Parness J, Horwitz SB (1981) Taxol binds to polymerized tubulin in vitro. J Cell Biol 91: 479–487

    Google Scholar 

  • Schröder G, Beck M, Eichel J, Vetter HP, Schröder J (1993) HSP90 homologue from Madagascar periwinkle (Catharanthus roseus): cDNA sequence, regulation of protein expression and localization in the endoplasmic reticulum. Plant Mol Biol 23: 583–594

    Google Scholar 

  • Shelanski ML, Gaskin F, Cantor CR (1973) Assembly of microtubules in the absence of added nucleotide. Proc Natl Acad Sci USA 70: 765–768

    Google Scholar 

  • Shibaoka H (1994) Plant hormone-induced changes in the orientation of cortical microtubules: alterations in the cross-linking between microtubules and the plasma membrane. Annu Rev Plant Physiol Plant Mol Biol 45: 527–544

    Google Scholar 

  • Smertenko AP, Blume Y, Viklicky V, Draber P (1997a) Exposure of tubulin structural domains inNicotiana tabacum microtubules probed by monoclonal antibodies. Eur J Cell Biol 72: 104–112

    Google Scholar 

  • —, Draber P, Viklický V, Opatrný Z (1997b) Heat stress affects the organization of microtubules and cell division inNicotiana tabacum cells. J Exp Bot 20: 1534–1542

    Google Scholar 

  • Stoppin V, Vantard M, Schmit AC, Lambert AM (1994) Isolated plant nuclei nucleate microtubule assembly: the nucleus surface in higher plants has centrosome-like activity. Plant Cell 6: 1099–1106

    Google Scholar 

  • Sullivan KF (1988) Structure and utilization of tubulin isotypes. Annu Rev Cell Biol 1: 687–713

    Google Scholar 

  • Toyomasu T, Yamane H, Murofushi N, Nick P (1994) Phytochrome inhibits the effectiveness of gibberellins to induce cell elongation in rice. Planta 194: 256–263

    Google Scholar 

  • Vantard M, Levilliers N, Hill AM, Adoutte A, Lambert AM (1990) Incorporation ofParamecium axonemal tubulin into higher plant cells reveals functional sites of microtubule assembly. Proc Natl Acad Sci USA 87: 8825–8829

    Google Scholar 

  • —, Schellenbaum P, Fellous A, Lambert AM (1991) Characterization of maize microtubule-associated proteins, one of which is immunologically related to tau. Biochemistry 30: 9334–9340

    Google Scholar 

  • —, Peter C, Fellous A, Schellenbaum P, Lambert AM (1994) Characterization of a 100-kDa heat-stable microtubule-associated protein from higher plants. Eur J Biochem 220: 847–853

    Google Scholar 

  • Wiech H, Buchner J, Zimmermann R, Jakob U (1992) Hsp90 chaperones protein folding in vitro. Nature 358: 169–172

    Google Scholar 

  • Williamson RE (1991) Orientation of cortical microtubules in interphase plant cells. Int Rev Cytol 129: 135–206

    Google Scholar 

  • Yasuhara H, Sonobe S, Shibaoka H (1993) Effects of taxol on the development of the cell plate and of the phragmoplast in tobacco BY-2 cells. Plant Cell Physiol 34: 21–29

    Google Scholar 

  • Yuan M, Shaw PJ, Warn RM, Lloyd CW (1994) Dynamic reorientation of cortical microtubules from transverse to longitudinal, in living plant cells. Proc Natl Acad Sci USA 91: 6050–6053

    Google Scholar 

  • Zhang D, Waldsworth P, Hepler PK (1990) Microtubule dynamics in living dividing plant cells: confocal imaging of microinjected fluorescent brain tubulin. Proc Natl Acad Sci USA 87: 8820–8824

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Biologie II, Albert-Ludwigs-Universität Freiburg, Schänzlestrasse 1, D-79104, Freiburg, Federal Republic of Germany

    J. Petrášek, A. Freudenreich, A. Heuing & P. Nick

  2. Research Institute of Crop Production, Prague

    Z. Opatrný

  3. Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Prague

    J. Petrášek

Authors
  1. J. Petrášek
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Freudenreich
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Heuing
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Z. Opatrný
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. Nick
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Petrášek, J., Freudenreich, A., Heuing, A. et al. Heat-shock protein 90 is associated with microtubules in tobacco cells. Protoplasma 202, 161–174 (1998). https://doi.org/10.1007/BF01282544

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01282544

Keywords

Search

Navigation