Advertisement

Statistical Mechanical Integral Equation Approach to Reveal the Solvation Effect on Hydrolysis Free Energy of ATP and Its Analogue

  • Norio Yoshida
  • Fumio Hirata
Chapter

Abstract

Investigations of the hydrolysis reactions of adenosine triphosphate (ATP) and pyrophosphate in solution by the three-dimensional reference interaction site model self-consistent field (3D-RISM-SCF) theory are briefly reviewed. The theory is applied to the four different charged states of pyrophosphate, for which experimental data of hydrolysis free energies are available. The results of the reaction free energy for all the four charged states are almost constant, ~−8 kcal/mol, in accord with the experimental results, but in marked contrast to the conventional view, or the high-energy PO bond hypothesis. The theory is also applied to the hydrolysis reaction of ATP to clarify the molecular origin of the energy produced by the ATP hydrolysis.

Keywords

3D-RISM-SCF ATP hydrolysis Pyrophosphate 

References

  1. Akola J, Jones R (2003) Atp hydrolysis in water—a density functional study. J Phys Chem B 107(42):11774–11783CrossRefGoogle Scholar
  2. Andersen H, Chandler D (1972) Optimized cluster expansions for classical fluids. 1. General theory and variational formulation of mean spherical model and hard-sphere percus-yevick equations. J Chem Phys 57(5):1918–1929CrossRefGoogle Scholar
  3. Andersen H, Chandler D, Weeks J (1972) Optimized cluster expansions for classical fluids. 3. Applications to ionic solutions and simple liquids. J Chem Phys 57(7):2626–2631CrossRefGoogle Scholar
  4. Aqvist J, Warshel A (1993) Simulation of enzyme-reactions using valence-bond force-fields and other hybrid quantum-classical approaches. Chem Rev 93(7):2523–2544CrossRefGoogle Scholar
  5. Beglov D, Roux B (1996) Solvation of complex molecules in a polar liquid: an integral equation theory. J Chem Phys 104(21):8678–8689CrossRefGoogle Scholar
  6. Beglov D, Roux B (1997) An integral equation to describe the solvation of polar molecules in liquid water. J Phys Chem B 101(39):7821–7826CrossRefGoogle Scholar
  7. Boyd DB, Lipscomb WN (1969) Electronic structures for energy-rich phosphates. J Theor Biol 25(3):403–420CrossRefGoogle Scholar
  8. Chandler D, Andersen HC (1972) Optimized cluster expansions for classical fluids. 2. Theory of molecular liquids. J Chem Phys 57(5):1930–1937CrossRefGoogle Scholar
  9. Colvin M, Evleth E, Akacem Y (1995) Quantum-chemical studies of pyrophosphate hydrolysis. J Am Chem Soc 117(15):4357–4362CrossRefGoogle Scholar
  10. Field MJ, Bash PA, Karplus M (1990) A combined quantum-mechanical and molecular mechanical potential for molecular-dynamics simulations. J Comput Chem 11(6):700–733CrossRefGoogle Scholar
  11. Gao JL, Xia XF (1992) A priori evaluation of aqueous polarization effects through monte-carlo qm-mm simulations. Science 258(5082):631–635CrossRefGoogle Scholar
  12. George P, Witonsky RJ, Trachtma M, Wu C, Dorwart W, Richman L, Richman W, Shurayh F, Lentz B (1970) Squiggle-H2O—an enquiry into importance of solvation effects in phosphate ester and anhydride reactions. Biochim Biophys Acta 223(1):1–15CrossRefGoogle Scholar
  13. Grigorenko BL, Rogov AV, Nemukhin AV (2006) Mechanism of triphosphate hydrolysis in aqueous solution: QM/MM simulations in water clusters. J Phys Chem B 110(9):4407–4412CrossRefGoogle Scholar
  14. Hammond C, Kartenbeck J, Helenius A (1992) Effects of dithiothreitol on beta-cop distribution and golgi to er membrane traffic. Mol Biol Cell 3:A35–A35Google Scholar
  15. Hansen JP, McDonald IR (2006) Theory of simple liquids. Academic Press, AmsterdamGoogle Scholar
  16. Hill TL, Morales MF (1951) On high energy phosphate bonds of biochemical interest. J Am Chem Soc 73(4):1656–1660CrossRefGoogle Scholar
  17. Hirata F (2003) Molecular theory of solvation. Kluwer, DordrechtGoogle Scholar
  18. Hofmann KP, Zundel G (1974) Large hydration structure changes on hydrolyzing atp. Experientia 30(2):139–140CrossRefGoogle Scholar
  19. Hong J, Yoshida N, Chong S-H, Lee C, Ham S, Hirata F (2012) Elucidating the molecular origin of hydrolysis energy of pyrophosphate in water. J Chem Theory Comput 8:2239–2246CrossRefGoogle Scholar
  20. Kamerlin SCL, Warshel A (2009) On the energetics of atp hydrolysis in solution. J Phys Chem B 113(47):15692–15698CrossRefGoogle Scholar
  21. Kido K, Kasahara K, Yokogawa D, Sato H (2015) A hybrid framework of first principles molecular orbital calculations and a three-dimensional integral equation theory for molecular liquids: Multi-center molecular ornstein-zernike self-consistent field approach. J Chem Phys 143(1):014103CrossRefGoogle Scholar
  22. Klaehn M, Rosta E, Warshel A (2006) On the mechanism of hydrolysis of phosphate monoesters dianions in solutions and proteins. J Am Chem Soc 128(47):15310–15323CrossRefGoogle Scholar
  23. Kovalenko A, Hirata F (1998) Three-dimensional density profiles of water in contact with a solute of arbitrary shape: a RISM approach. Chem Phys Lett 290(1–3):237–244CrossRefGoogle Scholar
  24. Kovalenko A, Hirata F (1999) Self-consistent description of a metal-water interface by the kohn-sham density functional theory and the three-dimensional reference interaction site model. J Chem Phys 110(20):10095–10112CrossRefGoogle Scholar
  25. Kovalenko A, Hirata F (2001) First-principles realization of a van der waals-maxwell theory for water. Chem Phys Lett 349(5–6):496–502CrossRefGoogle Scholar
  26. Lipmann F (1941) Metabolic generation and utilization of phosphate bond energy. Adv Enzymol Rel S Bi 1:99–162Google Scholar
  27. Maruyama Y, Yoshida N, Tadano H, Takahashi D, Sato M, Hirata F (2014) Massively parallel implementation of 3D-RISM calculation with volumetric 3D-FFT. J Comput Chem 35(18):1347–1355CrossRefGoogle Scholar
  28. Meyerhof O, Lohmann K (1932) Energetic exchange connections amongst the volume of phosphoric acetic acid in muscle extracts. Biochem Z 253:431–461Google Scholar
  29. Nishihara S, Otani M (2017) Hybrid solvation models for bulk, interface, and membrane: reference interaction site methods coupled with density functional theory. Phys Rev B 96(11)Google Scholar
  30. Sato H (2013) A modern solvation theory: quantum chemistry and statistical chemistry. Phys Chem Chem Phys 15(20):7450–7465CrossRefGoogle Scholar
  31. Sato H, Kovalenko A, Hirata F (2000) Self-consistent field, ab initio molecular orbital and three-dimensional reference interaction site model study for solvation effect on carbon monoxide in aqueous solution. J Chem Phys 112(21):9463–9468CrossRefGoogle Scholar
  32. Sinnecker S, Rajendran A, Klamt A, Diedenhofen M, Neese F (2006) Calculation of solvent shifts on electronic g-tensors with the conductor-like screening model (COSMO) and its self-consistent generalization to real solvents (direct COSMO-RS). J Phys Chem A 110(6):2235–2245CrossRefGoogle Scholar
  33. Takahashi H, Kawashima Y, Nitta T, Matubayasi N (2005) A novel quantum mechanical/molecular mechanical approach to the free energy calculation for isomerization of glycine in aqueous solution. J Chem Phys 123(12):124504CrossRefGoogle Scholar
  34. Takahashi H, Matubayasi N, Nakahara M, Nitta T (2004) A quantum chemical approach to the free energy calculations in condensed systems: the QM/MM method combined with the theory of energy representation. J Chem Phys 121(9):3989–3999CrossRefGoogle Scholar
  35. Takahashi H, Umino S, Miki Y, Ishizuka R, Maeda S, Morita A, Suzuki M, Matubayasi N (2017) Drastic compensation of electronic and solvation effects on atp hydrolysis revealed through large-scale QM/MM simulations combined with a theory of solutions. J Phys Chem B 121(10):2279–2287CrossRefGoogle Scholar
  36. Ten-no S, Hirata F, Kato S (1993) A hybrid approach for the solvent effect on the electronic-structure of a solute based on the RISM and hartree-fock equations. Chem Phys Lett 214(3–4):391–396CrossRefGoogle Scholar
  37. Ten-no S, Hirata F, Kato S (1994) Reference interaction site model self-consistent-field study for solvation effect on carbonyl-compounds in aqueous-solution. J Chem Phys 100(10):7443–7453CrossRefGoogle Scholar
  38. Tomasi J, Mennucci B, Cammi R (2005) Quantum mechanical continuum solvation models. Chem Rev 105(8):2999–3093CrossRefGoogle Scholar
  39. Tomasi J, Persico M (1994) Molecular-interactions in solution—an overview of methods based on continuous distributions of the solvent. Chem Rev 94(7):2027–2094CrossRefGoogle Scholar
  40. Vinothkumar KR, Montgomery MG, Liu S, Walker JE (2016) Structure of the mitochondrial atp synthase from pichia angusta determined by electron cryo-microscopy. Proc Nat Acad Sci USA 113(45):12709–12714CrossRefGoogle Scholar
  41. Wang C, Huang WT, Liao JL (2015) QM/MM investigation of atp hydrolysis in aqueous solution. J Phys Chem B 119(9):3720–3726CrossRefGoogle Scholar
  42. Yamamoto T (2010) Preferred dissociative mechanism of phosphate monoester hydrolysis in low dielectric environments. Chem Phys Lett 500(4–6):263–266CrossRefGoogle Scholar
  43. Yokogawa D, Sato H, Sakaki S (2007) New generation of the reference interaction site model self-consistent field method: introduction of spatial electron density distribution to the solvation theory. J Chem Phys 126(24):244504CrossRefGoogle Scholar
  44. Yoshida N (2014) Efficient implementation of the three-dimensional reference interaction site model method in the fragment molecular orbital method. J Chem Phys 140(21):214118CrossRefGoogle Scholar
  45. Yoshida N, Imai T, Phongphanphanee S, Kovalenko A, Hirata F (2009) Molecular recognition in biomolecules studied by statistical-mechanical integral-equation theory of liquids. J Phys Chem B 113(4):873–886CrossRefGoogle Scholar
  46. Yoshida N, Kato S (2000) Molecular ornstein-zernike approach to the solvent effects on solute electronic structures in solution. J Chem Phys 113(12):4974–4984CrossRefGoogle Scholar
  47. Yoshida N, Kiyota Y, Hirata F (2011) The electronic-structure theory of a large-molecular system in solution: application to the intercalation of proflavine with solvated dna. J Mol Liq 159(1):83–92CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Graduate School of Science, Department of ChemistryKyushu UniversityFukuokaJapan
  2. 2.Toyota Physical & Chemical Research InstituteNagakute, AichiJapan

Personalised recommendations