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. 1983 Oct 1;97(4):1144–1155. doi: 10.1083/jcb.97.4.1144

Intranuclear membranes and the formation of the first meiotic spindle in Xenos peckii (Acroschismus wheeleri) oocytes

PMCID: PMC2112622  PMID: 6619190

Abstract

The ultrastructure of spindle formation during the first meiotic division in oocytes of the Strepsipteran insect Xenos peckii Kirby (Acroschismus wheeleri Pierce) was examined in serial thick (0.25- micron) and thin sections. During late prophase the nuclear envelope became extremely convoluted and fenestrated. At this time vesicular and tubular membrane elements permeated the nucleoplasm and formed a thin fusiform sheath, 5-7 micron in length, around each of the randomly oriented and condensing tetrads. These membrane elements appeared to arise from the nuclear envelope and/or in association with annulate lamellae in the nuclear region. All of the individual tetrads and their associated fusiform sheaths became aligned within the nucleus subsequent to the breakdown of the nuclear envelope. Microtubules (MTs) were found associated with membranes of the meiotic apparatus only after the nuclear envelope had broken down. Kinetochores, with associated MTs, were first recognizable as electron-opaque patches on the chromosomes at this time. The fully formed metaphase arrested Xenos oocyte meiotic apparatus contained an abundance of membranes and had diffuse poles that lacked distinct polar MT organizing centers. From these observations we conclude that the apparent individual chromosomal spindles--seen in the light microscope to form around each Xenos tetrad during "intranuclear prometaphase" (Hughes-Schrader, S., 1924, J. Morphol. 39:157-197)--actually form during late prophase, lack MTs, and are therefore not complete miniature bipolar spindles, as had been commonly assumed. Thus, the unique mode of spindle formation in Xenos oocytes cannot be used to support the hypothesis that chromosomes (kinetochores) induce the polymerization of their associated MTs. Our observation that MTs appeared in association with and parallel to tubular membrane components of the Xenos meiotic apparatus after these membranes became oriented with respect to the tetrads, is consistent with the notion that membranes associated with the spindle determine the orientation of spindle MTs and also play a part in regulating their formation.

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Selected References

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  1. Fuge H. Ultrastructure and function of the spindle apparatus. Microtubules and chromosomes during nuclear division. Protoplasma. 1974;82(4):289–320. doi: 10.1007/BF01275726. [DOI] [PubMed] [Google Scholar]
  2. Fuge H. Ultrastructure of the mitotic spindle. Int Rev Cytol Suppl. 1977;(6):1–58. [PubMed] [Google Scholar]
  3. Gould R. R., Borisy G. G. Quantitative initiation of microtubule assembly by chromosomes from Chinese hamster ovary cells. Exp Cell Res. 1978 May;113(2):369–374. doi: 10.1016/0014-4827(78)90377-4. [DOI] [PubMed] [Google Scholar]
  4. Harris P. The role of membranes in the ogranization of the mitotic apparatus. Exp Cell Res. 1975 Sep;94(2):409–425. doi: 10.1016/0014-4827(75)90507-8. [DOI] [PubMed] [Google Scholar]
  5. Hepler P. K. Membranes in the mitotic apparatus of barley cells. J Cell Biol. 1980 Aug;86(2):490–499. doi: 10.1083/jcb.86.2.490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Kessel R. G. Annulate lamellae. J Ultrastruct Res. 1968;10:1–82. [PubMed] [Google Scholar]
  7. Kiehart D. P. Studies on the in vivo sensitivity of spindle microtubules to calcium ions and evidence for a vesicular calcium-sequestering system. J Cell Biol. 1981 Mar;88(3):604–617. doi: 10.1083/jcb.88.3.604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Kubai D. F. Meiosis in Sciara coprophila: structure of the spindle and chromosome behavior during the first meiotic division. J Cell Biol. 1982 Jun;93(3):655–669. doi: 10.1083/jcb.93.3.655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Luykx P. Cellular mechanisms of chromosome distribution. Int Rev Cytol. 1970;(Suppl):1–173. [PubMed] [Google Scholar]
  10. McIntosh J. R., Cande W. Z., Snyder J. A. Structure and physiology of the mammalian mitotic spindle. Soc Gen Physiol Ser. 1975;30:31–76. [PubMed] [Google Scholar]
  11. Moll E., Paweletz N. Membranes of the mitotic apparatus of mammalian cells. Eur J Cell Biol. 1980 Aug;21(3):280–287. [PubMed] [Google Scholar]
  12. PORTER K. R., MACHADO R. D. Studies on the endoplasmic reticulum. IV. Its form and distribution during mitosis in cells of onion root tip. J Biophys Biochem Cytol. 1960 Feb;7:167–180. doi: 10.1083/jcb.7.1.167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Paweletz N. Membranes in the mitotic apparatus. Cell Biol Int Rep. 1981 Apr;5(4):323–336. doi: 10.1016/0309-1651(81)90001-1. [DOI] [PubMed] [Google Scholar]
  14. Pickett-Heaps J. D., Tippit D. H., Porter K. R. Rethinking mitosis. Cell. 1982 Jul;29(3):729–744. doi: 10.1016/0092-8674(82)90435-4. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Rieder C. L. High-voltage electron microscopy reveals new components in the axonemes and centroplast of the centrohelidian Raphidiophrys amibigua. J Cell Sci. 1979 Dec;40:215–234. doi: 10.1242/jcs.40.1.215. [DOI] [PubMed] [Google Scholar]
  17. Rieder C. L. The formation, structure, and composition of the mammalian kinetochore and kinetochore fiber. Int Rev Cytol. 1982;79:1–58. doi: 10.1016/s0074-7696(08)61672-1. [DOI] [PubMed] [Google Scholar]
  18. Rieder C. L. Thick and thin serial sectioning for the three-dimensional reconstruction of biological ultrastructure. Methods Cell Biol. 1981;22:215–249. doi: 10.1016/s0091-679x(08)61879-8. [DOI] [PubMed] [Google Scholar]
  19. Ring D., Hubble R., Kirschner M. Mitosis in a cell with multiple centrioles. J Cell Biol. 1982 Sep;94(3):549–556. doi: 10.1083/jcb.94.3.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Schatten G., Schatten H., Simerly C. Detection of sequestered calcium during mitosis in mammalian cell cultures and in mitotic apparatus isolated from sea urchin zygotes. Cell Biol Int Rep. 1982 Aug;6(8):717–724. doi: 10.1016/0309-1651(82)90163-1. [DOI] [PubMed] [Google Scholar]
  21. Silver R. B., Cole R. D., Cande W. Z. Isolation of mitotic apparatus containing vesicles with calcium sequestration activity. Cell. 1980 Feb;19(2):505–516. doi: 10.1016/0092-8674(80)90525-5. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. 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]
  25. Wick S. M., Hepler P. K. Localization of Ca++-containing antimonate precipitates during mitosis. J Cell Biol. 1980 Aug;86(2):500–513. doi: 10.1083/jcb.86.2.500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Witt P. L., Ris H., Borisy G. G. Structure of kinetochore fibers: microtubule continuity and inter-microtubule bridges. Chromosoma. 1981;83(4):523–540. doi: 10.1007/BF00328277. [DOI] [PubMed] [Google Scholar]
  27. Wolniak S. M., Hepler P. K., Jackson W. T. Detection of the membrane-calcium distribution during mitosis in Haemanthus endosperm with chlorotetracycline. J Cell Biol. 1980 Oct;87(1):23–32. doi: 10.1083/jcb.87.1.23. [DOI] [PMC free article] [PubMed] [Google Scholar]

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