Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1981 Jul 1;90(1):187–200. doi: 10.1083/jcb.90.1.187

Mechanism of retraction of the trailing edge during fibroblast movement

PMCID: PMC2111832  PMID: 7195906

Abstract

Retraction of the taut, trailing portion of a moving chick heart fibroblast in vitro is an abrupt dynamic process. Upon retraction, the fibroblast tail always ruptures, leaving a small amount of itself attached to the substratum by focal contacts. Time-lapse cinemicrography shows that retraction produces a sudden, massive movement of both surface and cytoplasmic material toward a cluster of focal contacts near the main body of the cell. The appearance of folds on the upper cell surface at this time and the absence of endocytotic vesicles are consistent with this forward movement. Retraction of the trailing edge, either occurring naturally or produced artificially with a microneedle, consists of an initial fast component followed and overlapped by a slow component. Upon artificial detachment in the presence of iodoacetate, dinitrophenol, and sodium fluoride, and at 4 degrees C, the slow component is strongly inhibited and the fast one only slightly inhibited. Moreover of the bundles of microfilaments oriented parallel to the long axis of the tail seen in TEM. Most of the birefringence is lost during the fast phase and the rest during the slow phase of retraction. Concurrently, the bundles of microfilaments disappear during the fast phase of retraction and are replaced by a microfilament meshwork. All of these results are consistent with the hypothesis that the initial fast component of retraction is a passive elastic recoil, associated with the oriented bundles of microfilaments, and that the slow component of retraction is an active contraction, associated with a meshwork of microfilaments.

Full Text

The Full Text of this article is available as a PDF (2.0 MB).

Selected References

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

  1. ALLEN R. D., NAKAJIMA H. TWO-EXPOSURE, FILM DENSITOMETRIC METHOD MEASURING PHASE RETARDATIONS DUE TO WEAK BIREFRINGENCE IN FIBRILLAR OR MEMBRANOUS CELL CONSTITUENTS. Exp Cell Res. 1965 Jan;37:230–249. doi: 10.1016/0014-4827(65)90172-2. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Abercrombie M., Dunn G. A. Adhesions of fibroblasts to substratum during contact inhibition observed by interference reflection microscopy. Exp Cell Res. 1975 Apr;92(1):57–62. doi: 10.1016/0014-4827(75)90636-9. [DOI] [PubMed] [Google Scholar]
  4. Abercrombie M., Dunn G. A., Heath J. P. The shape and movement of fibroblasts in culture. Soc Gen Physiol Ser. 1977;32:57–70. [PubMed] [Google Scholar]
  5. Abercrombie M., Heaysman J. E., Pegrum S. M. The locomotion of fibroblasts in culture. 3. Movements of particles on the dorsal surface of the leading lamella. Exp Cell Res. 1970 Oct;62(2):389–398. doi: 10.1016/0014-4827(70)90570-7. [DOI] [PubMed] [Google Scholar]
  6. Abercrombie M., Heaysman J. E., Pegrum S. M. The locomotion of fibroblasts in culture. I. Movements of the leading edge. Exp Cell Res. 1970 Mar;59(3):393–398. doi: 10.1016/0014-4827(70)90646-4. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Allen R. D., Francis D. W., Nakajima H. Cyclic birefringence changes in pseudopods of Chaos carolinensis revealing the localization of the motive force in pseudopod extension. Proc Natl Acad Sci U S A. 1965 Oct;54(4):1153–1161. doi: 10.1073/pnas.54.4.1153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Anderson R. G., Vasile E., Mello R. J., Brown M. S., Goldstein J. L. Immunocytochemical visualization of coated pits and vesicles in human fibroblasts: relation to low density lipoprotein receptor distribution. Cell. 1978 Nov;15(3):919–933. doi: 10.1016/0092-8674(78)90276-3. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Betchaku T., Trinkaus J. P. Contact relations, surface activity, and cortical microfilaments of marginal cells of the enveloping layer and of the yolk syncytial and yolk cytoplasmic layers of fundulus before and during epiboly. J Exp Zool. 1978 Dec;206(3):381–426. doi: 10.1002/jez.1402060310. [DOI] [PubMed] [Google Scholar]
  12. Brunk U., Ericsson J. L., Pontén J., Westermark B. Specialization of cell surfaces in contact-inhibited human glia-like cells in vitro. Exp Cell Res. 1971 Aug;67(2):407–415. doi: 10.1016/0014-4827(71)90426-5. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Buckley I. K., Raju T. R. Form and distribution of actin and myosin in non-muscle cells: a study using cultured chick embryo fibroblasts. J Microsc. 1976 Jul;107(2):129–149. doi: 10.1111/j.1365-2818.1976.tb02431.x. [DOI] [PubMed] [Google Scholar]
  15. Burnside B. Microtubules and microfilaments in newt neuralation. Dev Biol. 1971 Nov;26(3):416–441. doi: 10.1016/0012-1606(71)90073-x. [DOI] [PubMed] [Google Scholar]
  16. CURTIS A. S. THE MECHANISM OF ADHESION OF CELLS TO GLASS. A STUDY BY INTERFERENCE REFLECTION MICROSCOPY. J Cell Biol. 1964 Feb;20:199–215. doi: 10.1083/jcb.20.2.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Carter S. B. Cell movement and cell spreading: a passive or an active process? Nature. 1970 Feb 28;225(5235):858–859. doi: 10.1038/225858a0. [DOI] [PubMed] [Google Scholar]
  18. Carter S. B. Principles of cell motility: the direction of cell movement and cancer invasion. Nature. 1965 Dec 18;208(5016):1183–1187. doi: 10.1038/2081183a0. [DOI] [PubMed] [Google Scholar]
  19. Chen W. T. Induction of spreading during fibroblast movement. J Cell Biol. 1979 Jun;81(3):684–691. doi: 10.1083/jcb.81.3.684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Culp L. A. Molecular composition and origin of substrate-attached material from normal and virus-transformed cells. J Supramol Struct. 1976;5(2):239–255. doi: 10.1002/jss.400050210. [DOI] [PubMed] [Google Scholar]
  21. Erickson C. A., Trinkaus J. P. Microvilli and blebs as sources of reserve surface membrane during cell spreading. Exp Cell Res. 1976 May;99(2):375–384. doi: 10.1016/0014-4827(76)90595-4. [DOI] [PubMed] [Google Scholar]
  22. Follett E. A., Goldman R. D. The occurrence of microvilli during spreading and growth of BHK21-C13 fibroblasts. Exp Cell Res. 1970 Jan;59(1):124–136. doi: 10.1016/0014-4827(70)90631-2. [DOI] [PubMed] [Google Scholar]
  23. Harris A. K. Cell surface movements related to cell locomotion. Ciba Found Symp. 1973;14:3–26. doi: 10.1002/9780470719978.ch2. [DOI] [PubMed] [Google Scholar]
  24. Harris A. K., Wild P., Stopak D. Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science. 1980 Apr 11;208(4440):177–179. doi: 10.1126/science.6987736. [DOI] [PubMed] [Google Scholar]
  25. Harris A. Behavior of cultured cells on substrata of variable adhesiveness. Exp Cell Res. 1973 Mar 15;77(1):285–297. doi: 10.1016/0014-4827(73)90579-x. [DOI] [PubMed] [Google Scholar]
  26. Harris A. Location of cellular adhesions to solid substrata. Dev Biol. 1973 Nov;35(1):97–114. doi: 10.1016/0012-1606(73)90009-2. [DOI] [PubMed] [Google Scholar]
  27. Harris J. K. A photoelastic substrate technique for dynamic measurements of forces exerted by moving organisms. J Microsc. 1978 Nov;114(2):219–228. doi: 10.1111/j.1365-2818.1978.tb00132.x. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Heaysman J. E., Pegrum S. M. Early contacts between fibroblasts. An ultrastructural study. Exp Cell Res. 1973 Mar 30;78(1):71–78. doi: 10.1016/0014-4827(73)90039-6. [DOI] [PubMed] [Google Scholar]
  30. Ishikawa H., Bischoff R., Holtzer H. Formation of arrowhead complexes with heavy meromyosin in a variety of cell types. J Cell Biol. 1969 Nov;43(2):312–328. [PMC free article] [PubMed] [Google Scholar]
  31. Izzard C. S., Izzard S. L. Calcium regulation of the contractile state of isolated mammalian fibroblast cytoplasm. J Cell Sci. 1975 Jul;18(2):241–256. doi: 10.1242/jcs.18.2.241. [DOI] [PubMed] [Google Scholar]
  32. Izzard C. S., Lochner L. R. Cell-to-substrate contacts in living fibroblasts: an interference reflexion study with an evaluation of the technique. J Cell Sci. 1976 Jun;21(1):129–159. doi: 10.1242/jcs.21.1.129. [DOI] [PubMed] [Google Scholar]
  33. James D. W., Taylor J. F. The stress developed by sheets of chick fibroblasts in vitro. Exp Cell Res. 1969 Jan;54(1):107–110. doi: 10.1016/0014-4827(69)90299-7. [DOI] [PubMed] [Google Scholar]
  34. Karfunkel P. The role of microtubules and microfilaments in neurulation in Xenopus. Dev Biol. 1971 May;25(1):30–56. doi: 10.1016/0012-1606(71)90018-2. [DOI] [PubMed] [Google Scholar]
  35. Lloyd C. W., Smith C. G., Woods A., Rees D. A. Mechanisms of cellular adhesion. II. The interplay between adhesion, the cytoskeleton and morphology in substrate-attached cells. Exp Cell Res. 1977 Dec;110(2):427–437. doi: 10.1016/0014-4827(77)90309-3. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Nagai R., Yoshimoto R. N., Kamiya N. Cyclic production of tension force in the plasmodial strand of Physarum polycephalum and its relation to microfilament morphology. J Cell Sci. 1978 Oct;33:205–225. doi: 10.1242/jcs.33.1.205. [DOI] [PubMed] [Google Scholar]
  38. Singer S. J., Nicolson G. L. The fluid mosaic model of the structure of cell membranes. Science. 1972 Feb 18;175(4023):720–731. doi: 10.1126/science.175.4023.720. [DOI] [PubMed] [Google Scholar]
  39. Spooner B. S., Ash J. F., Wrenn J. T., Frater R. B., Wessells N. K. Heavy meromyosin binding to microfilaments involved in cell and morphogenetic movements. Tissue Cell. 1973;5(1):37–46. doi: 10.1016/s0040-8166(73)80004-7. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. Taylor D. L., Condeelis J. S., Moore P. L., Allen R. D. The contractile basis of amoeboid movement. I. The chemical control of motility in isolated cytoplasm. J Cell Biol. 1973 Nov;59(2 Pt 1):378–394. doi: 10.1083/jcb.59.2.378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Trinkaus J. P., Betchaku T., Krulikowski L. S. Local inhibition of ruffling during contact inhibition of cell movement. Exp Cell Res. 1971 Feb;64(2):291–300. doi: 10.1016/0014-4827(71)90079-6. [DOI] [PubMed] [Google Scholar]
  43. WEISS L., COOMBS R. R. The demonstration of rupture of cell surfaces by an immunological technique. Exp Cell Res. 1963 Apr;30:331–338. doi: 10.1016/0014-4827(63)90304-5. [DOI] [PubMed] [Google Scholar]
  44. WEISS L. The measurement of cell adhesion. Exp Cell Res. 1961;Suppl 8:141–153. doi: 10.1016/0014-4827(61)90345-7. [DOI] [PubMed] [Google Scholar]
  45. Weiss P., Garber B. Shape and Movement of Mesenchyme Cells as Functions of the Physical Structure of the Medium: Contributions to a Quantitative Morphology. Proc Natl Acad Sci U S A. 1952 Mar;38(3):264–280. doi: 10.1073/pnas.38.3.264. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES