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. 1985 Aug 1;101(2):590–596. doi: 10.1083/jcb.101.2.590

Increase in actin contents and elongation of apical projections in retinal pigmented epithelial cells during development of the chicken eye

PMCID: PMC2113652  PMID: 3894378

Abstract

The structural and biochemical changes of cytoskeletal components of retinal pigmented epithelial cells were studied during the development of chicken eyes. When the cytoskeletal components of the pigmented epithelial cells from various stages of development were examined by SDS PAGE, actin contents in the cells markedly increased between the 15- d-old and hatching stages. Immunofluorescence microscopy showed that chicken pigmented epithelial cells have two types of actin bundles. One is the circumferential bundle associated with the zonula adherens region as previously reported (Owaribe, K., and H. Masuda, 1982, J. Cell Biol., 95:310-315). The other is the paracrystalline bundle forming the core of the apical projections. The increase in actin contents after the 15-d-old stage is accompanied by the formation and elongation of core filaments of apical projections in the cells. During this period the apical projections extend into extracellular space among outer and inner segments of photoreceptor cells. Accompanying this change is an elongation of the paracrystalline bundles of actin filaments in the core of the projection. By electron microscopy, the bundles decorated with muscle heavy meromyosin showed unidirectional polarity, and had transverse striations with approximately 12-nm intervals, as determined by optical diffraction of electron micrographs. Since the shape of these bundles was not altered in the presence or absence of Ca2+, they seemed not to have villin-like proteins. Unlike the circumferential bundles, the paracrystalline bundles did not contract when exposed to Mg-ATP. These observations indicate that the paracrystalline bundles are structurally and functionally different from the circumferential actin bundles.

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Selected References

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  1. Bretscher A., Weber K. Localization of actin and microfilament-associated proteins in the microvilli and terminal web of the intestinal brush border by immunofluorescence microscopy. J Cell Biol. 1978 Dec;79(3):839–845. doi: 10.1083/jcb.79.3.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bretscher A., Weber K. Villin is a major protein of the microvillus cytoskeleton which binds both G and F actin in a calcium-dependent manner. Cell. 1980 Jul;20(3):839–847. doi: 10.1016/0092-8674(80)90330-x. [DOI] [PubMed] [Google Scholar]
  3. Bryan J., Kane R. E. Separation and interaction of the major components of sea urchin actin gel. J Mol Biol. 1978 Oct 25;125(2):207–224. doi: 10.1016/0022-2836(78)90345-5. [DOI] [PubMed] [Google Scholar]
  4. Burnside B., Adler R., O'Connor P. Retinomotor pigment migration in the teleost retinal pigment epithelium. I. Roles for actin and microtubules in pigment granule transport and cone movement. Invest Ophthalmol Vis Sci. 1983 Jan;24(1):1–15. [PubMed] [Google Scholar]
  5. Burnside B., Laties A. M. Actin filaments in apical projections of the primate pigmented epithelial cell. Invest Ophthalmol. 1976 Jul;15(7):570–575. [PubMed] [Google Scholar]
  6. Clarke M., Spudich J. A. Nonmuscle contractile proteins: the role of actin and myosin in cell motility and shape determination. Annu Rev Biochem. 1977;46:797–822. doi: 10.1146/annurev.bi.46.070177.004053. [DOI] [PubMed] [Google Scholar]
  7. Crawford B., Cloney R. A., Cahn R. D. Cloned pigmented retinal cells; the affects of cytochalasin B on ultrastructure and behavior. Z Zellforsch Mikrosk Anat. 1972;130(2):135–151. doi: 10.1007/BF00306953. [DOI] [PubMed] [Google Scholar]
  8. DeRosier D., Mandelkow E., Silliman A. Structure of actin-containing filaments from two types of non-muscle cells. J Mol Biol. 1977 Jul 15;113(4):679–695. doi: 10.1016/0022-2836(77)90230-3. [DOI] [PubMed] [Google Scholar]
  9. Docherty R. J., Edwards J. G., Garrod D. R., Mattey D. L. Chick embryonic pigmented retina is one of the group of epithelioid tissues that lack cytokeratins and desmosomes and have intermediate filaments composed of vimentin. J Cell Sci. 1984 Oct;71:61–74. doi: 10.1242/jcs.71.1.61. [DOI] [PubMed] [Google Scholar]
  10. Drenckhahn D., Gröschel-Stewart U. Localization of myosin and actin in ocular nonmuscle cells. Immunofluorescence-microscopic, biochemical, and electron-microscopic studies. Cell Tissue Res. 1977 Jul 19;181(4):493–503. doi: 10.1007/BF00221771. [DOI] [PubMed] [Google Scholar]
  11. Edds K. T. Isolation and characterization of two forms of a cytoskeleton. J Cell Biol. 1979 Oct;83(1):109–115. doi: 10.1083/jcb.83.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. FARQUHAR M. G., PALADE G. E. Junctional complexes in various epithelia. J Cell Biol. 1963 May;17:375–412. doi: 10.1083/jcb.17.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Garrels J. I., Gibson W. Identification and characterization of multiple forms of actin. Cell. 1976 Dec;9(4 Pt 2):793–805. doi: 10.1016/0092-8674(76)90142-2. [DOI] [PubMed] [Google Scholar]
  14. Gowing L. R., Tellam R. L., Banyard M. R. Microfilament organization and total actin content are decreased in hybrids derived from the fusion of HeLa cells with human fibroblasts. J Cell Sci. 1984 Jul;69:137–146. doi: 10.1242/jcs.69.1.137. [DOI] [PubMed] [Google Scholar]
  15. Hull B. E., Staehelin L. A. The terminal web. A reevaluation of its structure and function. J Cell Biol. 1979 Apr;81(1):67–82. doi: 10.1083/jcb.81.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. KLUG A., BERGER J. E. AN OPTICAL METHOD FOR THE ANALYSIS OF PERIODICITIES IN ELECTRON MICROGRAPHS, AND SOME OBSERVATIONS ON THE MECHANISM OF NEGATIVE STAINING. J Mol Biol. 1964 Dec;10:565–569. doi: 10.1016/s0022-2836(64)80081-4. [DOI] [PubMed] [Google Scholar]
  17. Korn E. D. Actin polymerization and its regulation by proteins from nonmuscle cells. Physiol Rev. 1982 Apr;62(2):672–737. doi: 10.1152/physrev.1982.62.2.672. [DOI] [PubMed] [Google Scholar]
  18. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  19. Mazia D., Schatten G., Sale W. Adhesion of cells to surfaces coated with polylysine. Applications to electron microscopy. J Cell Biol. 1975 Jul;66(1):198–200. doi: 10.1083/jcb.66.1.198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mooseker M. S., Graves T. A., Wharton K. A., Falco N., Howe C. L. Regulation of microvillus structure: calcium-dependent solation and cross-linking of actin filaments in the microvilli of intestinal epithelial cells. J Cell Biol. 1980 Dec;87(3 Pt 1):809–822. doi: 10.1083/jcb.87.3.809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Murray R. L., Dubin M. W. The occurrence of actinlike filaments in association with migrating pigment granules in frog retinal pigment epithelium. J Cell Biol. 1975 Mar;64(3):705–710. doi: 10.1083/jcb.64.3.705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nachmias V. T. Platelet and megakaryocyte shape change: triggered alterations in the cytoskeleton. Semin Hematol. 1983 Oct;20(4):261–281. [PubMed] [Google Scholar]
  23. Otto J. J., Kane R. E., Bryan J. Redistribution of actin and fascin in sea urchin eggs after fertilization. Cell Motil. 1980;1(1):31–40. doi: 10.1002/cm.970010104. [DOI] [PubMed] [Google Scholar]
  24. Owaribe K., Kodama R., Eguchi G. Demonstration of contractility of circumferential actin bundles and its morphogenetic significance in pigmented epithelium in vitro and in vivo. J Cell Biol. 1981 Aug;90(2):507–514. doi: 10.1083/jcb.90.2.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Owaribe K., Masuda H. Isolation and characterization of circumferential microfilament bundles from retinal pigmented epithelial cells. J Cell Biol. 1982 Oct;95(1):310–315. doi: 10.1083/jcb.95.1.310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pollard T. D. Cytoplasmic contractile proteins. J Cell Biol. 1981 Dec;91(3 Pt 2):156s–165s. doi: 10.1083/jcb.91.3.156s. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Santerre R. F., Rich A. Actin accumulation in developing chick brain and other tissues. Dev Biol. 1976 Nov;54(1):1–12. doi: 10.1016/0012-1606(76)90281-5. [DOI] [PubMed] [Google Scholar]
  28. Spudich J. A., Amos L. A. Structure of actin filament bundles from microvilli of sea urchin eggs. J Mol Biol. 1979 Apr 5;129(2):319–331. doi: 10.1016/0022-2836(79)90285-7. [DOI] [PubMed] [Google Scholar]
  29. Stossel T. P. Contribution of actin to the structure of the cytoplasmic matrix. J Cell Biol. 1984 Jul;99(1 Pt 2):15s–21s. doi: 10.1083/jcb.99.1.15s. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tilney L. G., Tilney M. S. Observations on how actin filaments become organized in cells. J Cell Biol. 1984 Jul;99(1 Pt 2):76s–82s. doi: 10.1083/jcb.99.1.76s. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Turksen K., Opas M., Aubin J. E., Kalnins V. I. Microtubules, microfilaments and adhesion patterns in differentiating chick retinal pigment epithelial (RPE) cells in vitro. Exp Cell Res. 1983 Sep;147(2):379–391. doi: 10.1016/0014-4827(83)90220-3. [DOI] [PubMed] [Google Scholar]
  32. Weeds A. G., Pope B. Studies on the chymotryptic digestion of myosin. Effects of divalent cations on proteolytic susceptibility. J Mol Biol. 1977 Apr;111(2):129–157. doi: 10.1016/s0022-2836(77)80119-8. [DOI] [PubMed] [Google Scholar]
  33. Witt D. P., Brown D. J., Gordon J. A. Transformation-sensitive isoactin in passaged chick embryo fibroblasts transformed by Rous sarcoma virus. J Cell Biol. 1983 Jun;96(6):1766–1771. doi: 10.1083/jcb.96.6.1766. [DOI] [PMC free article] [PubMed] [Google Scholar]

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