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. 1984 Feb 1;98(2):699–708. doi: 10.1083/jcb.98.2.699

Are annulate lamellae in the Drosophila embryo the result of overproduction of nuclear pore components?

PMCID: PMC2113103  PMID: 6420420

Abstract

Annulate lamellae are cytoplasmic organelles composed of stacked sheets of membrane containing pores that are structurally indistinguishable from nuclear pores. The functions of annulate lamellae are not well understood. Although they may be found in virtually any eucaryotic cell, they occur most commonly in transformed and embryonic tissues. In Drosophila, annulate lamellae are found in the syncytial blastoderm embryo as it is cleaved to form the cellular blastoderm. The cytological events of the cellularization process are well documented, and may be used as temporal landmarks when studying changes in annulate lamellae. By using morphometric techniques to analyze electron micrographs of embryos, we are able to calculate the number of pores per nucleus in nuclear envelopes and annulate lamellae during progressive stages of cellularization. We find that annulate lamellae pores remain at a low level while nuclear envelopes are expanding and acquiring pores in early interphase. Once nuclear envelopes are saturated with pores, however, the number of annulate lamellae pores increases more than 10-fold in 9 min. Over the next 30 min it gradually declines to the initial low level. On the basis of these results, we propose (a) that pore synthesis and assembly continues after nuclear envelopes have been saturated with pores; (b) that these supernumerary pores accumulate transiently in cytoplasmic annulate lamellae; and (c) that because these pores are not needed by the embryo they are subsequently degraded.

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Selected References

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  1. AFZELIUS B. A. The ultrastructure of the nuclear membrane of the sea urchin oocyte as studied with the electron microscope. Exp Cell Res. 1955 Feb;8(1):147–158. doi: 10.1016/0014-4827(55)90051-3. [DOI] [PubMed] [Google Scholar]
  2. Blobel G. Intracellular protein topogenesis. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1496–1500. doi: 10.1073/pnas.77.3.1496. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Fisher P. A., Berrios M., Blobel G. Isolation and characterization of a proteinaceous subnuclear fraction composed of nuclear matrix, peripheral lamina, and nuclear pore complexes from embryos of Drosophila melanogaster. J Cell Biol. 1982 Mar;92(3):674–686. doi: 10.1083/jcb.92.3.674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Foe V. E., Alberts B. M. Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci. 1983 May;61:31–70. doi: 10.1242/jcs.61.1.31. [DOI] [PubMed] [Google Scholar]
  5. Fullilove S. L., Jacobson A. G. Nuclear elongation and cytokinesis in Drosophila montana. Dev Biol. 1971 Dec;26(4):560–577. doi: 10.1016/0012-1606(71)90141-2. [DOI] [PubMed] [Google Scholar]
  6. Gall J. G. Octagonal nuclear pores. J Cell Biol. 1967 Feb;32(2):391–399. doi: 10.1083/jcb.32.2.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gerace L., Ottaviano Y., Kondor-Koch C. Identification of a major polypeptide of the nuclear pore complex. J Cell Biol. 1982 Dec;95(3):826–837. doi: 10.1083/jcb.95.3.826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hertig A. T. The primary human oocyte: some observations on the fine structure of Balbiani's vitelline body and the origin of the annulate lamellae. Am J Anat. 1968 Jan;122(1):107–137. doi: 10.1002/aja.1001220107. [DOI] [PubMed] [Google Scholar]
  9. Illmensee K., Mahowald A. P., Loomis M. R. The ontogeny of germ plasm during oogenesis in Drosophila. Dev Biol. 1976 Mar;49(1):40–65. doi: 10.1016/0012-1606(76)90257-8. [DOI] [PubMed] [Google Scholar]
  10. KESSEL R. G. ELECTRON MICROSCOPE STUDIES ON THE ORIGIN OF ANNULATE LAMELLAE IN OOCYTES OF NECTURUS. J Cell Biol. 1963 Nov;19:391–414. doi: 10.1083/jcb.19.2.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kessel R. G. Annulate lamellae. J Ultrastruct Res. 1968;10:1–82. [PubMed] [Google Scholar]
  12. Kessel R. G., Beams H. W. Annulate lamellae and "yolk nuclei" in oocytes of the dragonfly, Libellula pulchella. J Cell Biol. 1969 Jul;42(1):185–201. doi: 10.1083/jcb.42.1.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kessel R. G. Origin, differentiation, distribution and possible functional role of annulate lamellae during spermatogenesis in Drosophila melanogaster. J Ultrastruct Res. 1981 Apr;75(1):72–96. doi: 10.1016/s0022-5320(81)80101-3. [DOI] [PubMed] [Google Scholar]
  14. Kessel R. G. The structure and function of annulate lamellae: porous cytoplasmic and intranuclear membranes. Int Rev Cytol. 1983;82:181–303. doi: 10.1016/s0074-7696(08)60826-8. [DOI] [PubMed] [Google Scholar]
  15. Krohne G., Franke W. W., Scheer U. The major polypeptides of the nuclear pore complex. Exp Cell Res. 1978 Oct 1;116(1):85–102. doi: 10.1016/0014-4827(78)90067-8. [DOI] [PubMed] [Google Scholar]
  16. MAHOWALD A. P. ELECTRON MICROSCOPY OF THE FORMATION OF THE CELLULAR BLASTODERM IN DROSOPHILA MELANOGASTER. Exp Cell Res. 1963 Dec;32:457–468. doi: 10.1016/0014-4827(63)90186-1. [DOI] [PubMed] [Google Scholar]
  17. MAHOWALD A. P. ULTRASTRUCTURAL DIFFERENTIATIONS DURING FORMATION OF THE BLASTODERM IN THE DROSOPHILA MELANOGASTER EMBRYO. Dev Biol. 1963 Oct;8:186–204. doi: 10.1016/0012-1606(63)90041-1. [DOI] [PubMed] [Google Scholar]
  18. Maul G. G. On the relationship between the Golgi apparatus and annulate lamellae. J Ultrastruct Res. 1970 Feb;30(3):368–384. doi: 10.1016/s0022-5320(70)80069-7. [DOI] [PubMed] [Google Scholar]
  19. Maul G. G. The nuclear and the cytoplasmic pore complex: structure, dynamics, distribution, and evolution. Int Rev Cytol Suppl. 1977;(6):75–186. [PubMed] [Google Scholar]
  20. OKADA E., WADDINGTON C. H. The submicroscopic structure of the Drosophila egg. J Embryol Exp Morphol. 1959 Dec;7:583–597. [PubMed] [Google Scholar]
  21. Rickoll W. L. Cytoplasmic continuity between embryonic cells and the primitive yolk sac during early gastrulation in Drosophila melanogaster. Dev Biol. 1976 Mar;49(1):304–310. doi: 10.1016/0012-1606(76)90278-5. [DOI] [PubMed] [Google Scholar]
  22. Sabatini D. D., Kreibich G., Morimoto T., Adesnik M. Mechanisms for the incorporation of proteins in membranes and organelles. J Cell Biol. 1982 Jan;92(1):1–22. doi: 10.1083/jcb.92.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Scheer U. Ultrastructure of the nuclear envelope of amphibian oocytes. IV. Chemical nature of the nuclear pore complex material. Z Zellforsch Mikrosk Anat. 1972;127(1):127–148. doi: 10.1007/BF00582762. [DOI] [PubMed] [Google Scholar]
  24. Spindler M., Hemleben C. Formation and possible function of annulate lamellae in a planktic foraminifer. J Ultrastruct Res. 1982 Dec;81(3):341–350. doi: 10.1016/s0022-5320(82)90062-4. [DOI] [PubMed] [Google Scholar]
  25. Stick R., Krohne G. Immunological localization of the major architectural protein associated with the nuclear envelope of the Xenopus laevis oocyte. Exp Cell Res. 1982 Apr;138(2):319–313. doi: 10.1016/0014-4827(82)90181-1. [DOI] [PubMed] [Google Scholar]
  26. Turner F. R., Mahowald A. P. Scanning electron microscopy of Drosophila embryogenesis. 1. The structure of the egg envelopes and the formation of the cellular blastoderm. Dev Biol. 1976 May;50(1):95–108. doi: 10.1016/0012-1606(76)90070-1. [DOI] [PubMed] [Google Scholar]
  27. Unwin P. N., Milligan R. A. A large particle associated with the perimeter of the nuclear pore complex. J Cell Biol. 1982 Apr;93(1):63–75. doi: 10.1083/jcb.93.1.63. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Warn R. M., Magrath R. Observations by a novel method of surface changes during the syncytial blastoderm stage of the Drosophila embryo. Dev Biol. 1982 Feb;89(2):540–548. doi: 10.1016/0012-1606(82)90344-x. [DOI] [PubMed] [Google Scholar]
  29. Wischnitzer S. The annulate lamellae. Int Rev Cytol. 1970;27:65–100. doi: 10.1016/s0074-7696(08)61246-2. [DOI] [PubMed] [Google Scholar]
  30. Zalokar M., Erk I. Phase-partition fixation and staining of Drosophila eggs. Stain Technol. 1977 Mar;52(2):89–95. doi: 10.3109/10520297709116753. [DOI] [PubMed] [Google Scholar]

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