Abstract
Free full text
Comparison of actin and cell surface dynamics in motile fibroblasts
Abstract
We have investigated the dynamic behavior of actin in fibroblast lamellipodia using photoactivation of fluorescence. Activated regions of caged resorufin (CR)-labeled actin in lamellipodia of IMR 90 and MC7 3T3 fibroblasts were observed to move centripetally over time. Thus in these cells, actin filaments move centripetally relative to the substrate. Rates were characteristic for each cell type; 0.66 +/- 0.27 microns/min in IMR 90 and 0.36 +/- 0.16 microns/min in MC7 3T3 cells. In neither case was there any correlation between the rate of actin movement and the rate of lamellipodial protrusion. The half-life of the activated CR-actin filaments was approximately 1 min in IMR 90 lamellipodia, and approximately 3 min in MC7 3T3 lamellipodia. Thus continuous filament turnover accompanies centripetal movement. In both cell types, the length of time required for a section of the actin meshwork to traverse the lamellipodium was several times longer than the filament half-life. The dynamic behavior of the dorsal surface of the cell was also observed by tracking lectin-coated beads on the surface and phase-dense features within lamellipodia of MC7 3T3 cells. The movement of these dorsal features occurred at rates approximately three times faster than the rate of movement of the underlying bulk actin cytoskeleton, even when measured in the same individual cells. Thus the transport of these dorsal features must occur by some mechanism other than simple attachment to the moving bulk actin cytoskeleton.
Full Text
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Abercrombie M, Heaysman JE, Pegrum SM. The locomotion of fibroblasts in culture. I. Movements of the leading edge. Exp Cell Res. 1970 Mar;59(3):393–398. [Abstract] [Google Scholar]
- Abercrombie M, Heaysman JE, Pegrum SM. 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. [Abstract] [Google Scholar]
- Amato PA, Taylor DL. Probing the mechanism of incorporation of fluorescently labeled actin into stress fibers. J Cell Biol. 1986 Mar;102(3):1074–1084. [Europe PMC free article] [Abstract] [Google Scholar]
- AMBROSE EJ. The movements of fibrocytes. Exp Cell Res. 1961;Suppl 8:54–73. [Abstract] [Google Scholar]
- Bray D, White JG. Cortical flow in animal cells. Science. 1988 Feb 19;239(4842):883–888. [Abstract] [Google Scholar]
- Bretscher MS. Directed lipid flow in cell membranes. Nature. 1976 Mar 4;260(5546):21–23. [Abstract] [Google Scholar]
- Dembo M, Harris AK. Motion of particles adhering to the leading lamella of crawling cells. J Cell Biol. 1981 Nov;91(2 Pt 1):528–536. [Europe PMC free article] [Abstract] [Google Scholar]
- Fisher GW, Conrad PA, DeBiasio RL, Taylor DL. Centripetal transport of cytoplasm, actin, and the cell surface in lamellipodia of fibroblasts. Cell Motil Cytoskeleton. 1988;11(4):235–247. [Abstract] [Google Scholar]
- Forscher P, Smith SJ. Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J Cell Biol. 1988 Oct;107(4):1505–1516. [Europe PMC free article] [Abstract] [Google Scholar]
- Heath JP, Holifield BF. Cell locomotion: new research tests old ideas on membrane and cytoskeletal flow. Cell Motil Cytoskeleton. 1991;18(4):245–257. [Abstract] [Google Scholar]
- Hill TL, Kirschner MW. Subunit treadmilling of microtubules or actin in the presence of cellular barriers: possible conversion of chemical free energy into mechanical work. Proc Natl Acad Sci U S A. 1982 Jan;79(2):490–494. [Europe PMC free article] [Abstract] [Google Scholar]
- Holifield BF, Jacobson K. Mapping trajectories of Pgp-1 membrane protein patches on surfaces of motile fibroblasts reveals a distinct boundary separating capping on the lamella and forward transport on the retracting tail. J Cell Sci. 1991 Feb;98(Pt 2):191–203. [Abstract] [Google Scholar]
- Holifield BF, Ishihara A, Jacobson K. Comparative behavior of membrane protein-antibody complexes on motile fibroblasts: implications for a mechanism of capping. J Cell Biol. 1990 Dec;111(6 Pt 1):2499–2512. [Europe PMC free article] [Abstract] [Google Scholar]
- Kreis TE, Geiger B, Schlessinger J. Mobility of microinjected rhodamine actin within living chicken gizzard cells determined by fluorescence photobleaching recovery. Cell. 1982 Jul;29(3):835–845. [Abstract] [Google Scholar]
- Kucik DF, Elson EL, Sheetz MP. Cell migration does not produce membrane flow. J Cell Biol. 1990 Oct;111(4):1617–1622. [Europe PMC free article] [Abstract] [Google Scholar]
- Lee J, Gustafsson M, Magnusson KE, Jacobson K. The direction of membrane lipid flow in locomoting polymorphonuclear leukocytes. Science. 1990 Mar 9;247(4947):1229–1233. [Abstract] [Google Scholar]
- Mitchison TJ. Polewards microtubule flux in the mitotic spindle: evidence from photoactivation of fluorescence. J Cell Biol. 1989 Aug;109(2):637–652. [Europe PMC free article] [Abstract] [Google Scholar]
- Mitchison T, Kirschner M. Cytoskeletal dynamics and nerve growth. Neuron. 1988 Nov;1(9):761–772. [Abstract] [Google Scholar]
- Okabe S, Hirokawa N. Incorporation and turnover of biotin-labeled actin microinjected into fibroblastic cells: an immunoelectron microscopic study. J Cell Biol. 1989 Oct;109(4 Pt 1):1581–1595. [Europe PMC free article] [Abstract] [Google Scholar]
- Okabe S, Hirokawa N. Actin dynamics in growth cones. J Neurosci. 1991 Jul;11(7):1918–1929. [Europe PMC free article] [Abstract] [Google Scholar]
- Oster GF, Perelson AS. The physics of cell motility. J Cell Sci Suppl. 1987;8:35–54. [Abstract] [Google Scholar]
- Pollard TD. Rate constants for the reactions of ATP- and ADP-actin with the ends of actin filaments. J Cell Biol. 1986 Dec;103(6 Pt 2):2747–2754. [Europe PMC free article] [Abstract] [Google Scholar]
- Rinnerthaler G, Herzog M, Klappacher M, Kunka H, Small JV. Leading edge movement and ultrastructure in mouse macrophages. J Struct Biol. 1991 Feb;106(1):1–16. [Abstract] [Google Scholar]
- Smith SJ. Neuronal cytomechanics: the actin-based motility of growth cones. Science. 1988 Nov 4;242(4879):708–715. [Abstract] [Google Scholar]
- Soranno T, Bell E. Cytostructural dynamics of spreading and translocating cells. J Cell Biol. 1982 Oct;95(1):127–136. [Europe PMC free article] [Abstract] [Google Scholar]
- Svitkina TM, Neyfakh AA, Jr, Bershadsky AD. Actin cytoskeleton of spread fibroblasts appears to assemble at the cell edges. J Cell Sci. 1986 Jun;82:235–248. [Abstract] [Google Scholar]
- Symons MH, Mitchison TJ. Control of actin polymerization in live and permeabilized fibroblasts. J Cell Biol. 1991 Aug;114(3):503–513. [Europe PMC free article] [Abstract] [Google Scholar]
- Theriot JA, Mitchison TJ. Actin microfilament dynamics in locomoting cells. Nature. 1991 Jul 11;352(6331):126–131. [Abstract] [Google Scholar]
- Wang YL. Exchange of actin subunits at the leading edge of living fibroblasts: possible role of treadmilling. J Cell Biol. 1985 Aug;101(2):597–602. [Europe PMC free article] [Abstract] [Google Scholar]
Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press
Full text links
Read article at publisher's site: https://doi.org/10.1083/jcb.119.2.367
Read article for free, from open access legal sources, via Unpaywall: https://rupress.org/jcb/article-pdf/119/2/367/1418411/367.pdf
Citations & impact
Impact metrics
Citations of article over time
Alternative metrics
Smart citations by scite.ai
Explore citation contexts and check if this article has been
supported or disputed.
https://scite.ai/reports/10.1083/jcb.119.2.367
Article citations
Mechanisms of actin disassembly and turnover.
J Cell Biol, 222(12):e202309021, 10 Nov 2023
Cited by: 10 articles | PMID: 37948068 | PMCID: PMC10638096
Review Free full text in Europe PMC
Extraction of accurate cytoskeletal actin velocity distributions from noisy measurements.
Nat Commun, 13(1):4749, 13 Aug 2022
Cited by: 4 articles | PMID: 35963858 | PMCID: PMC9376101
Early Events in Actin Cytoskeleton Dynamics and E-Cadherin-Mediated Cell-Cell Adhesion during Epithelial-Mesenchymal Transition.
Cells, 9(3):E578, 29 Feb 2020
Cited by: 26 articles | PMID: 32121325 | PMCID: PMC7140442
Coupling of β2 integrins to actin by a mechanosensitive molecular clutch drives complement receptor-mediated phagocytosis.
Nat Cell Biol, 21(11):1357-1369, 28 Oct 2019
Cited by: 72 articles | PMID: 31659275 | PMCID: PMC6858589
The matrix environmental and cell mechanical properties regulate cell migration and contribute to the invasive phenotype of cancer cells.
Rep Prog Phys, 82(6):064602, 04 Apr 2019
Cited by: 100 articles | PMID: 30947151
Review
Go to all (90) article citations
Similar Articles
To arrive at the top five similar articles we use a word-weighted algorithm to compare words from the Title and Abstract of each citation.
Centripetal transport of cytoplasm, actin, and the cell surface in lamellipodia of fibroblasts.
Cell Motil Cytoskeleton, 11(4):235-247, 01 Jan 1988
Cited by: 76 articles | PMID: 3219732
On the mechanisms of cortical actin flow and its role in cytoskeletal organisation of fibroblasts.
Symp Soc Exp Biol, 47:35-56, 01 Jan 1993
Cited by: 39 articles | PMID: 8165576
Review
Lamellipodia architecture: actin filament turnover and the lateral flow of actin filaments during motility.
Semin Cell Biol, 5(3):157-163, 01 Jun 1994
Cited by: 44 articles | PMID: 7919229
Review
Integrin-cytoskeletal interactions in migrating fibroblasts are dynamic, asymmetric, and regulated.
J Cell Biol, 123(4):977-991, 01 Nov 1993
Cited by: 183 articles | PMID: 8227153 | PMCID: PMC2200147