Skip to main content
PMC home page
The Plant Cell logoLink to The Plant Cell
. 1998 Nov;10(11):1791–1799. doi: 10.1105/tpc.10.11.1791

Nuclear localization signal receptor importin alpha associates with the cytoskeleton.

H M Smith 1, N V Raikhel 1
PMCID: PMC143961  PMID: 9811789

Abstract

Importin alpha is the nuclear localization signal (NLS) receptor that is involved in the nuclear import of proteins containing basic NLSs. Using importin alpha as a tool, we were interested in determining whether the cytoskeleton could function in the transport of NLS-containing proteins from the cytoplasm to the nucleus. Double-labeling immunofluorescence studies showed that most of the cytoplasmic importin alpha coaligned with microtubules and microfilaments in tobacco protoplasts. Treatment of tobacco protoplasts with microtubule- or microfilament-depolymerizing agents disrupted the strands of importin alpha in the cytoplasm, whereas a microtubule-stabilizing agent had no effect. Biochemical analysis showed that importin alpha associated with microtubules and microfilaments in vitro in an NLS-dependent manner. The interaction of importin alpha with the cytoskeleton could be an essential element of protein transport from the cytoplasm to the nucleus in vivo.

Full Text

The Full Text of this article is available as a PDF (861.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abe S., Davies E. Methods for isolation and analysis of the cytoskeleton. Methods Cell Biol. 1995;50:223–236. doi: 10.1016/s0091-679x(08)61033-x. [DOI] [PubMed] [Google Scholar]
  2. Ambron R. T., Schmied R., Huang C. C., Smedman M. A signal sequence mediates the retrograde transport of proteins from the axon periphery to the cell body and then into the nucleus. J Neurosci. 1992 Jul;12(7):2813–2818. doi: 10.1523/JNEUROSCI.12-07-02813.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barth A. I., Näthke I. S., Nelson W. J. Cadherins, catenins and APC protein: interplay between cytoskeletal complexes and signaling pathways. Curr Opin Cell Biol. 1997 Oct;9(5):683–690. doi: 10.1016/s0955-0674(97)80122-6. [DOI] [PubMed] [Google Scholar]
  4. Bassell G., Singer R. H. mRNA and cytoskeletal filaments. Curr Opin Cell Biol. 1997 Feb;9(1):109–115. doi: 10.1016/s0955-0674(97)80159-7. [DOI] [PubMed] [Google Scholar]
  5. Blank V., Kourilsky P., Israël A. NF-kappa B and related proteins: Rel/dorsal homologies meet ankyrin-like repeats. Trends Biochem Sci. 1992 Apr;17(4):135–140. doi: 10.1016/0968-0004(92)90321-y. [DOI] [PubMed] [Google Scholar]
  6. Clore A. M., Dannenhoffer J. M., Larkins B. A. EF-1[alpha] Is Associated with a Cytoskeletal Network Surrounding Protein Bodies in Maize Endosperm Cells. Plant Cell. 1996 Nov;8(11):2003–2014. doi: 10.1105/tpc.8.11.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Clubb B. H., Locke M. Peripheral nuclear matrix actin forms perinuclear shells. J Cell Biochem. 1998 Aug 1;70(2):240–251. doi: 10.1002/(sici)1097-4644(19980801)70:2<240::aid-jcb10>3.0.co;2-r. [DOI] [PubMed] [Google Scholar]
  8. Greber U. F., Suomalainen M., Stidwill R. P., Boucke K., Ebersold M. W., Helenius A. The role of the nuclear pore complex in adenovirus DNA entry. EMBO J. 1997 Oct 1;16(19):5998–6007. doi: 10.1093/emboj/16.19.5998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Görlich D., Dabrowski M., Bischoff F. R., Kutay U., Bork P., Hartmann E., Prehn S., Izaurralde E. A novel class of RanGTP binding proteins. J Cell Biol. 1997 Jul 14;138(1):65–80. doi: 10.1083/jcb.138.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Görlich D. Nuclear protein import. Curr Opin Cell Biol. 1997 Jun;9(3):412–419. doi: 10.1016/s0955-0674(97)80015-4. [DOI] [PubMed] [Google Scholar]
  11. Harter K., Kircher S., Frohnmeyer H., Krenz M., Nagy F., Schäfer E. Light-regulated modification and nuclear translocation of cytosolic G-box binding factors in parsley. Plant Cell. 1994 Apr;6(4):545–559. doi: 10.1105/tpc.6.4.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Heinlein M., Epel B. L., Padgett H. S., Beachy R. N. Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science. 1995 Dec 22;270(5244):1983–1985. doi: 10.1126/science.270.5244.1983. [DOI] [PubMed] [Google Scholar]
  13. Hicks G. R., Raikhel N. V. Protein import into the nucleus: an integrated view. Annu Rev Cell Dev Biol. 1995;11:155–188. doi: 10.1146/annurev.cb.11.110195.001103. [DOI] [PubMed] [Google Scholar]
  14. Hicks G. R., Raikhel N. V. Specific binding of nuclear localization sequences to plant nuclei. Plant Cell. 1993 Aug;5(8):983–994. doi: 10.1105/tpc.5.8.983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hicks G. R., Smith H. M., Lobreaux S., Raikhel N. V. Nuclear import in permeabilized protoplasts from higher plants has unique features. Plant Cell. 1996 Aug;8(8):1337–1352. doi: 10.1105/tpc.8.8.1337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hirokawa N. Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science. 1998 Jan 23;279(5350):519–526. doi: 10.1126/science.279.5350.519. [DOI] [PubMed] [Google Scholar]
  17. Hovland R., Hesketh J. E., Pryme I. F. The compartmentalization of protein synthesis: importance of cytoskeleton and role in mRNA targeting. Int J Biochem Cell Biol. 1996 Oct;28(10):1089–1105. doi: 10.1016/1357-2725(96)00059-3. [DOI] [PubMed] [Google Scholar]
  18. Izaurralde E., Kutay U., von Kobbe C., Mattaj I. W., Görlich D. The asymmetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus. EMBO J. 1997 Nov 3;16(21):6535–6547. doi: 10.1093/emboj/16.21.6535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jans D. A., Hübner S. Regulation of protein transport to the nucleus: central role of phosphorylation. Physiol Rev. 1996 Jul;76(3):651–685. doi: 10.1152/physrev.1996.76.3.651. [DOI] [PubMed] [Google Scholar]
  20. Jiang C. J., Weeds A. G., Hussey P. J. The maize actin-depolymerizing factor, ZmADF3, redistributes to the growing tip of elongating root hairs and can be induced to translocate into the nucleus with actin. Plant J. 1997 Nov;12(5):1035–1043. doi: 10.1046/j.1365-313x.1997.12051035.x. [DOI] [PubMed] [Google Scholar]
  21. Marc J., Sharkey D. E., Durso N. A., Zhang M., Cyr R. J. Isolation of a 90-kD Microtubule-Associated Protein from Tobacco Membranes. Plant Cell. 1996 Nov;8(11):2127–2138. doi: 10.1105/tpc.8.11.2127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. McLean B. G., Zupan J., Zambryski P. C. Tobacco mosaic virus movement protein associates with the cytoskeleton in tobacco cells. Plant Cell. 1995 Dec;7(12):2101–2114. doi: 10.1105/tpc.7.12.2101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mermall V., Post P. L., Mooseker M. S. Unconventional myosins in cell movement, membrane traffic, and signal transduction. Science. 1998 Jan 23;279(5350):527–533. doi: 10.1126/science.279.5350.527. [DOI] [PubMed] [Google Scholar]
  24. Palacios I., Hetzer M., Adam S. A., Mattaj I. W. Nuclear import of U snRNPs requires importin beta. EMBO J. 1997 Nov 17;16(22):6783–6792. doi: 10.1093/emboj/16.22.6783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Peifer M., Berg S., Reynolds A. B. A repeating amino acid motif shared by proteins with diverse cellular roles. Cell. 1994 Mar 11;76(5):789–791. doi: 10.1016/0092-8674(94)90353-0. [DOI] [PubMed] [Google Scholar]
  26. Sakamoto K., Nagatani A. Nuclear localization activity of phytochrome B. Plant J. 1996 Nov;10(5):859–868. doi: 10.1046/j.1365-313x.1996.10050859.x. [DOI] [PubMed] [Google Scholar]
  27. Schmalz D., Kalkbrenner F., Hucho F., Buchner K. Transport of protein kinase C alpha into the nucleus requires intact cytoskeleton while the transport of a protein containing a canonical nuclear localization signal does not. J Cell Sci. 1996 Sep;109(Pt 9):2401–2406. doi: 10.1242/jcs.109.9.2401. [DOI] [PubMed] [Google Scholar]
  28. Shimizu K., Shirataki H., Honda T., Minami S., Takai Y. Complex formation of SMAP/KAP3, a KIF3A/B ATPase motor-associated protein, with a human chromosome-associated polypeptide. J Biol Chem. 1998 Mar 20;273(12):6591–6594. doi: 10.1074/jbc.273.12.6591. [DOI] [PubMed] [Google Scholar]
  29. Smith E. F., Lefebvre P. A. PF16 encodes a protein with armadillo repeats and localizes to a single microtubule of the central apparatus in Chlamydomonas flagella. J Cell Biol. 1996 Feb;132(3):359–370. doi: 10.1083/jcb.132.3.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Smith H. M., Hicks G. R., Raikhel N. V. Importin alpha from Arabidopsis thaliana is a nuclear import receptor that recognizes three classes of import signals. Plant Physiol. 1997 Jun;114(2):411–417. doi: 10.1104/pp.114.2.411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sodeik B., Ebersold M. W., Helenius A. Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J Cell Biol. 1997 Mar 10;136(5):1007–1021. doi: 10.1083/jcb.136.5.1007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Staiger C. J., Cande W. Z. Microfilament Distribution in Maize Meiotic Mutants Correlates with Microtubule Organization. Plant Cell. 1991 Jun;3(6):637–644. doi: 10.1105/tpc.3.6.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Staiger C. J., Lloyd C. W. The plant cytoskeleton. Curr Opin Cell Biol. 1991 Feb;3(1):33–42. doi: 10.1016/0955-0674(91)90163-s. [DOI] [PubMed] [Google Scholar]
  34. Tiganis T., Flint A. J., Adam S. A., Tonks N. K. Association of the T-cell protein tyrosine phosphatase with nuclear import factor p97. J Biol Chem. 1997 Aug 22;272(34):21548–21557. doi: 10.1074/jbc.272.34.21548. [DOI] [PubMed] [Google Scholar]
  35. Ullman K. S., Powers M. A., Forbes D. J. Nuclear export receptors: from importin to exportin. Cell. 1997 Sep 19;90(6):967–970. doi: 10.1016/s0092-8674(00)80361-x. [DOI] [PubMed] [Google Scholar]
  36. Varagona M. J., Raikhel N. V. The basic domain in the bZIP regulatory protein Opaque2 serves two independent functions: DNA binding and nuclear localization. Plant J. 1994 Feb;5(2):207–214. doi: 10.1046/j.1365-313x.1994.05020207.x. [DOI] [PubMed] [Google Scholar]
  37. Varagona M. J., Schmidt R. J., Raikhel N. V. Nuclear localization signal(s) required for nuclear targeting of the maize regulatory protein Opaque-2. Plant Cell. 1992 Oct;4(10):1213–1227. doi: 10.1105/tpc.4.10.1213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wallin M., Strömberg E. Cold-stable and cold-adapted microtubules. Int Rev Cytol. 1995;157:1–31. doi: 10.1016/s0074-7696(08)62155-5. [DOI] [PubMed] [Google Scholar]
  39. Wang Y. X., Catlett N. L., Weisman L. S. Vac8p, a vacuolar protein with armadillo repeats, functions in both vacuole inheritance and protein targeting from the cytoplasm to vacuole. J Cell Biol. 1998 Mar 9;140(5):1063–1074. doi: 10.1083/jcb.140.5.1063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wedaman K. P., Meyer D. W., Rashid D. J., Cole D. G., Scholey J. M. Sequence and submolecular localization of the 115-kD accessory subunit of the heterotrimeric kinesin-II (KRP85/95) complex. J Cell Biol. 1996 Feb;132(3):371–380. doi: 10.1083/jcb.132.3.371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wozniak R. W., Rout M. P., Aitchison J. D. Karyopherins and kissing cousins. Trends Cell Biol. 1998 May;8(5):184–188. doi: 10.1016/s0962-8924(98)01248-3. [DOI] [PubMed] [Google Scholar]
  42. Yan C., Leibowitz N., Mélèse T. A role for the divergent actin gene, ACT2, in nuclear pore structure and function. EMBO J. 1997 Jun 16;16(12):3572–3586. doi: 10.1093/emboj/16.12.3572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. von Arnim A. G., Deng X. W. Light inactivation of Arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its nucleocytoplasmic partitioning. Cell. 1994 Dec 16;79(6):1035–1045. doi: 10.1016/0092-8674(94)90034-5. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES