Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1982 May 1;93(2):365–373. doi: 10.1083/jcb.93.2.365

Meiosis in Drosophila melanogaster. II. The prometaphase-I kinetochore microtubule bundle and kinetochore orientation in males

PMCID: PMC2112869  PMID: 6807996

Abstract

Fourteen prometaphase kinetochore microtubule bundles have been examined in electron micrographs of serial sections. The majority (54%) of the microtubules extended from the polar region towards the kinetochore but do not end in the kinetochore proper. Rather, they stop short of the kinetochore (21%), graze the kinetochore (19%), or pass through the kinetochore (9%), displaying a free end distal to the pole. Other microtubules that make up the kinetochore bundle include: kinetochore-to-pole microtubules (24%), chromosome-to-pole microtubules (5%), pieces with two free ends (14%), and those microtubules with one end in the kinetochore and a free end distal to the kinetochore (9%). We conclude that the majority of the microtubules in the kinetochore bundle are most likely of polar origin rather than having been nucleated at the kinetochore. Prometaphase-I kinetochores can display any one of four patterns of microtubule connections with the poles, but the pattern of microtubule connections is not always correlated with kinetochore position. For instance, a kinetochore directly facing one pole may have microtubule connections with both poles while a kinetochore positioned 90 degrees to the spindle axis may have microtubules running towards one pole only.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

Selected References

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

  1. BAUER H., DIETZ R., ROEBBELEN C. [Spermatocyte division of Tipulae. III. Movement behavior of chromosomes in translocation heterozygotes of Tipula oleracea]. Chromosoma. 1961;12:116–189. doi: 10.1007/BF00328918. [DOI] [PubMed] [Google Scholar]
  2. Begg D. A., Ellis G. W. Micromanipulation studies of chromosome movement. I. Chromosome-spindle attachment and the mechanical properties of chromosomal spindle fibers. J Cell Biol. 1979 Aug;82(2):528–541. doi: 10.1083/jcb.82.2.528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dietz R. Bau ud Fnktion des Spindelapparats. Naturwissenschaften. 1969 May;56(5):237–248. doi: 10.1007/BF00633917. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Fuge H. Ultrastructure of the mitotic spindle. Int Rev Cytol Suppl. 1977;(6):1–58. [PubMed] [Google Scholar]
  6. Goldstein L. S. Kinetochore structure and its role in chromosome orientation during the first meiotic division in male D. melanogaster. Cell. 1981 Sep;25(3):591–602. doi: 10.1016/0092-8674(81)90167-7. [DOI] [PubMed] [Google Scholar]
  7. Henderson S. A., Nicklas R. B., Koch C. A. Temperature-induced orientation instability during meiosis: an experimental analysis. J Cell Sci. 1970 Mar;6(2):323–350. doi: 10.1242/jcs.6.2.323. [DOI] [PubMed] [Google Scholar]
  8. ITO S. The lamellar systems of cytoplasmic membranes in dividing spermatogenic cells by Drosophila virilis. J Biophys Biochem Cytol. 1960 Jun;7:433–442. doi: 10.1083/jcb.7.3.433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kubai D. F. Unorthodox mitosis in Trichonympha agilis: kinetochore differentiation and chromosome movement. J Cell Sci. 1973 Sep;13(2):511–552. doi: 10.1242/jcs.13.2.511. [DOI] [PubMed] [Google Scholar]
  10. LUFT J. H. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol. 1961 Feb;9:409–414. doi: 10.1083/jcb.9.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. LaFountain J. R., Jr, Davidson L. A. An analysis of spindle ultrastructure during prometaphase and metaphase of micronuclear division in Tetrahymena. Chromosoma. 1979;75(3):293–308. doi: 10.1007/BF00293473. [DOI] [PubMed] [Google Scholar]
  12. Lin H. P., Ault J. G., Church K. Meiosis in Drosophila melanogaster. I. Chromosome identification and kinetochore microtubule numbers during the first and second meiotic divisions in males. Chromosoma. 1981;83(4):507–521. doi: 10.1007/BF00328276. [DOI] [PubMed] [Google Scholar]
  13. Luykx P. Kinetochore-to-pole connections during prometaphase of the meiotic divisions in Urechis eggs. Exp Cell Res. 1965 Sep;39(2):658–668. doi: 10.1016/0014-4827(65)90069-8. [DOI] [PubMed] [Google Scholar]
  14. McGill M., Brinkley B. R. Human chromosomes and centrioles as nucleating sites for the in vitro assembly of microtubules from bovine brain tubulin. J Cell Biol. 1975 Oct;67(1):189–199. doi: 10.1083/jcb.67.1.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Moens P. B., Moens T. Computer measurements and graphics of three-dimensional cellular ultrastructure. J Ultrastruct Res. 1981 May;75(2):131–141. doi: 10.1016/s0022-5320(81)80129-3. [DOI] [PubMed] [Google Scholar]
  16. Nicklas R. B., Brinkley B. R., Pepper D. A., Kubai D. F., Rickards G. K. Electron microscopy of spermatocytes previously studied in life: methods and some observations on micromanipulated chromosomes. J Cell Sci. 1979 Feb;35:87–104. doi: 10.1242/jcs.35.1.87. [DOI] [PubMed] [Google Scholar]
  17. Nicklas R. B. Chromosome micromanipulation. II. Induced reorientation and the experimental control of segregation in meiosis. Chromosoma. 1967;21(1):17–50. doi: 10.1007/BF00330545. [DOI] [PubMed] [Google Scholar]
  18. Nicklas R. B., Koch C. A. Chromosome micromanipulation. 3. Spindle fiber tension and the reorientation of mal-oriented chromosomes. J Cell Biol. 1969 Oct;43(1):40–50. doi: 10.1083/jcb.43.1.40. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nicklas R. B. Mitosis. Adv Cell Biol. 1971;2:225–297. doi: 10.1007/978-1-4615-9588-5_5. [DOI] [PubMed] [Google Scholar]
  20. Nicklas R. B., Staehly C. A. Chromosome micromanipulation. I. The mechanics of chromosome attachment to the spindle. Chromosoma. 1967;21(1):1–16. doi: 10.1007/BF00330544. [DOI] [PubMed] [Google Scholar]
  21. Rieder C. L., Borisy G. G. The attachment of kinetochores to the pro-metaphase spindle in PtK1 cells. Recovery from low temperature treatment. Chromosoma. 1981;82(5):693–716. doi: 10.1007/BF00285776. [DOI] [PubMed] [Google Scholar]
  22. Roos U. P. Light and electron microscopy of rat kangaroo cells in mitosis. III. Patterns of chromosome behavior during prometaphase. Chromosoma. 1976 Mar 10;54(4):363–385. doi: 10.1007/BF00292816. [DOI] [PubMed] [Google Scholar]
  23. Snyder J. A., McIntosh J. R. Initiation and growth of microtubules from mitotic centers in lysed mammalian cells. J Cell Biol. 1975 Dec;67(3):744–760. doi: 10.1083/jcb.67.3.744. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Telzer B. R., Haimo L. T. Decoration of spindle microtubules with Dynein: evidence for uniform polarity. J Cell Biol. 1981 May;89(2):373–378. doi: 10.1083/jcb.89.2.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Telzer B. R., Moses M. J., Rosenbaum J. L. Assembly of microtubules onto kinetochores of isolated mitotic chromosomes of HeLa cells. Proc Natl Acad Sci U S A. 1975 Oct;72(10):4023–4027. doi: 10.1073/pnas.72.10.4023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tippit D. H., Pickett-Heaps J. D., Leslie R. Cell division in two large pennate diatoms Hantzschia and Nitzschia III. A new proposal for kinetochore function during prometaphase. J Cell Biol. 1980 Aug;86(2):402–416. doi: 10.1083/jcb.86.2.402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Witt P. L., Ris H., Borisy G. G. Origin of kinetochore microtubules in Chinese hamster ovary cells. Chromosoma. 1980;81(3):483–505. doi: 10.1007/BF00368158. [DOI] [PubMed] [Google Scholar]

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

RESOURCES