863—Absorption and conversion of electric field energy by membrane bound ATPases

Tsong, Tian Yow; Astumian, R.D.

doi:10.1016/0302-4598(86)85034-6

Cited by 201ATP Synthase and ATPases ResearchIon Transport and Channel RegulationProtein Structure and Dynamics

863—Absorption and conversion of electric field energy by membrane bound ATPases

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Tsong, Tian Yow, Astumian, R.D.·1986·Bioelectrochemistry and Bioenergetics

DOI 10.1016/0302-4598(86)85034-6

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Abstract

Electric fields are ubiquitous in living organisms, yet, little is known of their effects on the function of enzymes and proteins. Recent experiments show that applied electric fields can induce active transport of K+, Rb+ and Ca2+ by transport-ATPases, as well as ATP synthesis by ATP-synthetases. In all cases, tightly sealed membrane vesicles have been essential. Here we present a kinetic model for the transduction of electric field energy based on three considerations: The equilibrium between any two conformational states of a protein is susceptible to perturbation by an electric field so long as there exists a difference between the molar electric moments. An integral membrane protein experiences an amplified electric field. The transmembrane potential is maintained only with non-leaky vesicles. This model consists of four steps to form a complete cycle (i.e. one enzyme turnover), namely, the conformational energy coupling (energy absorption), the substrate binding, the energy transduction (energy conversion), and the product release steps. The energy transduction step is mediated by reversal of the local field. Computer simulations show that this four state model converts electric field energy into chemical potential energy if the frequency and the strength of the applied field properly match the characteristics of the system. The model finds analogy in an electric rectifier, which conducts current only in certain directions. The results of simulation agree with the main features of the experimental data for voltage-stimulated active transport of Rb+via (Na,K)ATPase of erythrocytes. The concept is extended to the interpretation of data for the voltage-induced ATP synthesis by ATP-synthetases. In this case, F0 is treated as a voltage modulating subunit whose function is to effect a periodic attenuation of the local electric field. This modulation allows multiple enzyme turnover even when a d.c. field is imposed. For the in vivo ATP synthesis, the membrane potential (d.c. in nature) presumably is supplied by the electron transport reactions. Reduction of cytochromes reconstituted into the lipid bilayer is well known to generate transmembrane potentials. The model treats the energy coupling event as a field-induced conformational change, and reduces energy transduction to events pertinent to the study of molecular mechanisms of enzyme action. The equations derived are solidly based on fundamental thermodynamic principles.

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Computer simulation of a four-state enzyme electro-conformationally coupled to an alternating electric field reproduced the main features of the above results.
“Computer simulation of a four-state enzyme electro-conformationally coupled to an alternating electric field [81,82] reproduced the main features of the above results.”
From An Overview of Sub-Cellular Mechanisms Involved in the Action of TTFields (2016) · cites this paper as [81]

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Background
Resonance transduction of low level periodic signals by an enzyme: an oscillatory activation barrier model
Markin, V. S., Liu, D., Rosenberg, M. D., & Tsong, T. Y. (1992) · Biophysical Journal · doi:10.1016/s0006-3495(92)81913-6 · Cited by 38 · see citing works
Rapid and non-invasive quantification of metabolic substrates in biological cell suspensions using non-linear dielectric spectroscopy with multivariate calibration and artificial neural networks. Principles and applications
Woodward, A. M., Jones, A., Zhang, X.-Z., Rowland, J. J., & Kell, D. B. (1996) · Bioelectrochemistry and Bioenergetics · doi:10.1016/0302-4598(96)05065-9 · Cited by 38 · see citing works
Ion activation of the Na,K-ATPase in alternating currents
Blank, M., & Soo, L. (1990) · Bioelectrochemistry and Bioenergetics · doi:10.1016/0302-4598(80)85006-9 · Cited by 38 · see citing works
Confirmation by using mutant strains that the membrane-bound H+-ATPase is the major source of non-linear dielectricity in Saccharomyces cerevisiae
Woodward, A. M., & Kell, D. B. (1991) · FEMS Microbiology Letters · doi:10.1016/0378-1097(91)90401-u · Cited by 36 · see citing works
Changes in Water-Soluble Vitamins and Antioxidant Capacity of Fruit Juice–Milk Beverages As Affected by High-Intensity Pulsed Electric Fields (HIPEF) or Heat during Chilled Storage
Salvia‐Trujillo, L., la Peña, M. M., Rojas‐Graü, M. A., & Martín‐Belloso, O. (2011) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf2011497 · Cited by 35 · see citing works
On the relationship between the nonlinear dielectric properties and respiratory activity of the obligately aerobic bacterium Micrococcus luteus
Woodward, A. M., & Kell, D. B. (1991) · Bioelectrochemistry and Bioenergetics · doi:10.1016/0302-4598(91)85005-m · Cited by 34 · see citing works
External electric fields stimulate the electrogenic calcium/sodium exchange in plant protoplasts
Graziana, A., Ranjeva, R., & Teissié, J. (1990) · Biochemistry · doi:10.1021/bi00488a016 · Cited by 34 · see citing works
Mechanisms for the interaction between nonstationary electric fields and biological systems II. Nonlinear dielectric theory and free-energy transduction
Westerhoff, H. V., Astumian, R. D., & Kell, D. B. (1988) · Ferroelectrics · doi:10.1080/00150198808227005 · Cited by 34 · see citing works
Harmonic Response of Cellular Membrane Pumps to Low Frequency Electric Fields
Nawarathna, D., Miller, J. H., Claycomb, J. R., Cárdenas, G., & Warmflash, D. M. (2005) · Physical Review Letters · doi:10.1103/physrevlett.95.158103 · Cited by 32 · see citing works
Mechanisms for the interaction between nonstationary electric fields and biological systems I. Linear dielectric theory and its limitations
Kell, D. B., Astumian, R. D., & Westerhoff, H. V. (1988) · Ferroelectrics · doi:10.1080/00150198808227004 · Cited by 32 · see citing works
Estimates for ELF effects: Noise-based thresholds and the number of experimental conditions required for empirical searches
Weaver, J. C., & Astumian, R. D. (1992) · Bioelectromagnetics · doi:10.1002/bem.2250130712 · Cited by 32 · see citing works
Cell fission and formation of mini cell bodies by high frequency alternating electric field
Marszałek, P. E., & Tsong, T. Y. (1995) · Biophysical Journal · doi:10.1016/s0006-3495(95)80338-3 · Cited by 30 · see citing works
Interpretation of the effect of an oscillating electric field on membrane enzymes
Robertson, B., & Astumian, R. D. (1992) · Biochemistry · doi:10.1021/bi00116a020 · Cited by 30 · see citing works
The role of magnetic fields in neurodegenerative diseases
Riancho, J., de la Torre, J. R. S., Paz‐Fajardo, L., Limia, C., Santurtún, A., Cifra, M., Kourtidis, K., & Fdez-Arróyabe, P. (2020) · International Journal of Biometeorology · doi:10.1007/s00484-020-01896-y · Cited by 29 · see citing works
Enzymatic Inactivation by Pulsed Electric Fields
Martín‐Belloso, O., Marsellés-Fontanet, À. R., & Elez‐Martínez, P. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-411479-1.00009-7 · Cited by 29 · see citing works
Two approaches toward a high-efficiency flashing ratchet
Розенбаум, В. М., Korochkova, T. Y., Yang, D., Lin, S. H., & Tsong, T. Y. (2005) · Physical Review E · doi:10.1103/physreve.71.041102 · Cited by 27 · see citing works
Genetic programming as an analytical tool for non-linear dielectric spectroscopy
Woodward, A. M., Gilbert, R. J., & Kell, D. B. (1999) · Bioelectrochemistry and Bioenergetics · doi:10.1016/s0302-4598(99)00022-7 · Cited by 25 · see citing works
On electroporation of cell membranes and some related phenomena
Tsong, T. Y. (1990) · Journal of Electroanalytical Chemistry · doi:10.1016/0022-0728(90)87529-s · Cited by 24 · see citing works
Direct electric field effects and sequential processes in biosystems
Astumian, R. D., & Berg, H. (1991) · Bioelectrochemistry and Bioenergetics · doi:10.1016/0302-4598(91)80010-z · Cited by 24 · see citing works
Effect of the external electric field on selected tripeptides
Mazurkiewicz, J., Kołoczek, H., & Tomasik, P. (2015) · Amino Acids · doi:10.1007/s00726-015-1971-8 · Cited by 23 · see citing works
The role of thermal activation in motion and force generation by molecular motors
Astumian, R. D. (2000) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2000.0592 · Cited by 23 · see citing works
“B (2000) (Tsong & Astumian 1986).”
Electroconformational coupling for ion transport in an oscillating electric field: Rectification versus active pumping
Markin, V. S., & Tsong, T. Y. (1991) · Bioelectrochemistry and Bioenergetics · doi:10.1016/0302-4598(91)80028-2 · Cited by 22 · see citing works
Ion channel enzyme in an oscillating electric field
Markin, V., Liu, D., Gimsa, J., Strobel, R. S., Rosenberg, M. D., & Tsong, T. Y. (1992) · The Journal of Membrane Biology · doi:10.1007/bf00231912 · Cited by 22 · see citing works
“To explain these phenomena, an electroconformational coupling (ECC) model has been proposed ( Tsong & Astumian, 1986; Astumian et al., 1989; Astumian & Robertson, 1989; Markin et al., 1990, 1991; Robertson & Astumian, 1990a; Tsong, 1990; Weaver & Astumian, 1990).”
Method
Na,K-ATPase as A Brownian Motor: Electric Field-InducedConformational Fluctuation Leads to Uphill Pumping of Cation inthe Absence of ATP
Tsong, T. Y. (2002) · Journal of Biological Physics · doi:10.1023/a:1019991918315 · Cited by 21 · see citing works
“8. The efficiency of a TEC enzyme: Microscopic reversibility, detailed balancing and maximal energy transfer ensure a TEC enzyme to achieve its maximal efficiency [7, 12, 13, 29 ].”
Background
Electroconformational coupling for ion transport in an oscillating electric field: rectification versus active pumping
Markin, V. S., & Tsong, T. Y. (1991) · Journal of Electroanalytical Chemistry · doi:10.1016/0022-0728(91)85600-t · Cited by 21 · see citing works
On the nonlinear dielectric properties of biological systems
Woodward, A. M., & Kell, D. B. (1990) · Journal of Electroanalytical Chemistry · doi:10.1016/0022-0728(90)87511-h · Cited by 20 · see citing works
Noise-induced quantum transport
Ghosh, P. K., Barik, D., & Ray, D. S. (2005) · Physical Review E · doi:10.1103/physreve.71.041107 · Cited by 19 · see citing works
Enzymatic Inactivation by Pulsed Electric Fields
Martín‐Belloso, O., & Elez‐Martínez, P. (2005) · Elsevier eBooks · doi:10.1016/b978-012676757-5/50009-8 · Cited by 18 · see citing works
The Dielectric Properties of Cells and Tissues: What can They Tell Us about the Mechanisms of Field/Cell Interactions?
Davey, C. L., & Kell, D. B. (1990) · Springer eBooks · doi:10.1007/978-1-4612-3386-2_2 · Cited by 18 · see citing works
Stochastic energetics of quantum transport
Ghosh, P. K., & Ray, D. S. (2006) · Physical Review E · doi:10.1103/physreve.73.036103 · Cited by 17 · see citing works
Quadratic response of a chemical reaction to external oscillations
Astumian, R. D., Robertson, B., Li, R. S., & Ross, J. (1992) · The Journal of Chemical Physics · doi:10.1063/1.462592 · Cited by 17 · see citing works
A protet-based, protonic charge transfer model of energy coupling in oxidative and photosynthetic phosphorylation
Kell, D. B. (2021) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/bs.ampbs.2021.01.001 · Cited by 16 · see citing works
Non-linear dielectric spectroscopy: antifouling and stabilisation of electrodes by a polymer coating
Woodward, A. M., Davies, E. A., Denyer, S. P., Olliff, C. J., & Kell, D. B. (2000) · Bioelectrochemistry · doi:10.1016/s0302-4598(00)00063-5 · Cited by 16 · see citing works
Ion activation of the Na,K-ATPase in alternating currents
Blank, M., & Soo, L. (1990) · Journal of Electroanalytical Chemistry · doi:10.1016/0022-0728(90)87490-b · Cited by 16 · see citing works
Weak AC-electric fields promote root growth and ER abundance of root cap cells
Stenz, H. G., Wohlwend, B., & Weisenseel, M. H. (1998) · Bioelectrochemistry and Bioenergetics · doi:10.1016/s0302-4598(97)00071-8 · Cited by 15 · see citing works
Entrainment of Na/K pumps by a synchronization modulation electric field
Chen, W., Zhang, Z., & Huang, F. (2007) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-007-9096-8 · Cited by 15 · see citing works
“…have been built to explore the possible mechanisms involved in electrical activation of the pump molecules, such as the resonance frequency model (Tsong and Astumian 1986, 1987; Markin et al. 1992; Robertson and Astumian 1991), Brownian ratchet model (Astumian 1997; Tsong 2002), and adiabatic…”
Background
Stochastic resonance in a biological motor under complex fluctuations
Chang, C.-H., & Tsong, T. Y. (2004) · Physical Review E · doi:10.1103/physreve.69.021914 · Cited by 14 · see citing works
Ion pump as Brownian motor: theory of electroconformational coupling and proof of ratchet mechanism for Na,K-ATPase action
Tsong, T. Y., & Chang, C.-H. (2003) · Physica A Statistical Mechanics and its Applications · doi:10.1016/s0378-4371(02)01793-4 · Cited by 14 · see citing works
Synchronization of Na/K pump molecules by a train of squared pulses
Chen, W., & Zhang, Z. S. (2006) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-006-9049-7 · Cited by 14 · see citing works
“All of these studies are based on a concept from an elegant theory of resonance or optimal frequency windows in which an electric field can increase the enzyme reaction rate ( Tsong and Astumian, 1986, 1987; Markin et al., 1992; Robertson and Astumian, 1991).”
Background
Ac-field-induced KCl leakage from human red cells at low ionic strengths
Georgiewa, R., Donath, E., Gimsa, J., Löwe, U., & Glaser, R. W. (1989) · Bioelectrochemistry and Bioenergetics · doi:10.1016/0302-4598(89)87044-8 · Cited by 13 · see citing works

[18] Active cation pumping of Na+, K+-ATPase and sarcoplasmic reticulum Ca2+-ATPase induced by an electric field
Tsong, T. Y. (1988) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(88)57080-5 · Cited by 11 · see citing works
Charge-Field Interactions in Cell Membranes and Electroconformational Coupling: Transduction of Electric Energy by Membrane ATPases
Tsong, T. Y., & Astumian, R. D. (1989) · Springer eBooks · doi:10.1007/978-1-4613-0557-6_17
Resonance electroconformational coupling: A proposed mechanism for energy and signal transductions by membrane proteins
Tsong, T. Y., Liu, D., Chauvin, F., & Astumian, R. D. (1989) · Bioscience Reports · doi:10.1007/bf01117508 · Cited by 42 · see citing works
How enzymes can capture and transmit free energy from an oscillating electric field.
Westerhoff, H. V., Tsong, T. Y., Chock, P. B., Chen, Y. D., & Astumian, R. D. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.13.4734 · Cited by 167 · see citing works
Energy Transduction by Electroconformational Coupling
Astumian, R. D., Chock, P. B., Westerhoff, H. V., & Tsong, T. Y. (1988) · Springer eBooks · doi:10.1007/978-1-4612-3744-0_30

Authors: Tsong, T. Y., & Astumian, R. D.
Affiliations: Johns Hopkins University (US)
National Institutes of Health (US)
ORCID: Astumian, R.D.
Venue: Bioelectrochemistry and Bioenergetics
Publisher: Elsevier BV
Published: 1986-06
Volume: 15
Issue: 3
Pages: 457-476
ISSN: 0302-4598 (ISSN-L)
DOI: 10.1016/0302-4598(86)85034-6
OpenAlex: W2093893790
Cited by: 201
References: 36
Citations by year: 2026: 2 · 2025: 1 · 2024: 3 · 2022: 3 · 2021: 3 · 2020: 8 · 2018: 2 · 2017: 2 · 2016: 3 · 2015: 1 · 2014: 1 · 2013: 4 · 2012: 1
FWCI: 4.90
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by-nc-nd/4.0/ (vor, 6122 d)
Locations: Bioelectrochemistry and Bioenergetics (publishedVersion, cc-by-nc-nd)
Funders: National Institutes of Health
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › ATP Synthase and ATPases Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
Keywords: membrane ATPase, Na+/K+-ATPase, ATP synthase, potassium transport, rubidium transport, membrane potential, membrane vesicles, kinetic model, electric field reversal, F0 subunit, electron transport, enzyme mechanism

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863—Absorption and conversion of electric field energy by membrane bound ATPases

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