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PMID: 10465781 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

The actin-based nanomachine at the leading edge of migrating cells.

Biophysical journal ·Vol. 77 ·No. 3 ·1999-09-00 ·Pages 1721-32

Abraham VC, Krishnamurthi V, Taylor DL, Lanni F

Abstract

Two fundamental parameters of the highly dynamic, ultrathin lamellipodia of migrating fibroblasts have been determined-its thickness in living cells (176 +/- 14 nm), by standing-wave fluorescence microscopy, and its F-actin density (1580 +/- 613 microm of F-actin/microm(3)), via image-based photometry. In combination with data from previous studies, we have computed the density of growing actin filament ends at the lamellipodium margin (241 +/- 100/microm) and the maximum force (1.86 +/- 0.83 nN/microm) and pressure (10.5 +/- 4.8 kPa) obtainable via actin assembly. We have used cell deformability measurements (. J. Cell Sci. 44:187-200;. Proc. Natl. Acad. Sci. USA. 79:5327-5331) and an estimate of the force required to stall the polymerization of a single filament (. Proc. Natl. Acad. Sci. USA. 78:5613-5617;. Biophys. J. 65:316-324) to argue that actin assembly alone could drive lamellipodial extension directly.

MeSH Terms
3T3 Cells Actins/physiology Animals Calibration Cell Movement Cell Size Cytoplasm/physiology,ultrastructure Mice Microscopy, Electron Microscopy, Fluorescence/methods Models, Biological
Chemicals
Actins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Abraham V C
Center for Light Microscope Imaging and Biotechnology, and Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213 USA.
Krishnamurthi V
Taylor D L
Lanni F
References (49)
49 references, click to expand
  1. Life at the leading edge: the formation of cell protrusions.
    Annu Rev Cell Biol. 1993;9:411-44 PMID: 8280467
  2. Enhancement of axial resolution in fluorescence microscopy by standing-wave excitation.
    Nature. 1993 Nov 4;366(6450):44-8 PMID: 8232536
  3. Transient kinetic analysis of rhodamine phalloidin binding to actin filaments.
    Biochemistry. 1994 Dec 6;33(48):14387-92 PMID: 7981198
  4. Hemostatic, inflammatory, and fibroblast responses are blunted in mice lacking gelsolin.
    Cell. 1995 Apr 7;81(1):41-51 PMID: 7720072
  5. Measurement and manipulation of cytoskeletal dynamics in living cells.
    Curr Opin Cell Biol. 1995 Feb;7(1):4-12 PMID: 7755989
  6. Actin filament organization in the fish keratocyte lamellipodium.
    J Cell Biol. 1995 Jun;129(5):1275-86 PMID: 7775574
  7. Actin polymerization and intracellular solvent flow in cell surface blebbing.
    J Cell Biol. 1995 Jun;129(6):1589-99 PMID: 7790356
  8. Targeting of Listeria monocytogenes ActA protein to the plasma membrane as a tool to dissect both actin-based cell morphogenesis and ActA function.
    EMBO J. 1995 Jun 15;14(12):2731-44 PMID: 7796802
  9. A fluorescent protein biosensor of myosin II regulatory light chain phosphorylation reports a gradient of phosphorylated myosin II in migrating cells.
    Mol Biol Cell. 1995 Dec;6(12):1755-68 PMID: 8590803
  10. Myosin drives retrograde F-actin flow in neuronal growth cones.
    Neuron. 1996 Apr;16(4):769-82 PMID: 8607995
  11. Function of myosin-V in filopodial extension of neuronal growth cones.
    Science. 1996 Aug 2;273(5275):660-3 PMID: 8662560
  12. Myosin II transport, organization, and phosphorylation: evidence for cortical flow/solation-contraction coupling during cytokinesis and cell locomotion.
    Mol Biol Cell. 1996 Aug;7(8):1259-82 PMID: 8856669
  13. Cell motility driven by actin polymerization.
    Biophys J. 1996 Dec;71(6):3030-45 PMID: 8968574
  14. EGF stimulates an increase in actin nucleation and filament number at the leading edge of the lamellipod in mammary adenocarcinoma cells.
    J Cell Sci. 1998 Jan;111 ( Pt 2):199-211 PMID: 9405304
  15. Unconventional myosins in cell movement, membrane traffic, and signal transduction.
    Science. 1998 Jan 23;279(5350):527-33 PMID: 9438839
  16. Gelsolin is a downstream effector of rac for fibroblast motility.
    EMBO J. 1998 Mar 2;17(5):1362-70 PMID: 9482733
  17. Dimensional and mechanical dynamics of active and stable edges in motile fibroblasts investigated by using atomic force microscopy.
    Proc Natl Acad Sci U S A. 1999 Feb 2;96(3):921-6 PMID: 9927669
  18. The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin.
    J Biol Chem. 1971 Aug 10;246(15):4866-71 PMID: 4254541
  19. The locomotion of fibroblasts in culture. IV. Electron microscopy of the leading lamella.
    Exp Cell Res. 1971 Aug;67(2):359-67 PMID: 5097522
  20. Centripetal transport of attached particles on both surfaces of moving fibroblasts.
    Exp Cell Res. 1972 Aug;73(2):519-23 PMID: 4559927
  21. Interaction of actin with phalloidin: polymerization and stabilization of F-actin.
    Biochim Biophys Acta. 1975 Aug 19;400(2):407-14 PMID: 126084
  22. Phalloidin-induced actin polymerization in the cytoplasm of cultured cells interferes with cell locomotion and growth.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5613-7 PMID: 341163
  23. The deformability of BHK cells and polyoma virus-transformed BHK cells in relation to locomotory behaviour.
    J Cell Sci. 1980 Aug;44:187-200 PMID: 6254999
  24. Microfilament or microtubule assembly or disassembly against a force.
    Proc Natl Acad Sci U S A. 1981 Sep;78(9):5613-7 PMID: 6946498
  25. Organization of actin in the leading edge of cultured cells: influence of osmium tetroxide and dehydration on the ultrastructure of actin meshworks.
    J Cell Biol. 1981 Dec;91(3 Pt 1):695-705 PMID: 6799521
  26. Dependence of locally measured cellular deformability on position on the cell, temperature, and cytochalasin B.
    Proc Natl Acad Sci U S A. 1982 Sep;79(17):5327-31 PMID: 6957866
  27. Nucleated polymerization of actin from the membrane-associated ends of microvillar filaments in the intestinal brush border.
    J Cell Biol. 1982 Oct;95(1):223-33 PMID: 6890554
  28. The influence of contact-inhibited growth and of agents which alter cell morphology on the levels of G- and F-actin in cultured cells.
    Exp Cell Res. 1984 Aug;153(2):402-12 PMID: 6539711
  29. Detection and characterization of actin monomers, oligomers, and filaments in solution by measurement of fluorescence photobleaching recovery.
    Biophys J. 1984 Jul;46(1):97-110 PMID: 6743762
  30. Structural organization of interphase 3T3 fibroblasts studied by total internal reflection fluorescence microscopy.
    J Cell Biol. 1985 Apr;100(4):1091-102 PMID: 3980580
  31. Exchange of actin subunits at the leading edge of living fibroblasts: possible role of treadmilling.
    J Cell Biol. 1985 Aug;101(2):597-602 PMID: 4040521
  32. The structure of F-actin.
    J Muscle Res Cell Motil. 1985 Apr;6(2):129-51 PMID: 3897278
  33. The architecture of actin filaments and the ultrastructural location of actin-binding protein in the periphery of lung macrophages.
    J Cell Biol. 1986 Sep;103(3):1007-20 PMID: 3745263
  34. 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):2747-54 PMID: 3793756
  35. Hindered diffusion of inert tracer particles in the cytoplasm of mouse 3T3 cells.
    Proc Natl Acad Sci U S A. 1987 Jul;84(14):4910-3 PMID: 3474634
  36. Cofilin is a component of intranuclear and cytoplasmic actin rods induced in cultured cells.
    Proc Natl Acad Sci U S A. 1987 Aug;84(15):5262-6 PMID: 3474653
  37. Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone.
    J Cell Biol. 1988 Oct;107(4):1505-16 PMID: 3170637
  38. Neuronal cytomechanics: the actin-based motility of growth cones.
    Science. 1988 Nov 4;242(4879):708-15 PMID: 3055292
  39. The dynamic distribution of fluorescent analogues of actin and myosin in protrusions at the leading edge of migrating Swiss 3T3 fibroblasts.
    J Cell Biol. 1988 Dec;107(6 Pt 2):2631-45 PMID: 3204122
  40. Centripetal transport of cytoplasm, actin, and the cell surface in lamellipodia of fibroblasts.
    Cell Motil Cytoskeleton. 1988;11(4):235-47 PMID: 3219732
  41. Actin polymerization induces a shape change in actin-containing vesicles.
    Proc Natl Acad Sci U S A. 1989 Aug;86(15):5773-7 PMID: 2548187
  42. Correlated distribution of actin, myosin, and microtubules at the leading edge of migrating Swiss 3T3 fibroblasts.
    Cell Motil Cytoskeleton. 1989;14(4):527-43 PMID: 2696599
  43. Enhanced motility in NIH 3T3 fibroblasts that overexpress gelsolin.
    Science. 1991 Mar 8;251(4998):1233-6 PMID: 1848726
  44. The role of actin polymerization in cell motility.
    Annu Rev Physiol. 1991;53:585-605 PMID: 2042972
  45. Characterization of tetramethylrhodaminyl-phalloidin binding to cellular F-actin.
    Cell Motil Cytoskeleton. 1992;21(2):147-58 PMID: 1559266
  46. Phallotoxin and actin binding assay by fluorescence enhancement.
    Anal Biochem. 1992 Jan;200(1):199-204 PMID: 1595896
  47. Comparison of actin and cell surface dynamics in motile fibroblasts.
    J Cell Biol. 1992 Oct;119(2):367-77 PMID: 1400580
  48. Cellular motions and thermal fluctuations: the Brownian ratchet.
    Biophys J. 1993 Jul;65(1):316-24 PMID: 8369439
  49. The machinery of cell crawling.
    Sci Am. 1994 Sep;271(3):54-5, 58-63 PMID: 8091190
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
1999-09-00
Pages
1721-32
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1300458
Subset
IM
Grants
NIAMS NIH HHS · AR32461 · United States
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