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Modulation of the Sliding Movement of Myosin-Driven Actin Filaments Associated with Their Distortion: The Effect of ATP, ADP, and Inorganic Phosphate

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The Role of Water in ATP Hydrolysis Energy Transduction by Protein Machinery

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Abstract

The motility of actin filaments interacting with myosin motors during ATP hydrolysis can be evaluated using an in vitro motility assay. Motility assays with fluorescence imaging techniques allow us to measure the sliding velocity as an index of motility and fluctuations of actin filaments at nanometer accuracy. Because actin filaments are flexible, distortions such as deformation of their filamentous structure are also observed during the sliding movement. This chapter discusses an imaging analysis of velocity fluctuation and distortion of actin filaments in the case of myosin II motors derived from skeletal fast muscle. The relationship between the velocity and distortion is discussed. In addition, the effect of ADP and inorganic phosphate (Pi), which are products of ATP hydrolysis, on this relationship is explained through the kinetics of myosin–actin binding. Considering the fluctuation studies conducted to date, we review our concept with respect to the coordination of motion along single actin filaments, wherein distortions alter the geometric features surrounding actin–myosin in terms of water behavior.

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References

  • Amano KI, Yoshidome T, Iwaki M, Suzuki M, Kinoshita M (2010) Entropic potential field formed for a linear-motor protein near a filament: statistical-mechanical analyses using simple models. J Chem Phys 133:045103

    Article  Google Scholar 

  • Asakura S, Oosawa F (1954) On interaction between two bodies immersed in a solution of macromolecules. J Chem Phys 22:1255–1256

    Article  CAS  Google Scholar 

  • Astumian RD, Bier M (1996) Mechanochemical coupling of the motion of molecular motors to ATP hydrolysis. Biophys J 70:637–653

    Article  CAS  Google Scholar 

  • Batters C, Veigel C, Homsher E, Sellers JR (2014) To understand muscle you must take it apart. Front Physiol 5:90

    Article  Google Scholar 

  • Cho SS, Reddy G, Straub JE, Thirumalai D (2011) Entropic stabilization of proteins by TMAO. J Phys Chem B 115:13401–13407

    Article  CAS  Google Scholar 

  • Cooke R (2004) The Sliding Filament Model. J Gen Physiol 123:643–656

    Article  CAS  Google Scholar 

  • Crevenna AH, Arciniega M, Dupont A, Mizuno N, Kowalska K, Lange OF, Wedlich-Söldner R, Lamb DC (2015) Side-binding proteins modulate actin filament dynamics. Elife 4:1–18

    Article  Google Scholar 

  • Debold EP, Longyear TJ, Turner MA (2012) The effects of phosphate and acidosis on regulated thin-filament velocity in an in vitro motility assay. J Appl Physiol 113:1413–1422

    Article  CAS  Google Scholar 

  • Debold EP, Turner MA, Stout JC, Walcott S (2011) Phosphate enhances myosin-powered actin filament velocity under acidic conditions in a motility assay. Am J Physiol—Regul Integr Comp Physiol 300:R1401–R1408

    Article  CAS  Google Scholar 

  • Debold EP, Walcott S, Woodward M, Turner MA (2013) Direct observation of phosphate inhibiting the Force-generating capacity of a miniensemble of myosin molecules. Biophys J 105:2374–2384

    Article  CAS  Google Scholar 

  • Galkin VE, Orlova A, Egelman EH (2012) Actin filaments as tension sensors. Curr Biol 22:R96–R101

    Article  CAS  Google Scholar 

  • Hatori K, Iwasaki T, Wada R (2014) Effect of urea and trimethylamine N-oxide on the binding between actin molecules. Biophys Chem 193–194:20–26

    Article  Google Scholar 

  • Hatori K, Honda H, Matsuno K (1996a) ATP-dependent fluctuations of single actin filaments in vitro. Biophys Chem 58:267–272

    Article  CAS  Google Scholar 

  • Hatori K, Honda H, Matsuno K (1996b) Communicative interaction of myosins along an actin filament in the presence of ATP. Biophys Chem 60:149–152

    Article  CAS  Google Scholar 

  • Hatori K, Honda H, Shimada K, Matsuno K (1998) Propagation of a signal coordinating force generation along an actin filament in actomyosin complexes. Biophys Chem 75:81–85

    Article  CAS  Google Scholar 

  • Hatori K, Honda H, Shimada K, Matsuno K (1999) Onset of the sliding movement of an actin filament on myosin molecules: From isotropic to anisotropic fluctuations. Biophys Chem 82:29–33

    Article  CAS  Google Scholar 

  • Hatori K, Matsui M, Omote Y (2009) Slowly modulating fluctuations as mesoscopic distortions occurring on an actin filament. BioSystems 96:14–18

    Article  CAS  Google Scholar 

  • Hatori K, Sakamaki J, Honda H, Shimada K, Matsuno K (2004) Transition from contractile to protractile distortions occurring along an actin filament sliding on myosin molecules. Biophys Chem 107:283–288

    Article  CAS  Google Scholar 

  • Honda H, Hatori K, Igarashi Y, Shimada K, Matsuno K (1999) Contractile and protractile coordination within an actin filament sliding on myosin molecules. Biophys Chem 80:137–141

    Article  Google Scholar 

  • Honda H, Nagashima H, Asakura S (1986) Directional movement of F-actin in vitro. J Mol Biol 191:131–133

    Article  CAS  Google Scholar 

  • Hooft AM, Maki EJ, Cox KK, Baker JE (2007) An accelerated state of myosin-based actin motility. Biochemistry 46:3513–3520

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kabir SR, Yokoyama K, Mihashi K, Kodama T, Suzuki M (2003) Hyper-mobile water is induced around actin filaments. Biophys J 85:3154–3161

    Article  CAS  Google Scholar 

  • Kron SJ, Spudich JA (1986) Fluorescent actin filaments move on myosin fixed to a glass surface. Proc Natl Acad Sci U S A 83:6272–6276

    Article  CAS  Google Scholar 

  • Kumemoto R, Yusa K, Shibayama T, Hatori K (2012) Trimethylamine N-oxide suppresses the activity of the actomyosin motor. Biochim Biophys Acta 1820:1597–1604

    Article  CAS  Google Scholar 

  • Leijnse N, Oddershede LB, Bendix PM (2015) Helical buckling of actin inside filopodia generates traction. Proc Natl Acad Sci U S A 112:136–141

    Article  CAS  Google Scholar 

  • Lindemann CB, Lesich KA (2010) Flagellar and ciliary beating: the proven and the possible. J Cell Sci 123:519–528

    Article  CAS  Google Scholar 

  • Makhatadze GI, Privalov PL (1995) Energetics of protein structure. Adv Protein Chem 47:307–425

    Article  CAS  Google Scholar 

  • Matsushita S, Hatori K (2012) Insight into force transmission along actin filaments: Sliding movement of actin filaments containing inactive components on myosin molecules. In: Consuelas VA, Minas DJ (eds) Actin: structure, functions and disease. Nova Science Publishers, Hauppauge NY, pp 257–269

    Google Scholar 

  • McCullough BR, Blanchoin L, Martiel JL, De La Cruz EM (2008) Cofilin increases the bending flexibility of actin filaments: Implications for severing and cell mechanics. J Mol Biol 381:550–558

    Article  CAS  Google Scholar 

  • Nie QM, Togashi A, Sasaki TN, Takano M, Sasai M, Terada TP (2014) Coupling of lever arm swing and biased Brownian motion in actomyosin. PLoS Comput Biol 10:1–13

    Article  Google Scholar 

  • Munakata S, Hatori K (2013) The excluded volume effect induced by poly(ethylene glycol) modulates the motility of actin filaments interacting with myosin. FEBS J 280:5875–5883

    Article  CAS  Google Scholar 

  • 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 143:275–287

    Article  CAS  Google Scholar 

  • Murrell MP, Gardel ML (2012) F-actin buckling coordinates contractility and severing in a biomimetic actomyosin cortex. Proc Natl Acad Sci U S A 109:20820–20825

    Article  CAS  Google Scholar 

  • 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 6:35449

    Article  CAS  Google Scholar 

  • Oguchi Y, Mikhailenko SV, Ohki T, Olivares AO, De La Cruz EM, Ishiwata S (2008) Load-dependent ADP binding to myosins V and VI: Implications for subunit coordination and function. Proc Natl Acad Sci U S A 105:7714–7719

    Article  CAS  Google Scholar 

  • Ohnuki J, Sato T, Takano M (2016) Piezoelectric allostery of protein. Phys Rev E 94:12406

    Article  Google Scholar 

  • Oosawa F (2008) The unit event of sliding of the chemo-mechanical enzyme composed of myosin and actin with regulatory proteins. Biochem Biophys Res Commun 369:144–148

    Article  CAS  Google Scholar 

  • Rust MJ, Bates M, Zhuang X (2006) Stochastic optical reconstruction miscroscopy (STORM) provides sub-diffraction-limit image resolution. Nat Methods 3:793–795

    Article  CAS  Google Scholar 

  • Sakamaki J, Honda H, Imai E, Hatori K, Shimada K, Matsuno K (2003) Enhancement of the sliding velocity of actin filaments in the presence of ATP analogue: AMP-PNP. Biophys Chem 105:59–66

    Article  CAS  Google Scholar 

  • Shimo R, Mihashi K (2001) Fluctuation of local points of F-actin sliding on the surface-fixed H-meromyosin molecules in the presence of ATP. Biophys Chem 93:23–35

    Article  CAS  Google Scholar 

  • Steffen W, Smith D, Sleep J (2003) The working stroke upon myosin-nucleotide complexes binding to actin. Proc Natl Acad Sci U S A 100:6434–6439

    Article  CAS  Google Scholar 

  • Stewart TJ, Jackson DR, Smith RD, Shannon SF, Cremo CR, Baker JE (2013) Actin sliding velocities are influenced by the driving forces of actin-myosin binding. Cell Mol Bioeng 6:26–37

    Article  CAS  Google Scholar 

  • Taylor EW (1991) Kinetic studies on the association and dissociation of myosin subfragment 1 and actin. J Biol Chem 266:294–302

    CAS  PubMed  Google Scholar 

  • 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 386:149–162

    Article  CAS  Google Scholar 

  • 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:e26200

    Article  CAS  Google Scholar 

  • Uyeda TQP, Kron SJ, Spudich JA (1990) Myosin step size. estimation from slow sliding movement of actin over low densities of heavy meromyosin. J Mol Biol 214:699–710

    Article  CAS  Google Scholar 

  • Vikhorev PG, Vikhoreva NN, MĂĄnsson A (2008) Bending flexibility of actin filaments during motor-induced sliding. Biophys J 95:5809–5819

    Article  CAS  Google Scholar 

  • Walker ML, Burgess SA, Sellers JR, Wang F, Hammer JA, Trinick J, Knight PJ (2000) Two-headed binding of a processive myosin to F-actin. Nature 405:804–807

    Article  CAS  Google Scholar 

  • Wazawa T, Yasui S, Morimoto N, Suzuki M (2013) 1,3-Diethylurea-enhanced Mg-ATPase activity of skeletal muscle myosin with a converse effect on the sliding motility. Biochim Biophys Acta 1834:2620–2629

    Article  CAS  Google Scholar 

  • Yanagida T, Nakase M, Nishiyama K, Oosawa F (1984) Direct observation of motion of single F-actin filaments in the presence of myosin. Nature 307:58–60

    Article  CAS  Google Scholar 

  • Yildiz A, Forkey JN, McKinney SA, Ha T, Goldman YE, Selvin PR (2003) Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization. Science 300:2061–2065

    Article  CAS  Google Scholar 

  • Yoke H, Shingyoji C (2017) Effects of external strain on the regulation of microtubule sliding induced by outer arm dynein of sea urchin sperm flagella. J Exp Biol 220:1122–1134

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Bio-Systems Engineering, Graduate School of Science and Engineering, Yamagata University, Yonezawa, Japan

    Kuniyuki Hatori & Satoru Kikuchi

Authors
  1. Kuniyuki Hatori
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  2. Satoru Kikuchi
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Correspondence to Kuniyuki Hatori .

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Editors and Affiliations

  1. Institute of Engineering Education, Tohoku University, Sendai, Miyagi, Japan

    Makoto Suzuki

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Hatori, K., Kikuchi, S. (2018). Modulation of the Sliding Movement of Myosin-Driven Actin Filaments Associated with Their Distortion: The Effect of ATP, ADP, and Inorganic Phosphate. In: Suzuki, M. (eds) The Role of Water in ATP Hydrolysis Energy Transduction by Protein Machinery. Springer, Singapore. https://doi.org/10.1007/978-981-10-8459-1_20

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