Advertisement

Uni-directional Propagation of Structural Changes in Actin Filaments

  • Taro Q. P. Uyeda
  • Kien Xuan Ngo
  • Noriyuki Kodera
  • Kiyotaka Tokuraku
Chapter

Abstract

When a protein molecule is bound with another, its structure is likely to change in one way or the other. The structure of a protein molecule in a protein complex is also likely to change when binding partner in the complex undergoes a conformational change. It is therefore no surprise that binding of an actin-binding protein to a protomer in an actin filament changes the structure of that actin protomer, and that the resultant conformational change in the actin protomer affects the structure of the neighboring protomers in the same filament. Moreover, eukaryotic actin appears to have evolved to efficiently spread the conformational change in the actin protomer initially bound with actin-binding protein over a long distance along the filament (cooperative conformational change), as has been observed in the cases of cofilin- and myosin-induced cooperative conformational changes. We speculate that the high degree of cooperativity in conformational changes in actin filaments enables cooperative binding of actin-binding proteins, which is necessary for actin filaments to perform specific functions by selectively interacting with a subset of actin-binding proteins among the large number of actin-binding proteins present in the cell. Interestingly, cooperative conformational changes propagate to only one direction along the filament, at least in the cases of cofilin and myosin II-induced conformational changes. Functional significance of those uni-directional conformational changes in actin filaments is not known, but we propose that they play roles in directional signal transmission along one-dimensional polymer in cells, or in force generation by myosin.

Keywords

Actin Cooperativity Polarity Cofilin Myosin 

References

  1. Ando T, Uchihashi T, Kodera N (2013) High-speed AFM and applications to biomolecular systems. Annu Rev Biophys 42:393–414CrossRefGoogle Scholar
  2. Belyantseva IA, Perrin BJ, Sonnemann KJ, Zhu M, Stepanyan R, McGee J, Frolenkov GI, Walsh EJ, Friderici KH, Friedman TB, Ervasti JM (2009) Gamma-actin is required for cytoskeletal maintenance but not development. Proc Natl Acad Sci USA 106:9703–9708CrossRefGoogle Scholar
  3. Blanchoin L, Pollard TD (1999) Mechanism of interaction of Acanthamoeba actophorin (ADF/Cofilin) with actin filaments. J Biol Chem 274:15538–15546CrossRefGoogle Scholar
  4. Butters CA, Willadsen KA, Tobacman LS (1993) Cooperative interactions between adjacent troponin-tropomyosin complexes may be transmitted through the actin filament. J Biol Chem 268:15565–15570PubMedGoogle Scholar
  5. Carlier MF (1990) Actin polymerization and ATP hydrolysis. Adv Biophys 26:51–73CrossRefGoogle Scholar
  6. 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 136:1307–1322CrossRefGoogle Scholar
  7. Cheney RE, Riley MA, Mooseker MS (1993) Phylogenetic analysis of the myosin superfamily. Cell Motil Cytoskeleton 24:215–223CrossRefGoogle Scholar
  8. Collins A, Huang R, Jensen MH, Moore JR, Lehman W, Wang CL (2011) Structural studies on maturing actin filaments. Bioarchitecture 1:127–133CrossRefGoogle Scholar
  9. Cooke R, Crowder MS, Wendt CH, Bamett VA, Thomas DD (1984) Muscle cross-bridges: do they rotate? Adv Exp Med Biol 170:413–427CrossRefGoogle Scholar
  10. Craig-Schmidt MC, Robson RM, Goll DE, Stromer MH (1981) Effect of α-actinin on actin structure. Release of bound nucleotide. Biochim Biophys Acta 670:9–16CrossRefGoogle Scholar
  11. Critchley DR (2000) Focal adhesions—the cytoskeletal connection. Curr Opin Cell Biol 12:133–139CrossRefGoogle Scholar
  12. De La Cruz EM (2005) Cofilin binding to muscle and non-muscle actin filaments: isoform-dependent cooperative interactions. J Mol Biol 346:557–564CrossRefGoogle Scholar
  13. Fisher AJ, Smith CA, Thoden J, Smith R, Sutoh K, Holden HM, Rayment I (1995) Structural studies of myosin: nucleotide complexes: a revised model for the molecular basis of muscle contraction. Biophys J 68:19S–26S; Discussion 27S–28SGoogle Scholar
  14. Forkey JN, Quinlan ME, Shaw MA, Corrie JE, Goldman YE (2003) Three-dimensional structural dynamics of myosin V by single-molecule fluorescence polarization. Nature 422:399–404CrossRefGoogle Scholar
  15. Fujii T, Iwane AH, Yanagida T, Namba K (2010) Direct visualization of secondary structures of F-actin by electron cryomicroscopy. Nature 467:724–728CrossRefGoogle Scholar
  16. Fujii T, Namba K (2017). Structure of actomyosin rigour complex at 5.2 Å resolution and insights into the ATPase cycle mechanism. Nat Commun 8:13969CrossRefGoogle Scholar
  17. Fujime S, Ishiwata S (1971) Dynamic study of F-actin by quasielastic scattering of laser light. J Mol Biol 62:251–265CrossRefGoogle Scholar
  18. Furuta A, Amino M, Yoshio M, Oiwa K, Kojima H, Furuta K (2017) Creating biomolecular motors based on dynein and actin-binding proteins. Nat Nanotechnol 12:233–237CrossRefGoogle Scholar
  19. Galkin VE, Orlova A, Cherepanova O, Lebart MC, Egelman EH (2008) High-resolution cryo-EM structure of the F-actin-fimbrin/plastin ABD2 complex. Proc Natl Acad Sci USA 105:1494–1498CrossRefGoogle Scholar
  20. Galkin VE, Orlova A, Egelman EH (2012) Actin filaments as tension sensors. Curr Biol 22:R96–R101CrossRefGoogle Scholar
  21. Galkin VE, Orlova A, Kudryashov DS, Solodukhin A, Reisler E, Schröder GF, Egelman EH (2011) Remodeling of actin filaments by ADF/cofilin proteins. Proc Natl Acad Sci USA 108:20568–20572CrossRefGoogle Scholar
  22. Galkin VE, Orlova A, Lukoyanova N, Wriggers W, Egelman EH (2001) Actin depolymerizing factor stabilizes an existing state of F-actin and can change the tilt of F-actin subunits. J Cell Biol 153:75–86CrossRefGoogle Scholar
  23. Galkin VE, Orlova A, Salmazo A, Djinovic-Carugo K, Egelman EH (2010a) Opening of tandem calponin homology domains regulates their affinity for F-actin. Nat Struct Mol Biol 17:614–616CrossRefGoogle Scholar
  24. Galkin VE, Orlova A, Schröder GF, Egelman EH (2010b) Structural polymorphism in F-actin. Nat Struct Mol Biol 17:1318–1323CrossRefGoogle Scholar
  25. Galkin VE, Orlova A, Vos MR, Schröder GF, Egelman EH (2015) Near-atomic resolution for one state of F-actin. Structure. 23:173–182CrossRefGoogle Scholar
  26. Graceffa P, Dominguez R (2003) Crystal structure of monomeric actin in the ATP state. Structural basis of nucleotide-dependent actin dynamics. J Biol Chem 278:34172–34180CrossRefGoogle Scholar
  27. Hanein D, Matsudaira P, DeRosier DJ (1997) Evidence for a conformational change in actin induced by fimbrin (N375) binding. J Cell Biol 139:387–396CrossRefGoogle Scholar
  28. Hansen SD, Kwiatkowski AV, Ouyang CY, Liu H, Pokutta S, Watkins SC, Volkmann N, Hanein D, Weis WI, Mullins RD, Nelson WJ (2013) αE-catenin actin-binding domain alters actin filament conformation and regulates binding of nucleation and disassembly factors. Mol Biol Cell 24:3710–3720CrossRefGoogle Scholar
  29. Hawkins M, Pope B, Maciver SK, Weeds AG (1993) Human actin depolymerizing factor mediates a pH-sensitive destruction of actin filaments. Biochemistry 32:9985–9993CrossRefGoogle Scholar
  30. Hayakawa K, Sakakibara S, Sokabe M, Tatsumi H (2014) Single-molecule imaging and kinetic analysis of cooperative cofilin-actin filament interactions. Proc Natl Acad Sci USA 111:9810–9815CrossRefGoogle Scholar
  31. Hayden SM, Miller PS, Brauweiler A, Bamburg JR (1993) Analysis of the interactions of actin depolymerizing factor with G- and F-actin. Biochemistry 32:9994–10004CrossRefGoogle Scholar
  32. Hirakawa R, Nishikawa Y, Uyeda TQP, Tokuraku K (2017) Unidirectional growth of heavy meromyosin clusters along actin filaments revealed by real-time fluorescence microscopy. Cytoskeleton (Hoboken) 74:482–489CrossRefGoogle Scholar
  33. Holmes KC (1997) The swinging lever-arm hypothesis of muscle contraction. Curr Biol 7:112–118CrossRefGoogle Scholar
  34. Huang R, Grabarek Z, Wang CL (2010) Differential effects of caldesmon on the intermediate conformational states of polymerizing actin. J Biol Chem 285:71–79CrossRefGoogle Scholar
  35. Kandasamy MK, McKinney EC, Meagher RB (2009) A single vegetative actin isovariant overexpressed under the control of multiple regulatory sequences is sufficient for normal Arabidopsis development. Plant Cell 21:701–718CrossRefGoogle Scholar
  36. Kitamura K, Tokunaga M, Iwane AH, Yanagida T (1999) A single myosin head moves along an actin filament with regular steps of 5.3 nanometres. Nature 397:129–134CrossRefGoogle Scholar
  37. Kodera N, Yamamoto D, Ishikawa R, Ando T (2010) Video imaging of walking myosin V by high-speed atomic force microscopy. Nature 468:72–76CrossRefGoogle Scholar
  38. Kondo H, Ishiwata S (1976) Uni-directional growth of F-actin. J Biochem 79:159–171CrossRefGoogle Scholar
  39. Korn ED, Carlier MF, Pantaloni D (1987) Actin polymerization and ATP hydrolysis. Science 238:638–644CrossRefGoogle Scholar
  40. Kubota H, Mikhailenko SV, Okabe H, Taguchi H, Ishiwata S (2009) D-loop of actin differently regulates the motor function of myosins II and V. J Biol Chem 284:35251–35258CrossRefGoogle Scholar
  41. Le Clainche C, Dwivedi SP, Didry D, Carlier MF (2010) Vinculin is a dually regulated actin filament barbed end-capping and side-binding protein. J Biol Chem 285:23420–23432CrossRefGoogle Scholar
  42. Loscalzo J, Reed GH, Weber A (1975) Conformational change and cooperativity in actin filaments free of tropomyosin. Proc Natl Acad Sci USA 72:3412–3415CrossRefGoogle Scholar
  43. Lymn RW, Taylor EW (1971) Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10:4617–4624CrossRefGoogle Scholar
  44. McGough A, Pope B, Chiu W, Weeds A (1997) Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J Cell Biol 138:771–781CrossRefGoogle Scholar
  45. Michelot A, Drubin DG (2011) Building distinct actin filament networks in a common cytoplasm. Curr Biol 21:R560–R569CrossRefGoogle Scholar
  46. Miki M, Wahl P, Auchet JC (1982) Fluorescence anisotropy of labeled F-actin: influence of divalent cations on the interaction between F-actin and myosin heads. Biochemistry 21:3661–3665CrossRefGoogle Scholar
  47. Murakami K, Yasunaga T, Noguchi TQP, Gomibuchi Y, Ngo KX, Uyeda TQP, Wakabayashi T (2010) Structural basis for actin assembly, activation of ATP hydrolysis, and delayed phosphate release. Cell 143:275–287CrossRefGoogle Scholar
  48. Ngo KX, Kodera N, Katayama E, Ando T, Uyeda TQP (2015) Cofilin-induced unidirectional cooperative conformational changes in actin filaments revealed by high-speed atomic force microscopy. Elife 4:e04806Google Scholar
  49. Ngo KX, Umeki N, Kijima ST, Kodera N, Ueno H, Furutani-Umezu N, Nakajima J, Noguchi TQP, Nagasaki A, Tokuraku K, Uyeda TQP (2016) Allosteric regulation by cooperative conformational changes of actin filaments drives mutually exclusive binding with cofilin and myosin. Sci Rep 6:35449CrossRefGoogle Scholar
  50. Noguchi TQP, Komori T, Umeki N, Demizu N, Ito K, Iwane AH, Tokuraku K, Yanagida T, Uyeda TQP (2012) G146V mutation at the hinge region of actin reveals a myosin class-specific requirement of actin conformations for motility. J Biol Chem 287:24339–24345CrossRefGoogle Scholar
  51. Oda T, Iwasa M, Aihara T, Maeda Y, Narita A (2009) The nature of the globular- to fibrous-actin transition. Nature 457:441–445CrossRefGoogle Scholar
  52. Oosawa F, Fujime S, Ishiwata S, Mihashi K (1973) Dynamic properties of F-actin and thin filament. Cold Spring Harbor Symp Quant Biol 37:277–285CrossRefGoogle Scholar
  53. Orlova A, Egelman EH (1997) Cooperative rigor binding of myosin to actin is a function of F-actin structure. J Mol Biol 265:469–474CrossRefGoogle Scholar
  54. Orlova A, Prochniewicz E, Egelman EH (1995) Structural dynamics of F-actin: II. Cooperativity in structural transitions. J Mol Biol 245:598–607CrossRefGoogle Scholar
  55. Otterbein LR, Graceffa P, Dominguez R (2001) The crystal structure of uncomplexed actin in the ADP state. Science 293:708–711CrossRefGoogle Scholar
  56. Papp G, Bugyi B, Ujfalusi Z, Barko S, Hild G, Somogyi B, Nyitrai M (2006) Conformational changes in actin filaments induced by formin binding to the barbed end. Biophys J 91:2564–2572CrossRefGoogle Scholar
  57. Pollard TD, Cooper JA (2009) Actin, a central player in cell shape and movement. Science 326:1208–1212CrossRefGoogle Scholar
  58. Prochniewicz E, Katayama E, Yanagida T, Thomas DD (1993) Cooperativity in F-actin: chemical modifications of actin monomers affect the functional interactions of myosin with unmodified monomers in the same actin filament. Biophys J 65:113–123CrossRefGoogle Scholar
  59. Prochniewicz E, Yanagida T (1990) Inhibition of sliding movement of F-actin by crosslinking emphasizes the role of actin structure in the mechanism of motility. J Mol Biol 216:761–772CrossRefGoogle Scholar
  60. Prochniewicz E, Zhang Q, Janmey PA, Thomas DD (1996) Cooperativity in F-actin: binding of gelsolin at the barbed end affects structure and dynamics of the whole filament. J Mol Biol 260:756–766CrossRefGoogle Scholar
  61. Romet-Lemonne G, Jegou A (2013) Mechanotransduction down to individual actin filaments. Eur J Cell Biol 92:333–338CrossRefGoogle Scholar
  62. Ruff C, Furch M, Brenner B, Manstein DJ, Meyhofer E (2001) Single-molecule tracking of myosins with genetically engineered amplifier domains. Nat Struct Biol 8:226–229CrossRefGoogle Scholar
  63. Schoenenberger CA, Mannherz HG, Jockusch BM (2011) Actin: from structural plasticity to functional diversity. Eur J Cell Biol 90:797–804CrossRefGoogle Scholar
  64. Schwyter DH, Kron SJ, Toyoshima YY, Spudich JA, Reisler E (1990) Subtilisin cleavage of actin inhibits in vitro sliding movement of actin filaments over myosin. J Cell Biol 111:465–470CrossRefGoogle Scholar
  65. Sharma S, Grintsevich EE, Hsueh C, Reisler E, Gimzewski JK (2012) Molecular cooperativity of drebrin1-300 binding and structural remodeling of F-actin. Biophys J 103:275–283CrossRefGoogle Scholar
  66. Sharma S, Grintsevich EE, Phillips ML, Reisler E, Gimzewski JK (2011) Atomic force microscopy reveals drebrin induced remodeling of f-actin with subnanometer resolution. Nano Lett 11:825–827CrossRefGoogle Scholar
  67. Siddique MS, Mogami G, Miyazaki T, Katayama E, Uyeda TQP, Suzuki M (2005) Cooperative structural change of actin filaments interacting with activated myosin motor domain, detected with copolymers of pyrene-labeled actin and acto-S1 chimera protein. Biochem Biophys Res Commun 337:1185–1191CrossRefGoogle Scholar
  68. Skau CT, Kovar DR (2010) Fimbrin and tropomyosin competition regulates endocytosis and cytokinesis kinetics in fission yeast. Curr Biol 20:1415–1422CrossRefGoogle Scholar
  69. Suarez C, Roland J, Boujemaa-Paterski R, Kang H, McCullough BR, Reymann AC, Guerin C, Martiel JL, De La Cruz EM, Blanchoin L (2011) Cofilin tunes the nucleotide state of actin filaments and severs at bare and decorated segment boundaries. Curr Biol 21:862–868CrossRefGoogle Scholar
  70. Suzuki M, Kabir SR, Siddique MS, Nazia US, Miyazaki T, Kodama T (2004) Myosin-induced volume increase of the hyper-mobile water surrounding actin filaments. Biochem Biophys Res Commun 322:340–346CrossRefGoogle Scholar
  71. Suzuki M, Mogami G, Ohsugi H, Watanabe T, Matubayasi N (2017) Physical driving force of actomyosin motility based on the hydration effect. Cytoskeleton (Hoboken) 74:512–527CrossRefGoogle Scholar
  72. Takano M, Terada TP, Sasai M (2010) Unidirectional Brownian motion observed in an in silico single molecule experiment of an actomyosin motor. Proc Natl Acad Sci USA 107:7769–7774CrossRefGoogle Scholar
  73. Tawada K (1969) Physicochemical studies of F-actin-heavy meromyosin solutions. Biochim Biophys Acta 172:311–318CrossRefGoogle Scholar
  74. Thomas DD, Seidel JC, Gergely J (1979) Rotational dynamics of spin-labeled F-actin in the sub-millisecond time range. J Mol Biol 132:257–273CrossRefGoogle Scholar
  75. Tokuraku K, Kurogi R, Toya R, Uyeda TQP (2009) Novel mode of cooperative binding between myosin and Mg2+-actin filaments in the presence of low concentrations of ATP. J Mol Biol 386:149–162CrossRefGoogle Scholar
  76. Tsiavaliaris G, Fujita-Becker S, Manstein DJ (2004) Molecular engineering of a backwards-moving myosin motor. Nature 427:558–561CrossRefGoogle Scholar
  77. Uyeda TQP, Abramson PD, Spudich JA (1996) The neck region of the myosin motor domain acts as a lever arm to generate movement. Proc Natl Acad Sci USA 93:4459–4464CrossRefGoogle Scholar
  78. Uyeda TQP, Iwadate Y, Umeki N, Nagasaki A, Yumura S (2011) Stretching actin filaments within cells enhances their affinity for the myosin II motor domain. PLoS ONE 6:e26200CrossRefGoogle Scholar
  79. Wioland H, Guichard B, Senju Y, Myram S, Lappalainen P, Jegou A, Romet-Lemonne G (2017) ADF/cofilin accelerates actin dynamics by severing filaments and promoting their depolymerization at both ends. Curr Biol 27(1956–1967):e1957Google Scholar
  80. Zigmond SH (2004) Formin-induced nucleation of actin filaments. Curr Opin Cell Biol 16:99–105CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Taro Q. P. Uyeda
    • 1
  • Kien Xuan Ngo
    • 1
    • 2
  • Noriyuki Kodera
    • 3
  • Kiyotaka Tokuraku
    • 4
  1. 1.Faculty of Advanced Science and Engineering, Department of PhysicsWaseda UniversityShinjukuJapan
  2. 2.Laboratory for Molecular BiophysicsBrain Science Institute, RIKENWako, SaitamaJapan
  3. 3.Department of Physics and Bio-AFM Frontier Research CenterKanazawa UniversityKanazawaJapan
  4. 4.Department of Applied SciencesMuroran Institute of TechnologyMuroranJapan

Personalised recommendations