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. 1990 Jun 1;110(6):1993–1998. doi: 10.1083/jcb.110.6.1993

Identification of actin filaments in the rhabdomeral microvilli of Drosophila photoreceptors

PMCID: PMC2116135  PMID: 2112548

Abstract

The phototransductive microvilli of arthropod photoreceptors each contain an axial cytoskeleton. The present study shows that actin filaments are a component of this cytoskeleton in Drosophila. Firstly, actin was detected in the rhabdomeral microvilli and in the subrhabdomeral cytoplasm by immunogold labeling with antiactin. Secondly, the rhabdomeres were labeled with phalloidin, indicating the presence of filamentous actin. Finally, the actin filaments were decorated with myosin subfragment-1. The characteristic arrowhead complex formed by subfragment-1 decoration points towards the base of the microvilli, so that the fast growing end of each filament is at the distal end of the microvillus, where it is embedded in a detergent- resistant cap. Each microvillus contains more than one actin filament. Decorated filaments extend the entire length of each microvillus and project into the subrhabdomeral cytoplasm. This organization is comparable to that of the actin filaments in intestinal brush border microvilli. Similar observations were made with the photoreceptor microvilli of the crayfish, Procambarus. Our results provide an indication as to how any myosin that is associated with the rhabdomeres might function.

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Selected References

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

  1. Adams R. J., Pollard T. D. Binding of myosin I to membrane lipids. Nature. 1989 Aug 17;340(6234):565–568. doi: 10.1038/340565a0. [DOI] [PubMed] [Google Scholar]
  2. Adams R. J., Pollard T. D. Propulsion of organelles isolated from Acanthamoeba along actin filaments by myosin-I. Nature. 1986 Aug 21;322(6081):754–756. doi: 10.1038/322754a0. [DOI] [PubMed] [Google Scholar]
  3. Arikawa K., Williams D. S. Organization of actin filaments and immunocolocalization of alpha-actinin in the connecting cilium of rat photoreceptors. J Comp Neurol. 1989 Oct 22;288(4):640–646. doi: 10.1002/cne.902880410. [DOI] [PubMed] [Google Scholar]
  4. Begg D. A., Rodewald R., Rebhun L. I. The visualization of actin filament polarity in thin sections. Evidence for the uniform polarity of membrane-associated filaments. J Cell Biol. 1978 Dec;79(3):846–852. doi: 10.1083/jcb.79.3.846. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blest A. D., Stowe S., Eddey W. A labile, Ca2+-dependent cytoskeleton in rhabdomeral microvilli of blowflies. Cell Tissue Res. 1982;223(3):553–573. doi: 10.1007/BF00218476. [DOI] [PubMed] [Google Scholar]
  6. Blest A. D., Stowe S., Eddey W., Williams D. S. The local deletion of a microvillar cytoskeleton from photoreceptors of tipulid flies during membrane turnover. Proc R Soc Lond B Biol Sci. 1982 Jul 22;215(1201):469–479. doi: 10.1098/rspb.1982.0054. [DOI] [PubMed] [Google Scholar]
  7. Drenckhahn D., Dermietzel R. Organization of the actin filament cytoskeleton in the intestinal brush border: a quantitative and qualitative immunoelectron microscope study. J Cell Biol. 1988 Sep;107(3):1037–1048. doi: 10.1083/jcb.107.3.1037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Forer A., Behnke O. An actin-like component in sperm tails of a crane fly (Nephrotoma suturalis Loew). J Cell Sci. 1972 Sep;11(2):491–519. doi: 10.1242/jcs.11.2.491. [DOI] [PubMed] [Google Scholar]
  9. Matsumoto-Suzuki E., Hirosawa K., Hotta Y. Structure of the subrhabdomeric cisternae in the photoreceptor cells of Drosophila melanogaster. J Neurocytol. 1989 Feb;18(1):87–93. doi: 10.1007/BF01188427. [DOI] [PubMed] [Google Scholar]
  10. Miyata H., Bowers B., Korn E. D. Plasma membrane association of Acanthamoeba myosin I. J Cell Biol. 1989 Oct;109(4 Pt 1):1519–1528. doi: 10.1083/jcb.109.4.1519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Montell C., Rubin G. M. The Drosophila ninaC locus encodes two photoreceptor cell specific proteins with domains homologous to protein kinases and the myosin heavy chain head. Cell. 1988 Mar 11;52(5):757–772. doi: 10.1016/0092-8674(88)90413-8. [DOI] [PubMed] [Google Scholar]
  12. Mooseker M. S., Coleman T. R. The 110-kD protein-calmodulin complex of the intestinal microvillus (brush border myosin I) is a mechanoenzyme. J Cell Biol. 1989 Jun;108(6):2395–2400. doi: 10.1083/jcb.108.6.2395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Mooseker M. S. Organization, chemistry, and assembly of the cytoskeletal apparatus of the intestinal brush border. Annu Rev Cell Biol. 1985;1:209–241. doi: 10.1146/annurev.cb.01.110185.001233. [DOI] [PubMed] [Google Scholar]
  14. Mooseker M. S., Tilney L. G. Organization of an actin filament-membrane complex. Filament polarity and membrane attachment in the microvilli of intestinal epithelial cells. J Cell Biol. 1975 Dec;67(3):725–743. doi: 10.1083/jcb.67.3.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mukherjee T. M., Staehelin L. A. The fine-structural organization of the brush border of intestinal epithelial cells. J Cell Sci. 1971 May;8(3):573–599. doi: 10.1242/jcs.8.3.573. [DOI] [PubMed] [Google Scholar]
  16. Saibil H. R. An ordered membrane-cytoskeleton network in squid photoreceptor microvilli. J Mol Biol. 1982 Jul 5;158(3):435–456. doi: 10.1016/0022-2836(82)90208-x. [DOI] [PubMed] [Google Scholar]
  17. Saibil H., Hewat E. Ordered transmembrane and extracellular structure in squid photoreceptor microvilli. J Cell Biol. 1987 Jul;105(1):19–28. doi: 10.1083/jcb.105.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Tilney L. G., Mooseker M. Actin in the brush-border of epithelial cells of the chicken intestine. Proc Natl Acad Sci U S A. 1971 Oct;68(10):2611–2615. doi: 10.1073/pnas.68.10.2611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Williams D. S., Blest A. D. Extracellular shedding of photoreceptor membrane in the open rhabdom of a tipulid fly. Cell Tissue Res. 1980;205(3):423–438. doi: 10.1007/BF00232283. [DOI] [PubMed] [Google Scholar]
  20. de Couet H. G., Stowe S., Blest A. D. Membrane-associated actin in the rhabdomeral microvilli of crayfish photoreceptors. J Cell Biol. 1984 Mar;98(3):834–846. doi: 10.1083/jcb.98.3.834. [DOI] [PMC free article] [PubMed] [Google Scholar]

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