How tropomyosin regulates lamellipodial actin-based motility: A combined biochemical and reconstituted motility approach

EMBO Journal

Volumn 29, Issue 1, 2010, Pages 14-26

  Bugyi, Beáta ^a   Didry, Dominique ^a   Carlier, Marie France ^a  

^a LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

Author keywords

Actin; Lamella; Lamellipodium; Protrusion; Reconstituted motility; Tropomyosin

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; TROPOMYOSIN;

ACTIN FILAMENT; ARTICLE; CELL MOTILITY; CONTROLLED STUDY; DENDRITIC CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; NERVE FIBER GROWTH; PRIORITY JOURNAL; PROTEIN BINDING; ANIMAL; BINDING COMPETITION; BIOLOGICAL MODEL; CATTLE; CELL MOTION; IN VITRO STUDY; METABOLISM; PHYSIOLOGY; PSEUDOPODIUM; RABBIT; SKELETAL MUSCLE;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; ACTINS; ANIMALS; BINDING, COMPETITIVE; CATTLE; CELL MOVEMENT; HUMANS; MODELS, BIOLOGICAL; MUSCLE FIBERS, SKELETAL; PSEUDOPODIA; RABBITS; TROPOMYOSIN; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

EID: 75649129741     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.316     Document Type: Article

References (51)

1. Abercrombie M, Heaysman JE, Pegrum SM (1970) The locomotion of fibroblasts in culture. 3. Movements of particles on the dorsal surface of the leading lamella. Exp Cell Res 62: 389-398
2. Akin O, Mullins RD (2008) Capping protein increases the rate of actin-based motility by promoting filament nucleation by the Arp2/3 complex. Cell 133: 841-851
3. Bernstein BW, Bamburg JR (1982) Tropomyosin binding to F-actin protects the F-actin from disassembly by brain actin-depolymerizing factor (ADF). Cell Motil 2: 1-8
4. Blanchoin L, Pollard TD, Hitchcock-DeGregori SE (2001) Inhibition of the Arp2/3 complex-nucleated actin polymerization and branch formation by tropomyosin. Curr Biol 11: 1300-1304
5. Boussouf SE, Maytum R, Jaquet K, Geeves MA (2007) Role of tropomyosin isoforms in the calcium sensitivity of striated muscle thin filaments. J Muscle Res Cell Motil 28: 49-58
6. Broschat KO, Weber A, Burgess DR (1989) Tropomyosin stabilizes the pointed end of actin filaments by slowing depolymerization. Biochemistry 28: 8501-8506
7. Bugyi B, Le Clainche C, Romet-Lemonne G, Carlier MF (2008) How do in vitro reconstituted actin-based motility assays provide insight into in vivo behavior? FEBS Lett 582: 2086-2092
8. Cai L, Makhov AM, Schafer DA, Bear JE (2008) Coronin 1B antagonizes cortactin and remodels Arp2/3-containing actin branches in lamellipodia. Cell 134: 828-842
9. Carlier MF, Laurent V, Santolini J, Melki R, Didry D, Xia GX, Hong Y, Chua NH, Pantaloni D (1997) Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J Cell Biol 136: 1307-1322
10. Carlier MF, Pantaloni D, Korn ED (1986) Fluorescence measurements of the binding of cations to high-affinity and low-affinity sites on ATP-G-actin. J Biol Chem 261: 10778-10784
11. Carlsson AE (2003) Growth velocities of branched actin networks. Biophys J 84: 2907-2918
12. Cooper JA (2002) Actin dynamics: tropomyosin provides stability. Curr Biol 12: R523-R525
13. Delatour V, Helfer E, Didry D, Le KH, Gaucher JF, Carlier MF, Romet-Lemonne G (2008) Arp2/3 controls the motile behavior of N-WASP-functionalized GUVs and modulates N-WASP surface distribution by mediating transient links with actin filaments. Biophys J 94: 4890-4905
14. DesMarais V, Ichetovkin I, Condeelis J, Hitchcock-DeGregori SE (2002) Spatial regulation of actin dynamics: a tropomyosin-free, actin-rich compartment at the leading edge. J Cell Sci 115: 4649-4660
15. Disanza A, Carlier MF, Stradal TE, Didry D, Frittoli E, Confalonieri S, Croce A, Wehland J, Di Fiore PP, Scita G (2004) Eps8 controls actin-based motility by capping the barbed ends of actin filaments. Nat Cell Biol 6: 1180-1188
16. Gao L, Bretscher A (2008) Analysis of unregulated formin activity reveals how yeast can balance F-actin assembly between different microfilament-based organizations. Mol Biol Cell 19: 1474-1484
17. Giannone G, Dubin-Thaler BJ, Rossier O, Cai Y, Chaga O, Jiang G, Beaver W, Dobereiner HG, Freund Y, Borisy G, Sheetz MP (2007) Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell 128: 561-575
18. 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. J Cell Biol 168: 619-631
19. Gupton SL, Eisenmann K, Alberts AS, Waterman-Storer CM (2007) mDia2 regulates actin and focal adhesion dynamics and organization in the lamella for efficient epithelial cell migration. J Cell Sci 120: 3475-3487
20. Helfer E, Nevalainen EM, Naumanen P, Romero S, Didry D, Pantaloni D, Lappalainen P, Carlier MF (2006) Mammalian twinfilin sequesters ADP-G-actin and caps filament barbed ends: implications in motility. EMBO J 25: 1184-1195
21. Hillberg L, Zhao Rathje LS, Nyakern-Meazza M, Helfand B, Goldman RD, Schutt CE, Lindberg U (2006) Tropomyosins are present in lamellipodia of motile cells. Eur J Cell Biol 85: 399-409
22. Huber F, Kas J, Stuhrmann B (2008) Growing actin networks form lamellipodium and lamellum by self-assembly. Biophys J 95: 5508-5523
23. Isambert H, Venier P, Maggs AC, Fattoum A, Kassab R, Pantaloni D, Carlier MF (1995) Flexibility of actin filaments derived from thermal fluctuations. Effect of bound nucleotide, phalloidin, and muscle regulatory proteins. J Biol Chem 270: 11437-11444
24. Iwasa JH, Mullins RD (2007) Spatial and temporal relationships between actin-filament nucleation, capping, and disassembly. Curr Biol 17: 395-406
25. Karpova TS, Tatchell K, Cooper JA (1995) Actin filaments in yeast are unstable in the absence of capping protein or fimbrin. J Cell Biol 131: 1483-1493
26. Kiuchi T, Ohashi K, Kurita S, Mizuno K (2007) Cofilin promotes stimulus-induced lamellipodium formation by generating an abundant supply of actin monomers. J Cell Biol 177: 465-476
27. Koestler SA, Auinger S, Vinzenz M, Rottner K, Small JV (2008) Differentially oriented populations of actin filaments generated in lamellipodia collaborate in pushing and pausing at the cell front. Nat Cell Biol 10: 306-313
28. Kouyama T, Mihashi K (1981) Fluorimetry study of N-(1-pyrenyl) iodoacetamide-labelled F-actin. Local structural change of actin protomer both on polymerization and on binding of heavy meromyosin. Eur J Biochem 114: 33-38
29. Lai FP, Szczodrak M, Block J, Faix J, Breitsprecher D, Mannherz HG, Stradal TE, Dunn GA, Small JV, Rottner K (2008) Arp2/3 complex interactions and actin network turnover in lamellipodia. EMBO J 27: 982-992
30. Laine RO, Phaneuf KL, Cunningham CC, Kwiatkowski D, Azuma T, Southwick FS (1998) Gelsolin, a protein that caps the barbed ends and severs actin filaments, enhances the actin-based motility of Listeria monocytogenes in host cells. Infect Immun 66: 3775-3782
31. Le Clainche C, Carlier MF (2004) Actin-based motility assay. Curr Protoc Cell Biol Chapter 12, unit 12.7.1-12.7.20
32. Le Clainche C, Pantaloni D, Carlier MF (2003) ATP hydrolysis on actin-related protein 2/3 complex causes debranching of dendritic actin arrays. Proc Natl Acad Sci USA 100: 6337-6342
33. Loisel TP, Boujemaa R, Pantaloni D, Carlier MF (1999) Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401: 613-616
34. Machesky LM, Mullins RD, Higgs HN, Kaiser DA, Blanchoin L, May RC, Hall ME, Pollard TD (1999) Scar, a WASP-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc Natl Acad Sci USA 96: 3739-3744
35. Miyoshi T, Tsuji T, Higashida C, Hertzog M, Fujita A, Narumiya S, Scita G, Watanabe N (2006) Actin turnover-dependent fast dissociation of capping protein in the dendritic nucleation actin network: evidence of frequent filament severing. J Cell Biol 175: 947-955
36. Mogilner A, Oster G (1996) Cell motility driven by actin polymerization. Biophys J 71: 3030-3045
37. Nyakern-Meazza M, Narayan K, Schutt CE, Lindberg U (2002) Tropomyosin and gelsolin cooperate in controlling the microfilament system. J Biol Chem 277: 28774-28779
38. Ono S, Ono K (2002) Tropomyosin inhibits ADF/cofilin-dependent actin filament dynamics. J Cell Biol 156: 1065-1076
39. Pantaloni D, Boujemaa R, Didry D, Gounon P, Carlier MF (2000) The Arp2/3 complex branches filament barbed ends: functional antagonism with capping proteins. Nat Cell Biol 2: 385-391
40. Pantaloni D, Le Clainche C, Carlier MF (2001) Mechanism of actinbased motility. Science 292: 1502-1506
41. Pollard TD (1986) Rate constants for the reactions of ATP- and ADP-actin with the ends of actin filaments. J Cell Biol 103: 2747-2754
42. Ponti A, Machacek M, Gupton SL, Waterman-Storer CM, Danuser G (2004) Two distinct actin networks drive the protrusion of migrating cells. Science 305: 1782-1786
43. Sarmiento C, Wang W, Dovas A, Yamaguchi H, Sidani M, El-Sibai M, Desmarais V, Holman HA, Kitchen S, Backer JM, Alberts A, Condeelis J (2008) WASP family members and formin proteins coordinate regulation of cell protrusions in carcinoma cells. J Cell Biol 180: 1245-1260
44. Schaus TE, Taylor EW, Borisy GG (2007) Self-organization of actin filament orientation in the dendritic-nucleation/array-treadmilling model. Proc Natl Acad Sci USA 104: 7086-7091
45. Smillie LB (1982) Preparation and identification of alpha- and beta-tropomyosins. Methods Enzymol 85 (Pt B): 234-241
46. Svitkina TM, Borisy GG (1999) Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J Cell Biol 145: 1009-1026
47. Vallotton P, Small JV (2009) Shifting views on the leading role of the lamellipodium in cell migration: speckle tracking revisited. J Cell Sci 122: 1955-1958
48. Wawro B, Greenfield NJ, Wear MA, Cooper JA, Higgs HN, Hitchcock-DeGregori SE (2007) Tropomyosin regulates elongation by formin at the fast-growing end of the actin filament. Biochemistry 46: 8146-8155
49. Weigt C, Wegner A, Koch MH (1991) Rate and mechanism of the assembly of tropomyosin with actin filaments. Biochemistry 30: 10700-10707
50. Weisswange I, Newsome TP, Schleich S, Way M (2009) The rate of N-WASP exchange limits the extent of Arp2/3-complex-dependent actin-based motility. Nature 458: 87-91
51. Wiesner S, Helfer E, Didry D, Ducouret G, Lafuma F, Carlier MF, Pantaloni D (2003) A biomimetic motility assay provides insight into the mechanism of actin-based motility. J Cell Biol 160: 387-398