Cell migration without a lamellipodium

Translation of actin dynamics into cell movement mediated by tropomyosin

Stephanie L. Gupton, Karen L. Anderson, Thomas P. Kole, Robert S. Fischer, Aaron Ponti, Sarah E. Hitchcock-DeGregori, Gaudenz Danuser, Velia M. Fowler, Denis Wirtz, Dorit Hanein, Clare M. Waterman-Storer

Research output: Contribution to journalArticle

Abstract

The actin cytoskeleton is locally regulated for functional specializations for cell motility. Using quantitative fluorescent speckle microscopy (qFSM) of migrating epithelial cells, we previously defined two distinct F-actin networks based on their F-actin-binding proteins and distinct patterns of F-actin turnover and movement. The lamellipodium consists of a treadmilling F-actin array with rapid polymerization-dependent retrograde flow and contains high concentrations of Arp2/3 and ADF/cofilin, whereas the lamella exhibits spatially random punctae of F-actin assembly and disassembly with slow myosin-mediated retrograde flow and contains myosin II and tropomyosin (TM). In this paper, we micro-injected skeletal muscle α TM into epithelial cells, and using qFSM, electron microscopy, and immunolocalization show that this inhibits functional lamellipodium formation. Cells with inhibited lamellipodia exhibit persistent leading edge protrusion and rapid cell migration. Inhibition of endogenous long TM isoforms alters protrusion persistence. Thus, cells can migrate with inhibited lamellipodia, and we suggest that TM is a major regulator of F-actin functional specialization in migrating cells.

Original languageEnglish (US)
Pages (from-to)619-631
Number of pages13
JournalJournal of Cell Biology
Volume168
Issue number4
DOIs
StatePublished - Feb 14 2005

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Tropomyosin
Pseudopodia
Cell Movement
Actins
Microscopy
Epithelial Cells
Actin Depolymerizing Factors
Myosin Type II
Myosins
Actin Cytoskeleton
Polymerization
Electron Microscopy
Protein Isoforms
Skeletal Muscle

ASJC Scopus subject areas

  • Cell Biology

Cite this

Gupton, S. L., Anderson, K. L., Kole, T. P., Fischer, R. S., Ponti, A., Hitchcock-DeGregori, S. E., ... Waterman-Storer, C. M. (2005). Cell migration without a lamellipodium: Translation of actin dynamics into cell movement mediated by tropomyosin. Journal of Cell Biology, 168(4), 619-631. https://doi.org/10.1083/jcb.200406063

Cell migration without a lamellipodium : Translation of actin dynamics into cell movement mediated by tropomyosin. / Gupton, Stephanie L.; Anderson, Karen L.; Kole, Thomas P.; Fischer, Robert S.; Ponti, Aaron; Hitchcock-DeGregori, Sarah E.; Danuser, Gaudenz; Fowler, Velia M.; Wirtz, Denis; Hanein, Dorit; Waterman-Storer, Clare M.

In: Journal of Cell Biology, Vol. 168, No. 4, 14.02.2005, p. 619-631.

Research output: Contribution to journalArticle

Gupton, SL, Anderson, KL, Kole, TP, Fischer, RS, Ponti, A, Hitchcock-DeGregori, SE, Danuser, G, Fowler, VM, Wirtz, D, Hanein, D & Waterman-Storer, CM 2005, 'Cell migration without a lamellipodium: Translation of actin dynamics into cell movement mediated by tropomyosin', Journal of Cell Biology, vol. 168, no. 4, pp. 619-631. https://doi.org/10.1083/jcb.200406063
Gupton SL, Anderson KL, Kole TP, Fischer RS, Ponti A, Hitchcock-DeGregori SE et al. Cell migration without a lamellipodium: Translation of actin dynamics into cell movement mediated by tropomyosin. Journal of Cell Biology. 2005 Feb 14;168(4):619-631. https://doi.org/10.1083/jcb.200406063
Gupton, Stephanie L. ; Anderson, Karen L. ; Kole, Thomas P. ; Fischer, Robert S. ; Ponti, Aaron ; Hitchcock-DeGregori, Sarah E. ; Danuser, Gaudenz ; Fowler, Velia M. ; Wirtz, Denis ; Hanein, Dorit ; Waterman-Storer, Clare M. / Cell migration without a lamellipodium : Translation of actin dynamics into cell movement mediated by tropomyosin. In: Journal of Cell Biology. 2005 ; Vol. 168, No. 4. pp. 619-631.
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