A Solvent Model of Nucleotide–Protein Interaction—Partition Coefficients of Phosphates Between Water and Organic Solvent

Chapter

Abstract

In attempt to experimentally evaluate hydration/solvation of phosphoric compounds in aqueous solution, partitioning of phosphoric compounds from an aqueous solution to an organic solvent has been quantified. Transfer of phosphates from an aqueous solution into octanol was greatly enhanced by addition of alkylamine as an amphiphilic extractant. This alkylamine/octanol system exhibited amine basicity, and thus the pH of solution was controlled by equilibration with buffer. Further, enthalpy changes of the transfers of ATP and ADP from water to the alkylamine/octanol were estimated from van’t Hoff analysis, and these enthalpy changes depended on ionization enthalpy of buffer. This result suggests that the transfers are accompanied with protonation of phosphoric ions and deprotonation of alkylamine. Finally, the partition coefficients of ATP, ADP, AMP, and Pi were estimated under the pH-controlled condition at 25 °C. The partition coefficients depended on the pH of aqueous phase and the net charge of phosphoric compounds. Therefore, the transfer is likely to be determined by electrostatic interaction between phosphoric ion and amine. The solvent system with a nucleotide-uptake capacity may partly mimic the function of ATP-binding proteins.

Keywords

Partition coefficient Phosphoric compound Octanol Alkylamine Amphiphilic extractant 

6.1 Introduction

ATP hydrolysis is an important exergonic reaction providing the Gibbs free energy for thermodynamically unfavorable, endergonic reactions in living systems. In addition to the resonance stabilization of a phosphoanhydride bond and the electrostatic repulsions between a charged phosphoanhydride groups, the difference of solvation energies between ATP and products (ADP and Pi) has been presumed to provide the thermodynamic driving force for the ATP hydrolysis. This explanation was originally proposed by George et al. (1970) and then appeared in a biochemistry textbook (Voet et al. 2013). This presumption has been supported by experimental results by de Meis (1984), de Meis et al. (1985), Remero and de Meis (1989). They reported that the favorable free energy of pyrophosphate (PPi) hydrolysis was greatly reduced by the decrease in the water activity by adding cosolvents (glycerol, ethylene glycol, polyethylene glycol, and dimethyl sulfoxide) to the reaction medium, indicating a large contribution of solvation for free energy of hydrolysis. In addition, the favorable Gibbs energy change for hydrolysis step of enzyme-bound PPi is much less than that in water (Springs et al. 1981). The favorable Gibbs energy of ATP hydrolysis step on myosin is also dramatically decreased compared to that in water (Bagshaw and Trentham 1974; Kodama and Woledge 1979). These decreases of hydrolysis energy on enzyme may be attributed to the waterless environment surrounded by alkyl and aromatic side chains of the enzyme proteins.

Because transfer process of phosphoric compounds from aqueous solution to organic solvent involves the dehydration of the phosphoric compounds, the partitioning of phosphoric compounds between aqueous solution and organic solvent can be used as an indicator of the hydration energies of phosphoric compounds. An experimental assessment by partition coefficient of phosphoric compounds between aqueous solution and organic solvent was proposed by Wolfenden and Williams (1985) and was used for estimation of free energy of hydrolysis of phosphoric anhydrides in organic solvent (i.e., wet chloroform). Stockbridge and Wolfenden also estimated distribution coefficients of phosphoric compounds from water to organic solvent to investigate hydrolysis kinetics in water-saturated organic solvent (Stockbridge and Wolfenden 2009, 2010). The distribution coefficient for neopentyl phosphate and dineopentyl phosphate from water to cyclohexane in the presence of excess tetrabutylammonium was 7.0 × 10−6 and 3.9 × 10−5 at 25 °C, respectively. In addition, sodium pyrophosphate was saturated at 2 × 10−4 M in ~1% (v/v) water-contained dimethyl sulfoxide (Stockbridge and Wolfenden 2011). Thus, only slight amount of phosphoric compounds transfers from water to organic solvent, due to the high polarity of phosphate group. These low ratios of partition make it difficult to precisely estimate partition coefficients of phosphoric compounds from water and organic solvent, because extraordinarily low amount of compounds in organic solvent should be quantified.

To overcome the difficulty, amphiphilic extractants were dissolved in organic solvent, which enhance the transfer of phosphoric compounds from water to organic solvent and increase the change in concentration by partition. Phosphoric ions are probably present as their salts of amphiphilic ions in organic solvent. Such a solvent system contains the amphiphilic ions in hydrophobic alkyl chains of the organic solvent, and thus it is similar to the waterless environment on the enzyme protein. The transfer of phosphoric compounds from water to organic solvent can be regarded as a model of interaction between protein and phosphoric compounds. Such an organic solvent/amphiphilic extractant system has been developed to extract phosphoric compounds such as nucleotides from aqueous solutions by use of alkylamine as an amphiphilic extractant. In this chapter, partition of nucleotides and phosphate from water to organic solvent/amphiphilic extractant is illustrated.

6.2 Measurement of Partition Coefficients of Phosphoric Compounds Between Water and Alkylamine/Octanol

One volume of aqueous solutions containing ATP, ADP, AMP, or Pi was mixed into one volume of organic solvents and placed at 25 °C for 2–3 h. After the organic phase was removed, the concentration of solute in the aqueous phase was assayed. Concentrations of nucleotides (ATP, ADP, and AMP) were determined by absorbance at 260 nm, and concentration of Pi was determined by Malachite Green method (Kodama et al. 1986). Notably, when ATP concentration was lower than ~10−6 M due to the high partition coefficient, ATP concentration in aqueous phase was determined by a luciferin–luciferase assay. Amount of solute transferred to organic solvent was estimated by subtracting the amount of solute in aqueous phase from the total amount. Partition coefficient (KP) was estimated from ratio of concentration of solute transferred into organic solvents (cO) to that of retained in aqueous solution (cW) as follows.
$$ K_{p} = \frac{{c_{o} }}{{c_{w} }} $$
(6.1)

6.3 Enhancement of Transfer of Phosphoric Compounds from Water to Organic Solvent by Alkylamine

6.3.1 Effect of Alkylamine on Partition of Phosphoric Compounds from Water to Organic Solvent

More than 60 years ago, alkylamine was used as extractants for solvent extraction of phosphoric compounds from aqueous solution or biological materials (Plaut et al. 1950). According to this report, the partition coefficients of pyrophosphate and ATP between water and octadecylamine-dissolved n-octanol were more than 40. In search of better solvent/extractant system for quantitative estimation of partition coefficients, octadecylamine and hexadecylamine were dissolved in higher alcohols (n-butanol, n-pentanol, n-hexanol, and n-octanol) and the alkylamine/alcohol solvents were tested for the transfers of ATP, ADP, and Pi under pH-uncontrolled condition in comparison with chloroform (Fig. 6.1). The results show that octadecylamine and hexadecylamine markedly increased the transfer of ATP, ADP, and Pi from water to the organic solvent. The increases in the transfer by hexadecylamine were higher than those by octadecylamine. Note that the water contents in water-saturated octanol were determined by using Karl Fischer moisture meters and were ca. 3.5% both in the absence and presence of alkylamine.
Fig. 6.1

Effect of alkylamine on transfer of phosphoric compounds (ATP, ADP, and Pi) to organic solvent, a ATP, b ADP, c Pi. Solvent saturated by water (green bars), solvent containing octadecylamine (blue bars), solvent containing hexadecylamine (light blue bars). Transfer of ATP, ADP, and Pi was tested for chloroform, butanol, pentanol, hexanol, and octanol in the absence and presence of 5% (w/v) octadecylamine or 5% (w/v) hexadecylamine. The pH of solutions was not controlled. One volume of aqueous solutions containing ATP, ADP, or Pi was mixed into one volume of organic solvents. The samples were placed at 25 °C for ca. 90 min, and the organic phases then were removed. Concentrations of ATP, ADP, and Pi in aqueous phase were determined as described in 6.2. Amount of solute transferred to organic solvent was estimated by subtracting the amount of solute in aqueous phase from the total amount

Figure 6.2 shows the effect of hexadecylamine concentration on the amounts of transferred solutes from water to hexadecylamine/octanol system at pH 8.5. The transfers of ATP and ADP apparently increased with concentration of hexadecylamine, and ATP was more transferred than ADP. Transfers of AMP and Pi were not observed in this condition, due to their low partition coefficients at pH 8.5.
Fig. 6.2

Effect of hexadecylamine on the transfer of ATP (red circles), ADP (blue circles), AMP (green circles), and Pi (open circles) from aqueous solution (200 mM bicine–NaOH pH 8.5) to octanol. The initial concentration of each solute in aqueous solution was 100 mM

6.3.2 Homogenous Dispersion of Phosphoric Compounds in Alkylamine-Containing Organic Solvent

To determine whether phosphoric compounds adsorb on the water/octanol surface or absorb into hexadecylamine-containing octanol, fluorescent ATP analogue, 2′-(or 3′)-O-(N-methylanthraniloyl) ATP (mant-ATP), was used as a solute and its localization was visualized under UV light. As shown in Fig. 6.3, fluorescence was observed in the whole hexadecylamine-containing octanol, and therefore mant-ATP was homogeneously dispersed in the solvent.
Fig. 6.3

Partitioning of fluorescent ATP analogue (mant-ATP) from aqueous to organic solvents. Mant-ATP (500 μM) was visualized under UV light

Possibility of association of solute molecules in the organic solvent was checked by the partitioning across a wide range of solute concentrations. The concentrations of transferred phosphoric compounds to the solvent were plotted against those of remained solutes in water (Fig. 6.4). The linearities with slope of approximately 1 for ATP, ADP, and Pi suggest that association of solute does not occur in the organic solvent.
Fig. 6.4

Partitioning between water and octadecylamine/octanol of ATP (red circles), ADP (blue circles), and Pi (open circles) at various solute concentrations. cO: solute concentration transferred into organic solvents. cW: solute concentration retained in aqueous solution

6.4 Acid/Base Properties of Alkylamine-Containing Octanol Solvent System

Phosphate exists as four ionic forms depending on pH. On the other hand, alkylamine is base, and thus the pH of aqueous solution becomes basic. Therefore, pH of solution should be controlled for the accurate evaluation of the partitioning. In this section, acid/base properties of alkyl amine/octanol system are described.

6.4.1 Acid/Base Properties and pH Control of Alkylamine-Containing Octanol

The octadecylamine/octanol was titrated with HCl/isopropanol (Fig. 6.5). The titration curve indicated its basicity with a pKa of 9.3. In fact, after mixing with alkylamine/octanol, the pH of aqueous solution (20 mM MOPS–NaOH, pH 7.0) increased to 8.5. The protonation of alkylamine appears to decrease H+ concentration of aqueous solution.
Fig. 6.5

pH titration curve of alkylamine in octanol. The octadecylamine/octanol was titrated with HCl/isopropanol. The pH was measured by using 6377-10D pH electrode (HORIBA) which is sensitive to low conductivity water and non-aqueous solvents. The pKa was estimated as 9.3

In order to stabilize the pH of solution, alkylamine-containing octanol was equilibrated with buffer several times until pH became constant. Briefly, alkylamine was first dissolved in octanol at 100 mM and then mixed with equivalent volume of water. After liquid–liquid phase separation, the lower aqueous phase was discarded. This mixing–separating cycle was repeated three times to be saturated with water. Similarly, the water-saturated alkylamine/octanol was equilibrated with buffer solution by repeating mixing–separating cycle (mixing with buffer, liquid–liquid phase separation, and discarding the aqueous solution) until pH of aqueous phase was constant.

6.4.2 Thermodynamic Analysis of the Protonation/Deprotonation Accompanying Transfer of Phosphoric Compounds Form Water to Alkylamine/Octanol

Due to the basicity of alkylamine as described above, the transfer of phosphoric ions from water to the alkylamine/octanol may be involved in protonation of phosphoric ions and deprotonation of alkylamine. To investigate this possibility, van’t Hoff enthalpies of phosphoric ion transfer were roughly estimated in the buffers with varying deprotonation enthalpy. If the transfer entails the uptake and release of proton, the observed van’t Hoff enthalpy (ΔHVH, obs) should be dependent on the ionization enthalpy of buffer (ΔHi) (Eq. 6.2)
$$ \Delta H_{\text{VH, obs}} { = }\Delta H_{ 0} + n\Delta H_{\text{i}} $$
(6.2)
where ΔH0 is the intrinsic transfer enthalpy and n is the number of proton uptake to buffer.
The KP values of ATP and ADP from water to hexadecylamine/octanol were measured at 20–40 °C in four different kinds of buffer solution (Fig. 6.6). Significance difference of KP values between the buffers was not observed. On the other hand, the slopes of van’t Hoff plots (reciprocal temperature versus lnKP) were different in the buffers. The van’t Hoff enthalpy (ΔHVH, obs) was estimated by Eq 6.3 and plotted against deprotonation enthalpy of buffer (Fig. 6.7)
Fig. 6.6

van’t Hoff analysis of the partitioning of ATP (red circles) and ADP (blue circles) from water to hexadecylamine/octanol at 20–40 °C in four different buffer solutions, a bicine–NaOH, b tricine–NaOH, c TAPS–NaOH, d Tris-HCl. The ionization enthalpies of buffer were obtained from Goldberg et al. (2002)

Fig. 6.7

Relationship between ionization enthalpy of buffer and van’t Hoff enthalpy of the partitioning of ATP (red circles) and ADP (blue circles) from water to hexadecylamine/octanol. The data points of ATP and ADP are overlapped at 47.5 kJ/mol of ΔHi

$$ \Delta H_{\text{VH, obs}} { = } - R\left[ {\frac{{\Delta \ln K_{\text{P}} }}{{\Delta \left( {1/T} \right)}}} \right] $$
(6.3)
where R is the gas constant and T is the temperature. The plots show that the observed van’t Hoff enthalpies roughly linearly related to the buffer deprotonation enthalpy with reasonable values of slope (n) (2.18 for ATP and 1.96 for ADP). Therefore, the transfers of ATP and ADP from water to the alkylamine/octanol are probably accompanied with protonation of phosphoric ion and deprotonation of alkylamine. In the case of ATP transfer at pH 8.3, protonated alkylamine molecules (RNH3+) in organic phase donate one or more protons to ATP4− in aqueous phase, and ATP is transferred to organic phase as protonated ATP (ATP·nH(4−n)−)
$$ {\text{ATP}}^{ 4- } \left( {\text{aq}} \right) + n\,{\text{RNH}}_{3}^{ + } \left( {\text{or}} \right) \rightleftharpoons {\text{ATP}}\, \bullet \,n{\text{H}}^{{\left( { 4 { - }n} \right){- }}} \left( {\text{or}} \right) + n\,{\text{RNH}}_{ 2} \left( {\text{or}} \right) $$
(6.4)
The protonation and deprotonation of alkylamine and buffer were balanced at the equilibrium (see Sect. 6.4.1), and the ionization enthalpy of buffer (ΔHi) appeared to come from this reaction.
$$ {\text{RNH}}_{ 2} \left( {\text{or}} \right) + {\text{buffer}}\,\bullet\,{\text{H }}\left( {\text{aq}} \right)\, \rightleftharpoons \,{\text{RNH}}_{ 3}^{ + } \left( {\text{or}} \right) + {\text{buffer}}^{ - } \left( {\text{aq}} \right) $$
(6.5)

6.5 Partition Coefficients of Phosphoric Compounds Between Aqueous Solution and Organic Solvent

Taking into account the properties of alkylamine/octanol system mentioned above, the KP values of ATP, ADP, AMP, and Pi from aqueous to the organic phases were measured in the carefully controlled condition. These KP values and the transfer energies (ΔGtr = −RTlnKP) varied by pH of solution and net charges of phosphoric compounds (Table 6.1). The KP values at pH 7.2 were approximately 30- to 50-fold larger than those of pH 8.3, and the KP value for ATP was comparable to those of submillimolar dissociation constant for protein–ligand interaction. Because the alkylamine with a pKa of 9.3 is more protonated at lower pH, the protonation of alkylamine seems to be crucial to interact with the phosphate ions and to transfer the phosphate ions to the organic phase.
Table 6.1

Partition coefficients and transfer energies of ATP, ADP, AMP, and Pi from aqueous to organic phases

pH

Solute

Net charge

K P

\({\Delta G_{tr}}\) a

kJ·mol−1

8.3

ATP

−4

84.9

−11.0

ADP

−3

13.3

−6.41

AMP

−2

0.473

1.85

Pi

−2

0.623

1.17

7.2

ATP

−3.5

3010

−19.8

ADP

−2.5

440

−15.1

AMP

−1.5

24.4

−7.91

Pi

−1.5

30.9

−8.50

aΔGtr = −RTlnKP

In addition, the rank order of the KP was ATP > ADP > AMP ≈ Pi, in the order of the number of phosphate group both at pH 8.3 and 7.2. Four ionic forms of phosphate depend on pH, and their net charges are reasonably pH-dependent. Thus, the ΔGtr values for each compound were plotted as a function of the net charge (Fig. 6.8). The ΔGtr values were more favorable with increasing the net charge both at pH 8.3 and 7.2, indicating that the negative charge of phosphoric compounds is an important factor for the transfer.
Fig. 6.8

Plot of transfer energy as function of net charge of phosphoric compound in aqueous solution at pH 7.2 (open circles) and pH 8.3 (closed circles)

Taken together, the electrostatic interaction is likely to be dominant driving force for transfer from aqueous to organic phases. The ΔGtr values at pH 7.2 are substantially more favorable than those at pH 8.3. Thus, the protonation of alkylamine is probably more critical for the transfer than net charge of phosphoric compounds.

6.6 Discussion and Conclusion

Because the transfers of phosphoric compounds from water to the alkylamine/octanol are involved in the electrostatic interaction, the ΔGtr values are considered to include not only solvation energy but also electrostatic energy between alkylamine and phosphate. Thus, the ΔGtr values should not be interpreted as simple solvation energies of phosphoric compounds. Experimental separation of these two energies is difficult, and evolved strategies are needed to devise. On the other hand, in the recent QM/MM simulation of ATP and PPi hydrolysis, the solvation energies of phosphoric compounds are distinguished from the electronic energies (Takahashi et al. 2017).

In spite of such difficulty in the interpretation of the ΔGtr values, the difference of the transfer energy between ATP and its hydrolyzing products (ADP and Pi) (ΔΔGtr) was estimated (Eq. 6.6).
$$ \Delta \Delta G_{\text{tr}} { = (}\Delta G_{\text{tr, ADP}} + \Delta G_{\text{tr, Pi}} ) - \Delta G_{\text{tr, ATP}} $$
(6.6)
where ΔGtr,ATP, ΔGtr,ADP, and ΔGtr,Pi are the transfer energies of ATP, ADP, and Pi, respectively. The ΔΔGtr were estimated as 3.8 kJ·mol−1 at pH 7.2 and −5.8 kJ·mol−1 at pH 8.3. These values seem to be considerably smaller than the Gibbs energy of ATP hydrolysis in biological standard state (~−30 kJ·mol−1) (Alberty and Goldberg 1992). The free energy of ATP hydrolysis may not be explained by the difference of solubility to alkylamine-containing organic solvent between ATP and its hydrolyzing products. This interpretation appears to differ from the result that the free energy of PPi hydrolysis was drastically decreased with deceasing water activity (concentration) by adding cosolvents (de Meis 1984; de Meis et al. 1985; Remero and de Meis 1989). However, the free energy of hydrolysis of phosphoric compounds is highly sensitive to pH, magnesium ion concentration, and ion strength (Alberty and Goldberg 1992). Therefore, the difference in these conditions between the previous literature and this study should be taken into consideration and be carefully examined.

The binding of nucleotide to myosin is known to be associated with liberation of protons in the presence of magnesium ion (Bagshaw and Trentham 1974; Chock and Eisenberg 1974; Koretz and Taylor 1975; Kodama 1981). In contrast, in the absence of divalent cations, the ADP-binding of myosin was accompanied with absorption of protons (Kardami et al. 1979). This report indicated that the protonation of alkylamine accompanied the transfers of ATP and ADP from water to alkylamine/octanol solvent system in the absence of divalent cation (see Sect. 6.4.2). Thus, this solvent system could mimic the nucleotide-binding-induced proton absorption of myosin in the absence of divalent cation. Τhe standard Gibbs energy of deprotonated ATP hydrolysis is positively small (3.0 kJ·mol−1) and much larger than that of protonated ATP (−36 kJ·mol−1) (Alberty and Goldberg 1992). At present, the proton of ATPase-bound nucleotide cannot be visualized in crystal structures. Thus, analysis of the protonation/deprotonation state of ATPase-bound nucleotide (e.g., a neutron diffraction analysis) is necessary to discuss energetics of ATP hydrolysis.

From a viewpoint of applied research, the alkylamine/octanol solvent system could be applied to an extraction of phosphoric compounds from polluted water and to a reaction solvent of phosphoric compound. In fact, extractions of metal ions from an aqueous solution into an organic solvent with an amphiphilic extractant are useful in applications to environmental and industrial fields (Jiang and Jia 2008; Chen et al. 2009; Ellis et al. 2012; Bu et al. 2014; Pal et al. 2015).

In conclusion, this study has successfully measured the partition coefficients of phosphoric compounds between aqueous solution and organic solvent (octanol) by employing alkylamine as amphiphilic extractants in the pH-controlled condition. The transfer of phosphoric compounds is mainly driven by the electrostatic interaction between phosphoric compounds and alkylamine. This solvent system contains the amphiphilic ions in hydrophobic alkyl chains like proteins and exhibits the high uptake capacity for phosphoric compounds and the nucleotide-transfer-induced deprotonation. Thus, the solvent may partly mimic the nucleotide-binding function of ATPase enzymes. Further improvement of solvent system may be helpful for examining the solvation energy of phosphoric compound and in future applying to environmental and/or industrial fields.

References

  1. Alberty RA, Goldberg RN (1992) Standard thermodynamic formation properties for the adenosine 5′-triphosphate series. Biochemistry 31(43):10610–10615CrossRefGoogle Scholar
  2. Bagshaw CR, Trentham DR (1974) The characterization of myosin-product complexes and of product-release steps during the magnesium ion-dependent adenosine triphosphatase reaction. Biochem J 141(2):331–349CrossRefGoogle Scholar
  3. Bu W, Yu H, Luo G, Bera MK, Hou B, Schuman AW, Lin B, Meron M, Kuzmenko I, Antonio MR, Soderholm L, Schlossman ML (2014) Observation of a rare earth Ion−extractant complex arrested at the oil−water interface during solvent extraction. J Phys Chem B 118(36):10662–10674CrossRefGoogle Scholar
  4. Chen YH, Liu XL, Lu Y, Zhang XY (2009) Investigation of gallium partitioning behavior in aqueous two-phase systems containing polyethylene glycol and am-monium sulfate. J Chem Eng Data 54(7):2002–2004CrossRefGoogle Scholar
  5. Chock SP, Eisenberg E (1974) Heavy meromyosin Mg-ATPase: presteady-state and steady-state H+ release. Proc Nat Acad Sci USA 71(12):4915–4919CrossRefGoogle Scholar
  6. de Meis L (1984) Pyrophosphate of high and low energy. Contributions of pH, Ca2+, Mg2+, and water to free energy of hydrolysis. J Biol Chem 259(10):6090–6097PubMedGoogle Scholar
  7. de Meis L, Behrens MI, Petretski JH (1985) Contribution of water to free energy of hydrolysis of pyrophosphate. Biochemistry 24(26):7783–7789CrossRefGoogle Scholar
  8. Ellis RJ, Audras M, Antonio MR (2012) Mesoscopic aspects of phase transitions in a solvent extraction system. Langmuir 28(44):15498–15504CrossRefGoogle Scholar
  9. George P, Witonsky RJ, Trachtman M, Wu C, Dorwart W, Richman L, Richman W, Shurayh F, Lentz B (1970) “Squiggle-H2O”. An enquiry into the importance of solvation effects in phosphate ester and anhydride reactions. Biochim Biophys Acta 223(1):1–15CrossRefGoogle Scholar
  10. Goldberg RN, Kishore N, Lennen RM (2002) Thermodynamics quantities for the ionization reactions of buffers. J Phys Chem Ref Data 31(2):231–370CrossRefGoogle Scholar
  11. Jiang H, Jia J (2008) Complete reversible phase transfer of luminescent CdTe nanocrystals mediated by hexadecylamine. J Mater Chem 18(3):344–349CrossRefGoogle Scholar
  12. Kardami E, De Bruin S, Gratzer W (1979) Interaction of ADP with skeletal and cardiac myosin and their active fragments observed by proton release. Eur J Biochem 97(2):547–552CrossRefGoogle Scholar
  13. Kodama T (1981) Temperature-modulated binding of ADP and adenyl-5′-yl imidodiphosphate to myosin subfragment 1 studied by calorimetric titration. J Biol Chem 256(22):11503–11508Google Scholar
  14. Kodama T, Fukui K, Kometani K (1986) The initial phosphate burst in ATP hydrolysis by myosin and subfragment-1 as studied by a modified malachite green method for determination of inorganic phosphate. J Biochem 99(5):1465–1472 (Tokyo)CrossRefGoogle Scholar
  15. Kodama T, Woledge RC (1979) Enthalpy changes for intermediate steps of the ATP hydrolysis catalyzed by myosin subfragment-1. J Biol Chem 254(14):6382–6386PubMedGoogle Scholar
  16. Koretz JF, Taylor EW (1975) Transient state kinetic studies of proton liberation by myosin and subfragment 1. J Biol Chem 250(16):6344–6350PubMedGoogle Scholar
  17. Pal D, Tripathi A, Shukla A, Gupta KR, Keshav A (2015) Reactive extraction of pyruvic acid using tri-n-octylamine diluted in decanol/kerosene: equilibrium and effect of temperature. J Chem Eng Data 60(3):860–869CrossRefGoogle Scholar
  18. Plaut GW, Kuby SA, Lardy HA (1950) Systems for the separation of phosphoric esters by solvent distribution. J Biol Chem 184(1):243–249PubMedGoogle Scholar
  19. Romero PJ, de Meis L (1989) Role of water in the energy of hydrolysis of phosphoanhydride and phosphoester bonds. J Biol Chem 264(14):7869–7873PubMedGoogle Scholar
  20. Springs B, Welsh KM, Cooperman BS (1981) Thermodynamics, kinetics, and mechanism in yeast inorganic pyrophosphatase catalysis of inorganic pyrophosphate: inorganic phosphate equilibration. Biochemistry 20(22):6384–6391CrossRefGoogle Scholar
  21. Stockbridge RB, Wolfenden R (2009) Phosphate monoester hydrolysis in cyclohexane. J Am Chem Soc 131(51):18248–18249CrossRefGoogle Scholar
  22. Stockbridge RB, Wolfenden R (2010) The hydrolysis of phosphate diesters in cyclohexane and acetone. Chem Commun 46(24):4306–4308 (Camb)CrossRefGoogle Scholar
  23. Stockbridge RB, Wolfenden R (2011) Enhancement of the rate of pyrophosphate hydrolysis by nonenzymatic catalysts and by inorganic pyrophosphatase. J Biol Chem 286(21):18538–18546CrossRefGoogle Scholar
  24. 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
  25. Voet D, Voet JG, Pratt CW (2013) Fundamentals of biochemistry, 4th edn. Wiley, HobokenGoogle Scholar
  26. Wolfenden R, Williams R (1985) Solvent water and the biological group-transfer potential of phosphoric and carboxylic anhydrides. J Am Chem Soc 107(14):4345–4346CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Faculty of Computer Science and Systems Engineering, Department of Bioscience and BioinformaticsKyushu Institute of TechnologyFukuokaJapan

Personalised recommendations