Photosynthetica 2018, 56(4):1365-1369 | DOI: 10.1007/s11099-018-0840-6

Viscosimetric analysis of the mechanism of ATP hydrolysis by pea chloroplast F1-ATPase

A.N. Malyan1,*
1 Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia

Dependence of ATP hydrolysis kinetics by the chloroplast coupling factor (CF1) on medium viscosity was studied at varying temperatures. For samples with oxidized and reduced CF1 γ-subunit, this dependence was shown to be described by Cramers' relationship k ~ (η/ηo)-n, where k is the reaction rate constant, η/ηo is the medium/water viscosity ratio, and 0 < n < 1. Transition of the γ-subunit from its reduced to oxidized state was accompanied by increasing n value, which is indicative of increasing friction losses between certain enzyme sections and the solution. The increased medium viscosity produced no effect on the reaction activation energy which appeared to be almost the same for the both enzyme states. The molecular mechanisms responsible for CF1 activity loss in viscous media are discussed.

Keywords: ATP hydrolysis; F1-ATPase; kinetics; viscosity

Received: December 1, 2017; Accepted: March 9, 2018; Prepublished online: December 1, 2018; Published: November 1, 2018Show citation

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Malyan, A.N. (2018). Viscosimetric analysis of the mechanism of ATP hydrolysis by pea chloroplast F1-ATPase. Photosynthetica56(4), 1365-1369. doi: 10.1007/s11099-018-0840-6.
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References

  1. Abrahams J.P., Leslie A.G., Lutter R., Walker J.E.: Structure at 2.8A resolution of F1-ATPase from bovine heart mitochondria.-Nature 370: 621-628, 1994. Go to original source...
  2. Asada K.: Radical production and scavenging in the chloroplasts.-In: Baker N.R. (ed.): Photosynthesis and the Environment. Pp. 123-150. Kluwer Acad. Publ., Dordrecht-Boston-London 2004. Go to original source...
  3. Asadi M.: Beet-Sugar Handbook, Table A12, Viscosity of Pure Sucrose Solutions. Retrieved from: https://doi.org/www.wiley.com/doi/10.1002/9780471790990.cth1/pdf, 2005.
  4. Barbier G.G., Campbell W.H.: Viscosity effects on eucaryotic nitrate reductase activity.-J. Biol. Chem. 280: 26049-26054, 2005. Go to original source...
  5. Binder A., Jagendorf A., Ngo E.: Isolation and composition of the subunits of spinach chloroplast coupling factor protein.-J. Biol. Chem. 253: 3094-3100, 1978.
  6. Bradford M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.-Anal. Biochem. 72: 248-254, 1976. Go to original source...
  7. Chapman B., Loiselle D.: Thermodynamics and kinetics of the FoF1 ATPase: application of the probability isotherm.-R. Soc. Open Sci. 3: 150379, 2016. Go to original source...
  8. Ellis R.: The most abundant protein in the world.-Trends Biochem. Sci. 4: 241-244, 1979. Go to original source...
  9. Itoh H., Takahashi A., Adachi K. et al.: Mechanically driven ATP synthesis by F1-ATPase.-Nature 427: 465-468, 2004. Go to original source...
  10. Kartashov I.M., Opanasenko V.K., Malyan A.N.: [Effects of medium viscosity agents on ATP synthesis in chloroplast thylakoids.]-Biofizika 60: 481-486, 2015. [In Russian]
  11. Khoshtariya D.E., Goguadze N.G.: [Influence of the medium viscosity on the activity of myosin ATPase.]-Biofizika 31: 220-222, 1986. [In Russian]
  12. Kinosita K. Jr., Yasuda R., Noji H., Adachi K.: A rotary molecular motor that can work at near 100% efficiency.-Philos. T. Roy. Soc. B 355: 473-489, 2000. Go to original source...
  13. Konno H., Nakane T., Yoshida M. et al.: Thiol modulation of the chloroplast ATP synthase is dependent on the energization.-Plant Cell Physiol. 53: 626-634, 2012. Go to original source...
  14. Kramers H.A.: Brownian motion in a field of force and the diffusion model of chemical reactions.-Physica 7: 284-304, 1940. Go to original source...
  15. Kulish O., Wright A.D., Terentjev E.M.: F1 rotary motor of ATP synthase is driven by the torsionally asymmetric drive shaft.-Sci. Rep. 6: 28180, 2016. Go to original source...
  16. Malyan A.N.: The effect of medium viscosity on kinetics of ATP hydrolysis by the chloroplast coupling factor CF1.-Photosynth. Res. 128: 163-168, 2016. Go to original source...
  17. Martin J.L., Ishmukhametov R., Hornung T. et al.: Anatomy of F1-ATPase powered rotation.-P. Natl. Acad. Sci. USA 111: 3715-3720, 2014. Go to original source...
  18. Nakanishi-Matsui M., Sekiya M., Futai M.: ATP synthase from Escherichia coli: Mechanism of rotational catalysis, and inhibition with the e-subunit and phytopolyphenols.-Biochim. Biophys. Acta 1857: 129-140, 2016.
  19. Nalin C.M., McCarty R.E.: Role of a disulfide bond in the gamma subunit in activation of the ATPase of chloroplast coupling fator 1.-J. Biol. Chem. 159: 7275-7280, 1984.
  20. Noji H., Ueno H., McMillan D.G.G.: Catalytic robustness and torque generation of the F1-ATPase.-Biophys. Rev. 9: 103-118, 2017. Go to original source...
  21. Puchkov E.O.: Intracellular viscosity: methods of measurement and role in metabolism.-Biochemistry-Moscow+ 7: 270-279, 2013. Go to original source...
  22. Sampedro J., Uribe S.: Trehalose-enzyme interactions result in structure stabilization and activity inhibition. The role of viscosity.-Mol. Cell Biochem. 256-257: 319-327, 2004. Go to original source...
  23. Sashi P., Bhuyan A.K.: Viscosity dependence of some protein and enzyme reaction rates: seventy-five years after Kramers.-Biochemistry 54: 4453-4461, 2015. Go to original source...
  24. Sitnitsky A.E.: Model for solvent viscosity effect on enzymatic reactions.-Chem.. Phys. 369: 37-42, 2010.
  25. Soga N., Kimura K., Kinosita K.Jr. et al.: Perfect chemomechanical coupling of FoF1-ATP synthase.-P. Natl. Acad. Sci. USA 114: 4960-4965, 2017. Go to original source...
  26. Spetzler D., Ishmukhametov R., Hornung T. et al.: Single molecule measurements of F1-ATPase reveal an interdependence between the power stroke and the dwell duration.-Biochemistry 48: 7979-7985, 2009. Go to original source...
  27. Toyabe S., Watanabe-Nakayama T., Okamoto T. et al.: Thermodynamic efficiency and mechanochemical coupling of F1-ATPase.-P. Natl. Acad. Sci. USA 108: 17951-17956, 2011. Go to original source...
  28. Uribe S., Sampedro J.G.: Measuring solution viscosity and its effect on enzyme activity.-Biol. Proced. Online 5: 108-115, 2003. Go to original source...
  29. Wayne R.O.: Plant Cell Biology: from Astronomy to Zoology. Elsevier, Dordrecht-Boston-London 2009.
  30. Yasuda R., Noji H., Kinosita K.Jr., Yoshida M.: F1-ATPase is a highly efficient molecular motor that rotates with discrete 120° steps.-Cell 93: 1117-1124, 1998. Go to original source...