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. 1982 Oct 1;95(1):127–136. doi: 10.1083/jcb.95.1.127

Cytostructural dynamics of spreading and translocating cells

PMCID: PMC2112355  PMID: 6890553

Abstract

Cytostructural changes during fibroblast spreading and translocation and during the transition between the two states have been studied in living cells and in the same cells after fixation and immunofluorescent staining. In time-lapse sequences we observe that birefringent arcs, sometimes circles, concentric with the cell perimeter, form near the periphery of a spreading cell, or that arcs form near the leading edge of a locomoting cell. The arcs move toward the nucleus, where they disappear. In spreading cells, radial stress fibers extend from the region of the cell nucleus to the periphery. The arcs or circles and the stress fibers are visualized in the same cells after fixation and staining with fluorescein-conjugated antiactin antibodies. Stained images of spreading cells show the arcs and stress fibers in the same plane of focus. At points of intersection with arcs, stress fibers are bent toward the substrate on which the cell is moving. During a transitional stage between spreading and translocation the cytostructure undergoes reproducible changes. Arcs and circle cease to form. The radial stress fibers elongate, spiral around the nucleus, and move to the periphery as a band of filaments. We interpret the moving arcs as condensations of a microfilament network that move toward the nucleus as compression waves. As elements of the net are brought close together by the compression wave, contraction may occur and facilitate the condensations.

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Selected References

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  1. AMBROSE E. J. The movements of fibrocytes. Exp Cell Res. 1961;Suppl 8:54–73. doi: 10.1016/0014-4827(61)90340-8. [DOI] [PubMed] [Google Scholar]
  2. Abercrombie M., Heaysman J. E., Pegrum S. M. The locomotion of fibroblasts in culture. IV. Electron microscopy of the leading lamella. Exp Cell Res. 1971 Aug;67(2):359–367. doi: 10.1016/0014-4827(71)90420-4. [DOI] [PubMed] [Google Scholar]
  3. Allen R. D., David G. B., Nomarski G. The zeiss-Nomarski differential interference equipment for transmitted-light microscopy. Z Wiss Mikrosk. 1969 Nov;69(4):193–221. [PubMed] [Google Scholar]
  4. Badley R. A., Couchman J. R., Rees D. A. Comparison of the cell cytoskeleton in migratory and stationary chick fibroblasts. J Muscle Res Cell Motil. 1980 Mar;1(1):5–14. doi: 10.1007/BF00711922. [DOI] [PubMed] [Google Scholar]
  5. Barak L. S., Yocum R. R., Nothnagel E. A., Webb W. W. Fluorescence staining of the actin cytoskeleton in living cells with 7-nitrobenz-2-oxa-1,3-diazole-phallacidin. Proc Natl Acad Sci U S A. 1980 Feb;77(2):980–984. doi: 10.1073/pnas.77.2.980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Buckley I. K., Porter K. R. Cytoplasmic fibrils in living cultured cells. A light and electron microscope study. Protoplasma. 1967;64(4):349–380. doi: 10.1007/BF01666538. [DOI] [PubMed] [Google Scholar]
  7. Buckley I. K. Three dimensional fine structure of cultured cells: possible implications for subcellular motility. Tissue Cell. 1975;7(1):51–72. doi: 10.1016/s0040-8166(75)80007-3. [DOI] [PubMed] [Google Scholar]
  8. Couchman J. R., Rees D. A. Actomyosin organisation for adhesion, spreading, growth and movement in chick fibroblasts. Cell Biol Int Rep. 1979 Aug;3(5):431–439. doi: 10.1016/0309-1651(79)90004-3. [DOI] [PubMed] [Google Scholar]
  9. Eisenberg E., Kielley W. W. Troponin-tropomyosin complex. Column chromatographic separation and activity of the three, active troponin components with and without tropomyosin present. J Biol Chem. 1974 Aug 10;249(15):4742–4748. [PubMed] [Google Scholar]
  10. Heath J. P. Arcs: curved microfilament bundles beneath the dorsal surface of the leading lamellae of moving chick embryo fibroblasts. Cell Biol Int Rep. 1981 Oct;5(10):975–980. doi: 10.1016/0309-1651(81)90214-9. [DOI] [PubMed] [Google Scholar]
  11. Heath J. P., Dunn G. A. Cell to substratum contacts of chick fibroblasts and their relation to the microfilament system. A correlated interference-reflexion and high-voltage electron-microscope study. J Cell Sci. 1978 Feb;29:197–212. doi: 10.1242/jcs.29.1.197. [DOI] [PubMed] [Google Scholar]
  12. Herman I. M., Crisona N. J., Pollard T. D. Relation between cell activity and the distribution of cytoplasmic actin and myosin. J Cell Biol. 1981 Jul;90(1):84–91. doi: 10.1083/jcb.90.1.84. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hynes R. O., Destree A. T. Relationships between fibronectin (LETS protein) and actin. Cell. 1978 Nov;15(3):875–886. doi: 10.1016/0092-8674(78)90272-6. [DOI] [PubMed] [Google Scholar]
  14. Höglund A. S., Karlsson R., Arro E., Fredriksson B. A., Lindberg U. Visualization of the peripheral weave of microfilaments in glia cells. J Muscle Res Cell Motil. 1980 Jun;1(2):127–146. doi: 10.1007/BF00711795. [DOI] [PubMed] [Google Scholar]
  15. KIELLEY W. W., HARRINGTON W. F. A model for the myosin molecule. Biochim Biophys Acta. 1960 Jul 15;41:401–421. doi: 10.1016/0006-3002(60)90037-8. [DOI] [PubMed] [Google Scholar]
  16. Kaiho M., Misu Y. The role of microfilaments in the spreading process of JTC-12 cells. Exp Cell Res. 1980 Jun;127(2):434–438. doi: 10.1016/0014-4827(80)90448-6. [DOI] [PubMed] [Google Scholar]
  17. Kaiho M., Sato A. Circular distribution of microfilaments in cells spreading in vitro. Exp Cell Res. 1978 Apr;113(1):222–227. doi: 10.1016/0014-4827(78)90106-4. [DOI] [PubMed] [Google Scholar]
  18. Kato I., Anfinsen C. B. Purification of synthetic ribonuclease S-peptide derivatives by specific complex formation on columns of ribonuclease S-protein bound to agarose. J Biol Chem. 1969 Nov 10;244(21):5849–5855. [PubMed] [Google Scholar]
  19. Lazarides E. Immunofluorescence studies on the structure of actin filaments in tissue culture cells. J Histochem Cytochem. 1975 Jul;23(7):507–528. doi: 10.1177/23.7.1095651. [DOI] [PubMed] [Google Scholar]
  20. Lazarides E., Lindberg U. Actin is the naturally occurring inhibitor of deoxyribonuclease I. Proc Natl Acad Sci U S A. 1974 Dec;71(12):4742–4746. doi: 10.1073/pnas.71.12.4742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lewis L., Verna J. M., Levinstone D., Sher S., Marek L., Bell E. The relationship of fibroblast translocations to cell morphology and stress fibre density. J Cell Sci. 1982 Feb;53:21–36. doi: 10.1242/jcs.53.1.21. [DOI] [PubMed] [Google Scholar]
  22. Ludueña M. A., Wessells N. K. Cell locomotion, nerve elongation, and microfilaments. Dev Biol. 1973 Feb;30(2):427–440. doi: 10.1016/0012-1606(73)90100-0. [DOI] [PubMed] [Google Scholar]
  23. Reaven E. P., Axline S. G. Subplasmalemmal microfilaments and microtubules in resting and phagocytizing cultivated macrophages. J Cell Biol. 1973 Oct;59(1):12–27. doi: 10.1083/jcb.59.1.12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Schliwa M., van Blerkom J. Structural interaction of cytoskeletal components. J Cell Biol. 1981 Jul;90(1):222–235. doi: 10.1083/jcb.90.1.222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Small J. V., Celis J. E. Filament arrangements in negatively stained cultured cells: the organization of actin. Cytobiologie. 1978 Feb;16(2):308–325. [PubMed] [Google Scholar]
  26. Spooner B. S., Yamada K. M., Wessells N. K. Microfilaments and cell locomotion. J Cell Biol. 1971 Jun;49(3):595–613. doi: 10.1083/jcb.49.3.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Weihing R. R. The cytoskeleton and plasma membrane. Methods Achiev Exp Pathol. 1979;8:42–109. [PubMed] [Google Scholar]
  28. Wessells N. K., Spooner B. S., Ash J. F., Bradley M. O., Luduena M. A., Taylor E. L., Wrenn J. T., Yamada K. Microfilaments in cellular and developmental processes. Science. 1971 Jan 15;171(3967):135–143. doi: 10.1126/science.171.3967.135. [DOI] [PubMed] [Google Scholar]

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