Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1989 Apr 1;108(4):1445–1452. doi: 10.1083/jcb.108.4.1445

Microtubule polarities indicate that nucleation and capture of microtubules occurs at cell surfaces in Drosophila

PMCID: PMC2115526  PMID: 2925791

Abstract

Hook decoration with pig brain tubulin was used to assess the polarity of microtubules which mainly have 15 protofilaments in the transcellular bundles of late pupal Drosophila wing epidermal cells. The microtubules make end-on contact with cell surfaces. Most microtubules in each bundle exhibited a uniform polarity. They were oriented with their minus ends associated with their hemidesmosomal anchorage points at the apical cuticle-secreting surfaces of the cells. Plus ends were directed towards, and were sometimes connected to, basal attachment desmosomes at the opposite ends of the cells. The orientation of microtubules at cell apices, with minus ends directed towards the cell surface, is opposite to the polarity anticipated for microtubules which have elongated centrifugally from centrosomes. It is consistent, however, with evidence that microtubule assembly is nucleated by plasma membrane-associated sites at the apical surfaces of the cells (Mogensen, M. M., and J. B. Tucker. 1987. J. Cell Sci. 88:95- 107) after these cells have lost their centriole-containing, centrosomal, microtubule-organizing centers (Tucker, J. B., M. J. Milner, D. A. Currie, J. W. Muir, D. A. Forrest, and M.-J. Spencer. 1986. Eur. J. Cell Biol. 41:279-289). Our findings indicate that the plus ends of many of these apically nucleated microtubules are captured by the basal desmosomes. Hence, the situation may be analogous to the polar-nucleation/chromosomal-capture scheme for kinetochore microtubule assembly in mitotic and meiotic spindles. The cell surface-associated nucleation-elongation-capture mechanism proposed here may also apply during assembly of transcellular microtubule arrays in certain other animal tissue cell types.

Full Text

The Full Text of this article is available as a PDF (2.9 MB).

Selected References

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

  1. BYERS B., PORTER K. R. ORIENTED MICROTUBULES IN ELONGATING CELLS OF THE DEVELOPING LENS RUDIMENT AFTER INDUCTION. Proc Natl Acad Sci U S A. 1964 Oct;52:1091–1099. doi: 10.1073/pnas.52.4.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baas P. W., White L. A., Heidemann S. R. Microtubule polarity reversal accompanies regrowth of amputated neurites. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5272–5276. doi: 10.1073/pnas.84.15.5272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brinkley B. R. Microtubule organizing centers. Annu Rev Cell Biol. 1985;1:145–172. doi: 10.1146/annurev.cb.01.110185.001045. [DOI] [PubMed] [Google Scholar]
  4. Bré M. H., Kreis T. E., Karsenti E. Control of microtubule nucleation and stability in Madin-Darby canine kidney cells: the occurrence of noncentrosomal, stable detyrosinated microtubules. J Cell Biol. 1987 Sep;105(3):1283–1296. doi: 10.1083/jcb.105.3.1283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Calarco-Gillam P. D., Siebert M. C., Hubble R., Mitchison T., Kirschner M. Centrosome development in early mouse embryos as defined by an autoantibody against pericentriolar material. Cell. 1983 Dec;35(3 Pt 2):621–629. doi: 10.1016/0092-8674(83)90094-6. [DOI] [PubMed] [Google Scholar]
  6. Chalfie M., Thomson J. N. Structural and functional diversity in the neuronal microtubules of Caenorhabditis elegans. J Cell Biol. 1982 Apr;93(1):15–23. doi: 10.1083/jcb.93.1.15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Eichenlaub-Ritter U. Spatiotemporal control of functional specification and distribution of spindle microtubules with 13, 14 and 15 protofilaments during mitosis in the ciliate Nyctotherus. J Cell Sci. 1985 Jun;76:337–355. doi: 10.1242/jcs.76.1.337. [DOI] [PubMed] [Google Scholar]
  8. Eichenlaub-Ritter U., Tucker J. B. Microtubules with more than 13 protofilaments in the dividing nuclei of ciliates. Nature. 1984 Jan 5;307(5946):60–62. doi: 10.1038/307060a0. [DOI] [PubMed] [Google Scholar]
  9. Euteneuer U., McIntosh J. R. Polarity of midbody and phragmoplast microtubules. J Cell Biol. 1980 Nov;87(2 Pt 1):509–515. doi: 10.1083/jcb.87.2.509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Euteneuer U., McIntosh J. R. Polarity of some motility-related microtubules. Proc Natl Acad Sci U S A. 1981 Jan;78(1):372–376. doi: 10.1073/pnas.78.1.372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Euteneuer U., McIntosh J. R. Structural polarity of kinetochore microtubules in PtK1 cells. J Cell Biol. 1981 May;89(2):338–345. doi: 10.1083/jcb.89.2.338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Evans L., Mitchison T., Kirschner M. Influence of the centrosome on the structure of nucleated microtubules. J Cell Biol. 1985 Apr;100(4):1185–1191. doi: 10.1083/jcb.100.4.1185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Freeman M., Nüsslein-Volhard C., Glover D. M. The dissociation of nuclear and centrosomal division in gnu, a mutation causing giant nuclei in Drosophila. Cell. 1986 Aug 1;46(3):457–468. doi: 10.1016/0092-8674(86)90666-5. [DOI] [PubMed] [Google Scholar]
  14. Houliston E., Pickering S. J., Maro B. Redistribution of microtubules and pericentriolar material during the development of polarity in mouse blastomeres. J Cell Biol. 1987 May;104(5):1299–1308. doi: 10.1083/jcb.104.5.1299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Huitorel P., Kirschner M. W. The polarity and stability of microtubule capture by the kinetochore. J Cell Biol. 1988 Jan;106(1):151–159. doi: 10.1083/jcb.106.1.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Karr T. L., Alberts B. M. Organization of the cytoskeleton in early Drosophila embryos. J Cell Biol. 1986 Apr;102(4):1494–1509. doi: 10.1083/jcb.102.4.1494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Karsenti E., Kobayashi S., Mitchison T., Kirschner M. Role of the centrosome in organizing the interphase microtubule array: properties of cytoplasts containing or lacking centrosomes. J Cell Biol. 1984 May;98(5):1763–1776. doi: 10.1083/jcb.98.5.1763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kronebusch P. J., Singer S. J. The microtubule-organizing complex and the Golgi apparatus are co-localized around the entire nuclear envelope of interphase cardiac myocytes. J Cell Sci. 1987 Aug;88(Pt 1):25–34. doi: 10.1242/jcs.88.1.25. [DOI] [PubMed] [Google Scholar]
  19. McIntosh J. R., Euteneuer U. Tubulin hooks as probes for microtubule polarity: an analysis of the method and an evaluation of data on microtubule polarity in the mitotic spindle. J Cell Biol. 1984 Feb;98(2):525–533. doi: 10.1083/jcb.98.2.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. McNiven M. A., Porter K. R. Organization of microtubules in centrosome-free cytoplasm. J Cell Biol. 1988 May;106(5):1593–1605. doi: 10.1083/jcb.106.5.1593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mogensen M. M., Tucker J. B. Evidence for microtubule nucleation at plasma membrane-associated sites in Drosophila. J Cell Sci. 1987 Aug;88(Pt 1):95–107. doi: 10.1242/jcs.88.1.95. [DOI] [PubMed] [Google Scholar]
  22. Perry M. M. Further studies on the development of the eye of Drosophila melanogaster. I. The ommatidia. J Morphol. 1968 Feb;124(2):227–248. doi: 10.1002/jmor.1051240208. [DOI] [PubMed] [Google Scholar]
  23. Schatten H., Schatten G., Mazia D., Balczon R., Simerly C. Behavior of centrosomes during fertilization and cell division in mouse oocytes and in sea urchin eggs. Proc Natl Acad Sci U S A. 1986 Jan;83(1):105–109. doi: 10.1073/pnas.83.1.105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Slepecky N., Chamberlain S. C. Distribution and polarity of actin in inner ear supporting cells. Hear Res. 1983 Jun;10(3):359–370. doi: 10.1016/0378-5955(83)90098-9. [DOI] [PubMed] [Google Scholar]
  25. Stafstrom J. P., Staehelin L. A. Dynamics of the nuclear envelope and of nuclear pore complexes during mitosis in the Drosophila embryo. Eur J Cell Biol. 1984 May;34(1):179–189. [PubMed] [Google Scholar]
  26. Stebbings H., Hunt C. Microtubule polarity in the nutritive tubes of insect ovarioles. Cell Tissue Res. 1983;233(1):133–141. doi: 10.1007/BF00222238. [DOI] [PubMed] [Google Scholar]
  27. Szollosi D., Calarco P., Donahue R. P. Absence of centrioles in the first and second meiotic spindles of mouse oocytes. J Cell Sci. 1972 Sep;11(2):521–541. doi: 10.1242/jcs.11.2.521. [DOI] [PubMed] [Google Scholar]
  28. Tassin A. M., Maro B., Bornens M. Fate of microtubule-organizing centers during myogenesis in vitro. J Cell Biol. 1985 Jan;100(1):35–46. doi: 10.1083/jcb.100.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Tilney L. G., Bryan J., Bush D. J., Fujiwara K., Mooseker M. S., Murphy D. B., Snyder D. H. Microtubules: evidence for 13 protofilaments. J Cell Biol. 1973 Nov;59(2 Pt 1):267–275. doi: 10.1083/jcb.59.2.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tucker J. B. Cytoskeletal coordination and intercellular signalling during metazoan embryogenesis. J Embryol Exp Morphol. 1981 Oct;65:1–25. [PubMed] [Google Scholar]
  31. Tucker J. B. Spatial organization of microtubule-organizing centers and microtubules. J Cell Biol. 1984 Jul;99(1 Pt 2):55s–62s. doi: 10.1083/jcb.99.1.55s. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Walz B. Association between cytoskeletal microtubules and Ca2+-sequestering smooth ER in Semper cells of fly ommatidia. Eur J Cell Biol. 1983 Nov;32(1):92–98. [PubMed] [Google Scholar]
  33. Warn R. M. The cytoskeleton of the early Drosophila embryo. J Cell Sci Suppl. 1986;5:311–328. doi: 10.1242/jcs.1986.supplement_5.20. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES