Actomyosin contractility spatiotemporally regulates actin network dynamics in migrating cells

Journal of Biomechanics

Volumn 42, Issue 15, 2009, Pages 2540-2548

  Okeyo, Kennedy Omondi ^a   Adachi, Taiji ^a,b   Sunaga, Junko ^b   Hojo, Masaki ^a  

^a KYOTO UNIVERSITY   (Japan)

^b RIKEN   (Japan)

Author keywords

Actin filament network; Actomyosin contractility; Cell biomechanics; Cell migration; Cytoskeletal dynamics; Fluorescent speckle microscopy; Mechanobiology; Particle imaging velocimetry

Indexed keywords

ACTIN FILAMENT NETWORK; ACTOMYOSIN CONTRACTILITY; CELL MIGRATION; CYTOSKELETAL DYNAMICS; FLUORESCENT SPECKLE MICROSCOPY; MECHANOBIOLOGY; PARTICLE IMAGING VELOCIMETRY;

BIOMECHANICS; CELL MEMBRANES; DEFORMATION; FILAMENTS (LAMP); FLOW OF WATER; FLUORESCENCE; MECHANICAL ENGINEERING; SPECKLE; VELOCIMETERS; VELOCITY MEASUREMENT; VIBRATIONS (MECHANICAL);

CYTOLOGY;

F ACTIN; MYOSIN ADENOSINE TRIPHOSPHATASE;

ANIMAL CELL; ARTICLE; BIOMECHANICS; CELL ACTIVITY; CELL MIGRATION; CONTROLLED STUDY; CYTOSKELETON; DYNAMICS; ENZYME ACTIVITY; KERATINOCYTE; LAMELLIPODIUM; MECHANICAL STRESS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM;

ACTINS; ACTOMYOSIN; ANIMALS; CELL MOVEMENT; CELLS, CULTURED; CYTOSKELETON; FISHES; KERATINOCYTES; MOLECULAR MOTOR PROTEINS; STRESS, MECHANICAL;

EID: 70350400267     PISSN: 00219290     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiomech.2009.07.002     Document Type: Article

References (43)

1. Adachi T., Okeyo K.O., Shitagawa Y., and Hojo M. Strain field in actin filament network in lamellipodia of migrating cells: implication for network reorganization. Journal of Biomechanics 42 (2009) 297-302
2. Ananthakrishnan R., and Ehrlicher A. The forces behind cell movement. International Journal of Biological Sciences 3 (2007) 303-317
3. Anderson K.I., and Cross R. Contact dynamics during keratocyte motility. Current Biology 10 (2000) 253-260
4. Choquet D., Felsenfeld D.P., and Sheetz M.P. Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell 88 (1997) 39-48
5. Costa K.D., Hucker W.J., and Yin F.C. Buckling of actin stress fibers: a new wrinkle in the cytoskeletal tapestry. Cell Motility and the Cytoskeleton 52 (2002) 266-274
6. Dancker P., Low I., Hasselbach W., and Wieland T. Interaction of actin with phalloidin: polymerization and stabilization of F actin. Biochimica et Biophysica Acta 400 (1975) 407-414
7. Danuser G., and Waterman-Storer C.M. Quantitative fluorescent speckle microscopy of cytoskeleton dynamics. Annual Review of Biophysics and Biomolecular Structure 35 (2006) 361-387
8. Hayakawa K., Tatsumi H., and Sokabe M. Mechanical tension in actin filaments prevents cofilin from disassembling the filaments. Cell Structure and Function 30 (2005) 113
9. Henson J.H., Kolnik S.E., Fried C.A., Nazarian R., McGreevy J., Schulberg K.L., Detweiler M., and Trabosh V.A. Actin-based centripetal flow: phosphatase inhibition by calyculin-A alters flow pattern, actin organization, and actomyosin distribution. Cell Motility and the Cytoskeleton 56 (2003) 252-266
10. Henson J.H., Svitkina T.M., Burns A.R., Hughes H.E., MacPartland K.J., Nazarian R., and Borisy G.G. Two components of actin-based retrograde flow in sea urchin coelomocytes. Molecular Biology of the Cell 10 (1999) 4075-4090
11. Henson J.H., Svitkina T.M., Hughes H.E., Mendola R.J., and Borisy G.G. Structural organization of actin and myosin II in sea urchin coelomocytes undergoing centripetal/retrograde flow. Molecular Biology of the Cell 8 (1997) 969
12. Hu K., Ji L., Applegate K.T., Danuser G., and Waterman-Storer C.M. Differential transmission of actin motion within focal adhesions. Science 315 (2007) 111-115
13. Ishihara H., Martin B.L., Brautigan D.L., Karaki H., Ozaki H., Kato Y., Fusetani N., Watabe S., Hashimoto K., Uemura D., and Hartshorne D.J. Calyculin A and okadaic acid: Inhibitors of protein phosphatase activity. Biochemical and Biophysical Research Communications 159 (1989) 871-877
14. Ji L., Lim J., and Danuser G. Fluctuations of intracellular forces during cell protrusion. Nature Cell Biology 10 (2008) 1393-1400
15. Kaverina I., Krylyshkina O., and Small J.V. Regulation of substrate adhesion dynamics during cell motility. The International Journal Biochemistry and Cell Biology 34 (2002) 746-761
16. Kolega J. The role of myosin II motor activity in distributing myosin asymmetrically and coupling protrusive activity to cell translocation. Molecular Biology of the Cell 17 (2006) 4435-4445
17. Lauffenburger D.A., and Horwitz A.F. Cell migration: a physically integrated molecular process. Cell 84 (1996) 359-369
18. Lee J., Ishihara A., Theriot J.A., and Jacobson K. Principles of locomotion for simple-shaped cells. Nature 362 (1993) 167-171
19. Li Q., Sarna S.K., and Chien S. Nuclear Myosin II Regulates the Assembly of Preinitiation Complex for Icam-1 Gene Transcription. Gastroenterology 137 3 (2009) 1054-1063
20. Li S., Guan J.L., and Chien S. Biochemistry and biomechanics of cell motility. Annual Review of Biomedical Engineering 7 (2005) 105-150
21. Lin C.H., Espreafico E.M., Mooseker M.S., and Forscher P. Myosin drives retrograde F-actin flow in neuronal growth cones. Neuron 16 (1996) 769-782
22. Mitchison T.J., and Cramer L.P. Actin-based cell motility and cell locomotion. Cell 84 (1996) 371-379
23. Okeyo K.O., Shitagawa Y., Adachi T., and Hojo M. Quantitative evaluation of strain field in the lamella region of cellular fragments from fish keratocytes. Journal of Biomechanics 39 Supplement 1 (2006) S244
24. Palecek S.P., Loftus J.C., Ginsberg M.H., Lauffenburger D.A., and Horwitz A.F. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385 (1997) 537-540
25. Pollard T.D., and Borisy G.G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112 (2003) 453-465
26. Ponti A., Matov A., Adams M., Gupton S., Waterman-Storer C.M., and Danuser G. Periodic patterns of actin turnover in lamellipodia and lamellae of migrating epithelial cells analyzed by quantitative fluorescent speckle microscopy. Biophysical Journal 89 (2005) 3456-3469
27. Sato K., Adachi T., Shirai Y., and Tomita Y. Local disassembly of actin stress fibers induced by selected release of intracellular tension in osteoblastic cell. Journal of Biomechanical Science and Engineering 1 (2006) 204-214
28. Schaub S., Bohnet S., Laurent V.M., Meister J.J., and Verkhovsky A.B. Comparative maps of motion and assembly of filamentous actin and myosin II in migrating cells. Molecular Biology of the Cell 18 (2007) 3723-3732
29. Small J.V., Anderson K., and Rottner K. Actin and the coordination of protrusion, attachment and retraction in cell crawling. Bioscience Reports 16 (1996) 351-368
30. Straight A.F., Cheung A., Limouze J., Chen I., Westwood N.J., Sellers J.R., and Mitchison T.J. Dissecting temporal and spatial control of cytokinesis with a myosin II inhibitor. Science 299 (2003) 1743-1747
31. Svitkina T.M., Verkhovsky A.B., McQuade K.M., and Borisy G.G. Analysis of the actin-myosin II system in fish epidermal keratocytes: mechanism of cell body translocation. Journal of Cell Biology 139 (1997) 397-415
32. Tan J.L., Tien J., Pirone D.M., Gray D.S., Bhadriraju K., and Chen C.S. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proceedings of the National Academy of Sciences of the United States of America 100 (2003) 1484-1489
33. Vallotton P., Danuser G., Bohnet S., Meister J.J., and Verkhovsky A.B. Tracking retrograde flow in keratocytes: news from the front. Molecular Biology of the Cell 16 (2005) 1223-1231
34. Vallotton P., Gupton S.L., Waterman-Storer C.M., and Danuser G. Simultaneous mapping of filamentous actin flow and turnover in migrating cells by quantitative fluorescent speckle microscopy. Proceedings of the National Academy of Sciences of the United States of America 101 (2004) 9660-9665
35. Verkhovsky A.B., Svitkina T.M., and Borisy G.G. Myosin-II filament assemblies in the active lamella of fibroblasts-their morphogenesis and role in the formation of actin filament bundles. Journal of Cell Biology 131 (1995) 989-1002
36. Verkhovsky A.B., Svitkina T.M., and Borisy G.G. Contraction of actin-myosin II dynamic network drives cell translocation. Molecular Biology of the Cell 8 (1997) 974
37. Verkhovsky A.B., Svitkina T.M., and Borisy G.G. Network contraction model for cell translocation and retrograde flow. Biochemical Society Symposium 65 (1999) 207-222
38. Wang Y. Mobility of filamentous actin in living cytoplasm. Journal of Cell Biology 105 (1987) 2811-2816
39. Watanabe N., and Mitchison T.J. Single-molecule speckle analysis of actin filament turnover in lamellipodia. Science 295 (2002) 1083-1086
40. Waterman-Storer C.M., Desai A., Bulinski J.C., and Salmon E.D. Fluorescent speckle microscopy, a method to visualize the dynamics of protein assemblies in living cells. Current Biology 8 (1998) 1227-1230
41. Wehland J., Osborn M., and Weber K. Phalloidin-induced actin polymerization in the cytoplasm of cultured cells interferes with cell locomotion and growth. Proceedings of the National Academy of Sciences of the United States of America 74 (1977) 5613-5617
42. Wehland J., Osborn M., and Weber K. Phalloidin associates with microfilaments after microinjection into tissue culture cells. European Journal of Cell Biology 21 (1980) 188-194
43. Willert C.E., and Gharib M. Digital particle image velocimetry. Experiments in Fluids 10 (1991) 181-193