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. 1996 Apr 1;133(1):61–74. doi: 10.1083/jcb.133.1.61

Formation of actin filament bundles in the ring canals of developing Drosophila follicles

PMCID: PMC2120773  PMID: 8601614

Abstract

Growing the intracellular bridges that connect nurse cells with each o ther and to the developing oocyte is vital for egg development. These ring canals increase from 0.5 microns in diameter at stage 2 to 10 microns in diameter at stage 11. Thin sections cut horizontally as you would cut a bagel, show that there is a layer of circumferentially oriented actin filaments attached to the plasma membrane at the periphery of each canal. By decoration with subfragment 1 of myosin we find actin filaments of mixed polarities in the ring such as found in the "contractile ring" formed during cytokinesis. In vertical sections through the canal the actin filaments appear as dense dots. At stage 2 there are 82 actin filaments in the ring, by stage 6 there are 717 and by stage 10 there are 726. Taking into account the diameter, this indicates that there is 170 microns of actin filaments/canal at stage 2 (pi x 0.5 microns x 82), 14,000 microns at stage 9 and approximately 23,000 microns at stage 11 or one inch of actin filament! The density of actin filaments remains unchanged throughout development. What is particularly striking is that by stages 4-5, the ring of actin filaments has achieved its maximum thickness, even though the diameter has not yet increased significantly. Thereafter, the diameter increases. Throughout development, stages 2-11, the canal length also increases. Although the density (number of actin filaments/micron2) through a canal remains constant from stage 5 on, the actin filaments appear as a net of interconnected bundles. Further information on this net of bundles comes from studying mutant animals that lack kelch, a protein located in the ring canal that has homology to the actin binding protein, scruin. In this mutant, the actin filaments form normally but individual bundles that comprise the fibers of the net are not bound tightly together. Some bundles enter into the ring canal lumen but do not completely occlude the lumen. all these observations lay the groundwork for our understanding of how a noncontractile ring increases in thickness, diameter, and length during development.

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Selected References

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  1. Bardwell V. J., Treisman R. The POZ domain: a conserved protein-protein interaction motif. Genes Dev. 1994 Jul 15;8(14):1664–1677. doi: 10.1101/gad.8.14.1664. [DOI] [PubMed] [Google Scholar]
  2. Bullitt E. S., DeRosier D. J., Coluccio L. M., Tilney L. G. Three-dimensional reconstruction of an actin bundle. J Cell Biol. 1988 Aug;107(2):597–611. doi: 10.1083/jcb.107.2.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cooley L., Theurkauf W. E. Cytoskeletal functions during Drosophila oogenesis. Science. 1994 Oct 28;266(5185):590–596. doi: 10.1126/science.7939713. [DOI] [PubMed] [Google Scholar]
  4. Cooley L., Verheyen E., Ayers K. chickadee encodes a profilin required for intercellular cytoplasm transport during Drosophila oogenesis. Cell. 1992 Apr 3;69(1):173–184. doi: 10.1016/0092-8674(92)90128-y. [DOI] [PubMed] [Google Scholar]
  5. DeRosier D. J., Tilney L. G., Bonder E. M., Frankl P. A change in twist of actin provides the force for the extension of the acrosomal process in Limulus sperm: the false-discharge reaction. J Cell Biol. 1982 May;93(2):324–337. doi: 10.1083/jcb.93.2.324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. DiBello P. R., Withers D. A., Bayer C. A., Fristrom J. W., Guild G. M. The Drosophila Broad-Complex encodes a family of related proteins containing zinc fingers. Genetics. 1991 Oct;129(2):385–397. doi: 10.1093/genetics/129.2.385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Harrison S. D., Travers A. A. The tramtrack gene encodes a Drosophila finger protein that interacts with the ftz transcriptional regulatory region and shows a novel embryonic expression pattern. EMBO J. 1990 Jan;9(1):207–216. doi: 10.1002/j.1460-2075.1990.tb08097.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Lin H., Yue L., Spradling A. C. The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development. 1994 Apr;120(4):947–956. doi: 10.1242/dev.120.4.947. [DOI] [PubMed] [Google Scholar]
  9. Mahowald A. P. The formation of ring canals by cell furrows in Drosophila. Z Zellforsch Mikrosk Anat. 1971;118(2):162–167. doi: 10.1007/BF00341561. [DOI] [PubMed] [Google Scholar]
  10. Owen C., DeRosier D. A 13-A map of the actin-scruin filament from the limulus acrosomal process. J Cell Biol. 1993 Oct;123(2):337–344. doi: 10.1083/jcb.123.2.337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Peifer M., Orsulic S., Sweeton D., Wieschaus E. A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis. Development. 1993 Aug;118(4):1191–1207. doi: 10.1242/dev.118.4.1191. [DOI] [PubMed] [Google Scholar]
  12. Riparbelli M. G., Callaini G. Cytoskeleton of the Drosophila egg chamber: new observations on microfilament distribution during oocyte growth. Cell Motil Cytoskeleton. 1995;31(4):298–306. doi: 10.1002/cm.970310406. [DOI] [PubMed] [Google Scholar]
  13. Robinson D. N., Cant K., Cooley L. Morphogenesis of Drosophila ovarian ring canals. Development. 1994 Jul;120(7):2015–2025. doi: 10.1242/dev.120.7.2015. [DOI] [PubMed] [Google Scholar]
  14. Schmid M. F., Agris J. M., Jakana J., Matsudaira P., Chiu W. Three-dimensional structure of a single filament in the Limulus acrosomal bundle: scruin binds to homologous helix-loop-beta motifs in actin. J Cell Biol. 1994 Feb;124(3):341–350. doi: 10.1083/jcb.124.3.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Schmid M. F., Matsudaira P., Jeng T. W., Jakana J., Towns-Andrews E., Bordas J., Chiu W. Crystallographic analysis of acrosomal bundle from Limulus sperm. J Mol Biol. 1991 Sep 20;221(2):711–725. doi: 10.1016/0022-2836(91)80082-6. [DOI] [PubMed] [Google Scholar]
  16. Singleton K., Woodruff R. I. The osmolarity of adult Drosophila hemolymph and its effect on oocyte-nurse cell electrical polarity. Dev Biol. 1994 Jan;161(1):154–167. doi: 10.1006/dbio.1994.1017. [DOI] [PubMed] [Google Scholar]
  17. Tilney L. G. Actin filaments in the acrosomal reaction of Limulus sperm. Motion generated by alterations in the packing of the filaments. J Cell Biol. 1975 Feb;64(2):289–310. doi: 10.1083/jcb.64.2.289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Tilney L. G., Bonder E. M., DeRosier D. J. Actin filaments elongate from their membrane-associated ends. J Cell Biol. 1981 Aug;90(2):485–494. doi: 10.1083/jcb.90.2.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Tilney L. G., Tilney M. S., DeRosier D. J. Actin filaments, stereocilia, and hair cells: how cells count and measure. Annu Rev Cell Biol. 1992;8:257–274. doi: 10.1146/annurev.cb.08.110192.001353. [DOI] [PubMed] [Google Scholar]
  20. Tilney L. G., Tilney M. S. Methods to visualize actin polymerization associated with bacterial invasion. Methods Enzymol. 1994;236:476–481. doi: 10.1016/0076-6879(94)36036-7. [DOI] [PubMed] [Google Scholar]
  21. Tilney L. G., Tilney M. S. The wily ways of a parasite: induction of actin assembly by Listeria. Trends Microbiol. 1993 Apr;1(1):25–31. doi: 10.1016/0966-842x(93)90021-i. [DOI] [PubMed] [Google Scholar]
  22. Warn R. M., Gutzeit H. O., Smith L., Warn A. F-actin rings are associated with the ring canals of the Drosophila egg chamber. Exp Cell Res. 1985 Apr;157(2):355–363. doi: 10.1016/0014-4827(85)90120-x. [DOI] [PubMed] [Google Scholar]
  23. Way M., Sanders M., Garcia C., Sakai J., Matsudaira P. Sequence and domain organization of scruin, an actin-cross-linking protein in the acrosomal process of Limulus sperm. J Cell Biol. 1995 Jan;128(1-2):51–60. doi: 10.1083/jcb.128.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Xue F., Cooley L. kelch encodes a component of intercellular bridges in Drosophila egg chambers. Cell. 1993 Mar 12;72(5):681–693. doi: 10.1016/0092-8674(93)90397-9. [DOI] [PubMed] [Google Scholar]
  25. Yue L., Spradling A. C. hu-li tai shao, a gene required for ring canal formation during Drosophila oogenesis, encodes a homolog of adducin. Genes Dev. 1992 Dec;6(12B):2443–2454. doi: 10.1101/gad.6.12b.2443. [DOI] [PubMed] [Google Scholar]
  26. Zollman S., Godt D., Privé G. G., Couderc J. L., Laski F. A. The BTB domain, found primarily in zinc finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10717–10721. doi: 10.1073/pnas.91.22.10717. [DOI] [PMC free article] [PubMed] [Google Scholar]

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