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. 1992 Dec 1;119(5):1205–1218. doi: 10.1083/jcb.119.5.1205

Maternal effect mutations of the sponge locus affect actin cytoskeletal rearrangements in Drosophila melanogaster embryos

PMCID: PMC2289713  PMID: 1447298

Abstract

In the syncytial blastoderm stage of Drosophila embryogenesis, dome- shaped actin "caps" are observed above the interphase nuclei. During mitosis, this actin rearranges to participate in the formation of pseudocleavage furrows, transient membranous invaginations between dividing nuclei. Embryos laid by homozygous sponge mothers lack these characteristic actin structures, but retain other actin associated structures and processes. Our results indicate that the sponge product is specifically required for the formation of actin caps and metaphase furrows. The specificity of the sponge phenotype permits dissection of both the process of actin cap formation and the functions of actin caps and metaphase furrows. Our data demonstrate that the distribution of actin binding protein 13D2 is unaffected in sponge embryos and suggest that 13D2 is upstream of actin in cortical cap assembly. Although actin caps and metaphase furrows have been implicated in maintaining the fidelity of nuclear division and the positions of nuclei within the cortex, our observations indicate that these structures are dispensible during the early syncytial blastoderm cell cycles. A later requirement for actin metaphase furrows in preventing the nucleation of mitotic spindles between inappropriate centrosomes is observed. Furthermore, the formation of actin caps and metaphase furrows is not a prerequisite for the formation of the hexagonal array of actin instrumental in the conversion of the syncytial embryo into a cellular blastoderm.

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Selected References

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

  1. Edgar B. A., Odell G. M., Schubiger G. Cytoarchitecture and the patterning of fushi tarazu expression in the Drosophila blastoderm. Genes Dev. 1987 Dec;1(10):1226–1237. doi: 10.1101/gad.1.10.1226. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. 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]
  5. Hatanaka K., Okada M. Retarded nuclear migration in Drosophila embryos with aberrant F-actin reorganization caused by maternal mutations and by cytochalasin treatment. Development. 1991 Apr;111(4):909–920. doi: 10.1242/dev.111.4.909. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Kellogg D. R., Field C. M., Alberts B. M. Identification of microtubule-associated proteins in the centrosome, spindle, and kinetochore of the early Drosophila embryo. J Cell Biol. 1989 Dec;109(6 Pt 1):2977–2991. doi: 10.1083/jcb.109.6.2977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Kellogg D. R., Mitchison T. J., Alberts B. M. Behaviour of microtubules and actin filaments in living Drosophila embryos. Development. 1988 Aug;103(4):675–686. doi: 10.1242/dev.103.4.675. [DOI] [PubMed] [Google Scholar]
  9. Lin H. F., Wolfner M. F. The Drosophila maternal-effect gene fs(1)Ya encodes a cell cycle-dependent nuclear envelope component required for embryonic mitosis. Cell. 1991 Jan 11;64(1):49–62. doi: 10.1016/0092-8674(91)90208-g. [DOI] [PubMed] [Google Scholar]
  10. Miller K. G., Alberts B. M. F-actin affinity chromatography: technique for isolating previously unidentified actin-binding proteins. Proc Natl Acad Sci U S A. 1989 Jul;86(13):4808–4812. doi: 10.1073/pnas.86.13.4808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Miller K. G., Field C. M., Alberts B. M. Actin-binding proteins from Drosophila embryos: a complex network of interacting proteins detected by F-actin affinity chromatography. J Cell Biol. 1989 Dec;109(6 Pt 1):2963–2975. doi: 10.1083/jcb.109.6.2963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Miller K. G., Karr T. L., Kellogg D. R., Mohr I. J., Walter M., Alberts B. M. Studies on the cytoplasmic organization of early Drosophila embryos. Cold Spring Harb Symp Quant Biol. 1985;50:79–90. doi: 10.1101/sqb.1985.050.01.012. [DOI] [PubMed] [Google Scholar]
  13. Raff J. W., Glover D. M. Centrosomes, and not nuclei, initiate pole cell formation in Drosophila embryos. Cell. 1989 May 19;57(4):611–619. doi: 10.1016/0092-8674(89)90130-x. [DOI] [PubMed] [Google Scholar]
  14. Rice T. B., Garen A. Localized defects of blastoderm formation in maternal effect mutants of Drosophila. Dev Biol. 1975 Apr;43(2):277–286. doi: 10.1016/0012-1606(75)90027-5. [DOI] [PubMed] [Google Scholar]
  15. Simpson L., Wieschaus E. Zygotic activity of the nullo locus is required to stabilize the actin-myosin network during cellularization in Drosophila. Development. 1990 Nov;110(3):851–863. doi: 10.1242/dev.110.3.851. [DOI] [PubMed] [Google Scholar]
  16. Sullivan W., Minden J. S., Alberts B. M. daughterless-abo-like, a Drosophila maternal-effect mutation that exhibits abnormal centrosome separation during the late blastoderm divisions. Development. 1990 Oct;110(2):311–323. doi: 10.1242/dev.110.2.311. [DOI] [PubMed] [Google Scholar]
  17. Warn R. M., Flegg L., Warn A. An investigation of microtubule organization and functions in living Drosophila embryos by injection of a fluorescently labeled antibody against tyrosinated alpha-tubulin. J Cell Biol. 1987 Oct;105(4):1721–1730. doi: 10.1083/jcb.105.4.1721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Warn R. M., Magrath R. F-actin distribution during the cellularization of the Drosophila embryo visualized with FL-phalloidin. Exp Cell Res. 1983 Jan;143(1):103–114. doi: 10.1016/0014-4827(83)90113-1. [DOI] [PubMed] [Google Scholar]
  19. Warn R. M., Magrath R., Webb S. Distribution of F-actin during cleavage of the Drosophila syncytial blastoderm. J Cell Biol. 1984 Jan;98(1):156–162. doi: 10.1083/jcb.98.1.156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Warn R. M., Smith L., Warn A. Three distinct distributions of F-actin occur during the divisions of polar surface caps to produce pole cells in Drosophila embryos. J Cell Biol. 1985 Apr;100(4):1010–1015. doi: 10.1083/jcb.100.4.1010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Warn R. M., Warn A. Microtubule arrays present during the syncytial and cellular blastoderm stages of the early Drosophila embryo. Exp Cell Res. 1986 Mar;163(1):201–210. doi: 10.1016/0014-4827(86)90573-2. [DOI] [PubMed] [Google Scholar]
  22. Weeds A. Actin-binding proteins--regulators of cell architecture and motility. Nature. 1982 Apr 29;296(5860):811–816. doi: 10.1038/296811a0. [DOI] [PubMed] [Google Scholar]
  23. Whitfield W. G., Millar S. E., Saumweber H., Frasch M., Glover D. M. Cloning of a gene encoding an antigen associated with the centrosome in Drosophila. J Cell Sci. 1988 Apr;89(Pt 4):467–480. doi: 10.1242/jcs.89.4.467. [DOI] [PubMed] [Google Scholar]
  24. Wieschaus E., Sweeton D. Requirements for X-linked zygotic gene activity during cellularization of early Drosophila embryos. Development. 1988 Nov;104(3):483–493. doi: 10.1242/dev.104.3.483. [DOI] [PubMed] [Google Scholar]
  25. Yasuda G. K., Baker J., Schubiger G. Independent roles of centrosomes and DNA in organizing the Drosophila cytoskeleton. Development. 1991 Feb;111(2):379–391. doi: 10.1242/dev.111.2.379. [DOI] [PubMed] [Google Scholar]

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