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Tropomyosin pp 223–231Cite as

Tropomyosins Regulate the Impact of Actin Binding Proteins on Actin Filaments

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Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 644))

Abstract

The state of actin depends intimately on its interaction partners in eukaryotic cells. Classically, the cooperative force-generating acto-myosin couple is turned off and on by the calcium-dependent binding and release of tropomyosin molecules. The situation with nonmuscle cells appears to be much more complicated, with tropomyosin isoforms regulating the kinds of tension-producing and stress-bearing structures formed of actin filaments. The polymerization of even the shortest gelsolin-capped filaments is efficiently promoted by the binding of tropomyosin, for example, a process that might occur all the way out to the leading edges of advancing cells. Recently, multimers of tropomyosin have been discovered that appear to be assembly intermediates, formed from identical tropomyosin molecules, which act as ready pools of tropomyosin during the catalytic formation of lamellipodia and filopodia. Remarkably, these multimers apparently reform during the disassembly of cellular actin-containing structures. The existence of these recyclable, tropomyosin isoform-specific structures suggests how cells prevent nonproductive association of non-identical, but closely similar, tropomyosin isoforms.

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References

  1. Hoglund AS, Karlsson R, Arro E et al. Visualization of the peripheral weave of microfilaments in glia cells. J Muscle Res Cell Motil 1980; 1:127–46.

    Article  PubMed  CAS  Google Scholar 

  2. Small JV, Rinnerthaler G, Hinssen H. Organization of actin meshworks in cultured cells: the leading edge. Cold Spring Harb Symp Quant Biol 1982; 46 (Pt 2):599–611.

    PubMed  Google Scholar 

  3. Lindberg U, Karlsson R, Lassing I et al. The microfilament system and malignancy. Semin Cancer Biol 2007; 18:2–11.

    Article  PubMed  Google Scholar 

  4. Pollard TD, Borisy GG. Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003; 112:453–65.

    Article  PubMed  CAS  Google Scholar 

  5. Small JV, Stradal T, Vignal E et al. The lamellipodium: where motility begins. Trends Cell Biol 2002; 12:112–20.

    Article  PubMed  CAS  Google Scholar 

  6. Danuser G, Oldenbourg, R. Probing f-actin flow by tracking shape fluctuations of radial bundles in lamellipodia of motile cells. Biophys J 2000; 79:191–201.

    Article  PubMed  CAS  Google Scholar 

  7. Theriot JA, Mitchison TJ. Comparison of actin and cell surface dynamics in motile fibroblasts. J Cell Biol 1992; 119:367–77.

    Article  PubMed  CAS  Google Scholar 

  8. Watanabe N, Mitchison TJ. Single-molecule speckle analysis of actin filament turnover in lamellipodia. Science 2002; 295:1083–6.

    Article  PubMed  CAS  Google Scholar 

  9. Zhang H, Berg JS, Li Z et al. Myosin-X provides a motor-based link between integrins and the cytoskeleton. Nat Cell Biol 2004; 6:523–31.

    Article  PubMed  Google Scholar 

  10. Geiger B, Bershadsky A. Exploring the neighborhood: adhesion-coupled cell mechanosensors. Cell 2002; 110:139–42.

    Article  PubMed  CAS  Google Scholar 

  11. Geiger B, Bershadsky A, Pankov R et al. Transmembrane crosstalk between the extracellular matrix—cytoskeleton crosstalk. Nat Rev Mol Cell Biol 2001; 2:793–805.

    Article  PubMed  CAS  Google Scholar 

  12. Schwartz MA, Horwitz AR. Integrating adhesion, protrusion and contraction during cell migration. Cell 2006; 125:1223–5.

    Article  PubMed  CAS  Google Scholar 

  13. Nelson WJ, Drees F, Yamada S. Interaction of cadherin with the actin cytoskeleton. Novartis Found Symp 2005; 269:159–68; discussion 168–77:223–30.

    Article  PubMed  CAS  Google Scholar 

  14. Gunning P, O’Neill G, Hardeman E. Tropomyosin-based regulation of the actin cytoskeleton in time and space. Physiol Rev 2008; 88:1–35.

    Article  PubMed  CAS  Google Scholar 

  15. Gunning PW, Schevzov G, Kee AJ et al. Tropomyosin isoforms: divining rods for actin cytoskeleton function. Trends Cell Biol 2005; 15:333–41.

    Article  PubMed  CAS  Google Scholar 

  16. Bamburg JR. Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu Rev Cell Dev Biol 1999; 15:185–230.

    Article  PubMed  CAS  Google Scholar 

  17. Bamburg JR, Wiggan OP. ADF/cofilin and actin dynamics in disease. Trends Cell Biol 2002; 12:598–605.

    Article  PubMed  CAS  Google Scholar 

  18. McGough A. F-actin-binding proteins. Curr Opin Struct Biol 1998; 8:166–76.

    Article  PubMed  CAS  Google Scholar 

  19. DesMarais V, Macaluso F, Condeelis J et al. Synergistic interaction between the Arp2/3 complex and cofilin drives stimulated lamellipod extension. J Cell Sci 2004; 117:3499–510.

    Article  PubMed  CAS  Google Scholar 

  20. van Rheenen J, Song X, van Roosmalen W et al. EGF-induced PIP2 hydrolysis releases and activates cofilin locally in carcinoma cells. J Cell Biol 2007; 179:1247–59.

    Article  PubMed  Google Scholar 

  21. Blanchoin L, Pollard TD, Hitchcock-DeGregori SE. Inhibition of the Arp2/3 complex-nucleated actin polymerization and branch formation by tropomyosin. Curr Biol 2001; 11:1300–4.

    Article  PubMed  CAS  Google Scholar 

  22. Ono S, Ono K. Tropomyosin inhibits ADF/cofilin-dependent actin filament dynamics. J Cell Biol 2002; 156:1065–76.

    Article  PubMed  CAS  Google Scholar 

  23. Evangelista M, Zigmond S, Boone C. Formins: signaling effectors for assembly and polarization of actin filaments. J Cell Sci 2003; 116:2603–11.

    Article  PubMed  CAS  Google Scholar 

  24. Wawro B, Greenfield NJ, Wear MA et al. Tropomyosin regulates elongation by formin at the fast-growing end of the actin filament. Biochemistry 2007; 46:8146–55.

    Article  PubMed  CAS  Google Scholar 

  25. Le Clainche C, Pantaloni D, Carlier MF. ATP hydrolysis on actin-related protein 2/3 complex causes debranching of dendritic actin arrays. Proc Natl Acad Sci USA 2003; 100:6337–42.

    Article  PubMed  Google Scholar 

  26. Cooper JA, Bryan J, Schwab B 3rd et al. Microinjection of gelsolin into living cells. J Cell Biol 1987; 104:491–501.

    Article  PubMed  CAS  Google Scholar 

  27. Cooper JA, Loftus DJ, Frieden C et al. Localization and mobility of gelsolin in cells. J Cell Biol 1988; 106:1229–40.

    Article  PubMed  CAS  Google Scholar 

  28. Janmey PA, Chaponnier C, Lind SE et al. Interactions of gelsolin and gelsolin-actin complexes with actin. Effects of calcium on actin nucleation, filament severing and end blocking. Biochemistry 1985; 24:3714–23.

    Article  PubMed  CAS  Google Scholar 

  29. Glenney JR Jr, Kaulfus P, Weber K. F actin assembly modulated by villin: Ca++-dependent nucleation and capping of the barbed end. Cell 1981; 24:471–80.

    Article  PubMed  CAS  Google Scholar 

  30. Burtnick LD, Koepf EK, Grimes J et al. The crystal structure of plasma gelsolin: implications for actin severing, capping and nucleation. Cell 1997; 90:661–70.

    Article  PubMed  CAS  Google Scholar 

  31. Burtnick LD, Robinson RC, Choe S. Structure and function of gelsolin. Results Probl Cell Differ 2001; 32:201–11.

    PubMed  CAS  Google Scholar 

  32. McGough AM, Staiger CJ, Min JK et al. The gelsolin family of actin regulatory proteins: modular structures, versatile functions. FEBS Lett 2003; 552:75–81.

    Article  PubMed  CAS  Google Scholar 

  33. Ressad F, Didry D, Xia GX et al. Kinetic analysis of the interaction of actin-depolymerizing factor (ADF)/cofilin with G-and F-actins. Comparison of plant and human ADFs and effect of phosphorylation. J Biol Chem 1998; 273:20894–902.

    Article  PubMed  CAS  Google Scholar 

  34. Ressad F, Didry D, Egile C et al. Control of actin filament length and turnover by actin depolymerizing factor (ADF/cofilin) in the presence of capping proteins and ARP2/3 complex. J Biol Chem 1999; 274:20970–6.

    Article  PubMed  CAS  Google Scholar 

  35. Orlova A, Egelman EH. Structural dynamics of F-actin: I. Changes in the C terminus. J Mol Biol 1995; 245:582–97.

    Article  PubMed  CAS  Google Scholar 

  36. Orlova A, Prochniewicz E, Egelman EH. Structural dynamics of F-actin: II. Cooperativity in structural transitions. J Mol Biol 1995; 245:598–607.

    Article  PubMed  CAS  Google Scholar 

  37. Prochniewicz E, Zhang Q, Janmey PA et al. Cooperativity in F-actin: binding of gelsolin at the barbed end affects structure and dynamics of the whole filament. J Mol Biol 1996; 260:756–66.

    Article  PubMed  CAS  Google Scholar 

  38. Bernstein BW, Painter WB, Chen H et al. Intracellular pH modulation of ADF/cofilin proteins. Cell Motil Cytoskeleton 2000; 47:319–36.

    Article  PubMed  CAS  Google Scholar 

  39. Nishida E, Maekawa S, Sakai H. Cofilin, a protein in porcine brain that binds to actin filaments and inhibits their interactions with myosin and tropomyosin. Biochemistry 1984; 23:5307–13.

    Article  PubMed  CAS  Google Scholar 

  40. De La Cruz E, Pollard TD. Transient kinetic analysis of rhodamine phalloidin binding to actin filaments. Biochemistry 1994; 33:14387–92.

    Article  Google Scholar 

  41. Allen PG, Janmey PA. Gelsolin displaces phalloidin from actin filaments. A new fluorescence method shows that both Ca2+ and Mg2+ affect the rate at which gelsolin severs F-actin. J Biol Chem 1994; 269:32916–23.

    PubMed  CAS  Google Scholar 

  42. McGough A, Pope B, Chiu W et al. Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J Cell Biol 1997; 138:771–81.

    Article  PubMed  CAS  Google Scholar 

  43. Ishikawa R, Yamashiro S, Matsumura F. Annealing of gelsolin-severed actin fragments by tropomyosin in the presence of Ca2+. Potentiation of the annealing process by caldesmon. J Biol Chem 1989; 264:16764–70.

    PubMed  CAS  Google Scholar 

  44. Nyakern-Meazza M, Narayan K, Schutt CE et al. Tropomyosin and gelsolin cooperate in controlling the microfilament system. J Biol Chem 2002; 277:28774–9.

    Article  PubMed  CAS  Google Scholar 

  45. Amano T, Tanabe K, Eto T et al. LIM-kinase 2 induces formation of stress fibres, focal adhesions and membrane blebs, dependent on its activation by Rho-associated kinase-catalysed phosphorylation at threonine-505. Biochem J 2001; 354:149–59.

    Article  PubMed  CAS  Google Scholar 

  46. Dan C, Kelly A, Bernard O et al. Cytoskeletal changes regulated by the PAK4 serine/threonine kinase are mediated by LIM kinase 1 and cofilin. J Biol Chem 2001; 276:32115–21.

    Article  PubMed  CAS  Google Scholar 

  47. Hillberg L, Zhao Rathje LS, Nyakern-Meazza M et al. Tropomyosins are present in lamellipodia of motile cells. Eur J Cell Biol 2006; 85:399–409.

    Article  PubMed  CAS  Google Scholar 

  48. Lin JJ, Matsumura F, Yamashiro-Matsumura S. Tropomyosin-enriched and alpha-actinin-enriched microfilaments isolated from chicken embryo fibroblasts by monoclonal antibodies. J Cell Biol 1984; 98:116–27.

    Article  PubMed  CAS  Google Scholar 

  49. Holmes KC, Popp D, Gebhard W et al. Atomic model of the actin filament. Nature 1990; 347:44–9.

    Article  PubMed  CAS  Google Scholar 

  50. Poole KJ, Lorenz M, Evans G et al. A comparison of muscle thin filament models obtained from electron microscopy reconstructions and low-angle X-ray fibre diagrams from non-overlap muscle. J Struct Biol 2006; 155:273–84.

    Article  PubMed  CAS  Google Scholar 

  51. Lepault J, Erk I, Nicolas G et al. Time-resolved cryo-electron microscopy of vitrified muscular components. J Microsc 1991; 161:47–57.

    PubMed  CAS  Google Scholar 

  52. Narita A, Maeda Y. Molecular determination by electron microscopy of the actin filament end structure. J Mol Biol 2007; 365:480–501.

    Article  PubMed  CAS  Google Scholar 

  53. Schutt CE, Rozycki MD, Myslik JC et al. A discourse on modeling F-actin. J Struct Biol 1995; 115:186–98.

    Article  PubMed  CAS  Google Scholar 

  54. Schutt CE, Lindberg U. Actin as the generator of tension during muscle contraction. Proc Natl Acad Sci USA 1992; 89:319–23.

    Article  PubMed  CAS  Google Scholar 

  55. Schutt CE, Lindberg U. Muscle contraction as a Markov process. I: Energetics of the process. Acta Physiol Scand 1998; 163:307–23.

    Article  PubMed  CAS  Google Scholar 

  56. Houle F, Poirier A, Dumaresq J et al. DAP kinase mediates the phosphorylation of tropomyosin-1 downstream of the ERK pathway, which regulates the formation of stress fibers in response to oxidative stress. J Cell Sci 2007; 120:3666–77.

    Article  PubMed  CAS  Google Scholar 

  57. Blikstad I, Carlsson L. On the dynamics of the microfilament system in HeLa cells. J Cell Biol 1982; 93:122–8.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Uno Lindberg .

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© 2008 Landes Bioscience and Springer Science+Business Media

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Lindberg, U. et al. (2008). Tropomyosins Regulate the Impact of Actin Binding Proteins on Actin Filaments. In: Gunning, P. (eds) Tropomyosin. Advances in Experimental Medicine and Biology, vol 644. Springer, New York, NY. https://doi.org/10.1007/978-0-387-85766-4_17

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