Abstract
Previous work has shown that Na,K-ATPase of human erythrocytes can extract free energy from sinusoidal electric fields to pump cations up their respective concentration gradients. Because regularly oscillating waveform is not a feature of the transmembrane electric potential of cells, questions have been raised whether these observed effects are biologically relevant. Here we show that a random-telegraph fluctuating electric field (RTF) consisting of alternating square electric pulses with random lifetimes can also stimulate the Rb(+)-pumping mode of the Na,K-ATPase. The net RTF-stimulated, ouabain-sensitive Rb+ pumping was monitored with 86Rb+. The tracer-measured, Rb+ influx exhibited frequency and amplitude dependencies that peaked at the mean frequency of 1.0 kHz and amplitude of 20 V/cm. At 4 degrees C, the maximal pumping activity under these optimal conditions was 28 Rb+/RBC-hr, which is approximately 50% higher than that obtained with the sinusoidal electric field. These findings indicate that Na,K-ATPase can recognize an electric signal, either regularly oscillatory or randomly fluctuating, for energy coupling, with high fidelity. The use of RTF for activation also allowed a quantitative theoretical analysis of kinetics of a membrane transport model of any complexity according to the theory of electroconformational coupling (ECC) by the diagram methods. A four-state ECC model was shown to produce the amplitude and the frequency windows of the Rb(+)-pumping if the free energy of interaction of the transporter with the membrane potential was to include a nonlinear quadratic term. Kinetic constants for the ECC model have been derived. These results indicate that the ECC is a plausible mechanism for the recognition and processing of electric signals by proteins of the cell membrane.
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Selected References
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- Astumian R. D., Chock P. B., Tsong T. Y., Chen Y. D., Westerhoff H. V. Can free energy be transduced from electric noise? Proc Natl Acad Sci U S A. 1987 Jan;84(2):434–438. doi: 10.1073/pnas.84.2.434. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Astumian RD, Chock PB, Tsong TY, Westerhoff HV. Effects of oscillations and energy-driven fluctuations on the dynamics of enzyme catalysis and free-energy transduction. Phys Rev A Gen Phys. 1989 Jun 15;39(12):6416–6435. doi: 10.1103/physreva.39.6416. [DOI] [PubMed] [Google Scholar]
- Atwater I., Dawson C. M., Ribalet B., Rojas E. Potassium permeability activated by intracellular calcium ion concentration in the pancreatic beta-cell. J Physiol. 1979 Mar;288:575–588. [PMC free article] [PubMed] [Google Scholar]
- Berridge M. J. Calcium oscillations. J Biol Chem. 1990 Jun 15;265(17):9583–9586. [PubMed] [Google Scholar]
- Blank M. Na,K-ATPase function in alternating electric fields. FASEB J. 1992 Apr;6(7):2434–2438. doi: 10.1096/fasebj.6.7.1314204. [DOI] [PubMed] [Google Scholar]
- Cevc G. Membrane electrostatics. Biochim Biophys Acta. 1990 Oct 8;1031(3):311–382. doi: 10.1016/0304-4157(90)90015-5. [DOI] [PubMed] [Google Scholar]
- Chen Y. D. Asymmetry and external noise-induced free energy transduction. Proc Natl Acad Sci U S A. 1987 Feb;84(3):729–733. doi: 10.1073/pnas.84.3.729. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hill T. L., Chen Y. On the theory of ion transport across the nerve membrane. VI. Free energy and activation free energies of conformational change. Proc Natl Acad Sci U S A. 1972 Jul;69(7):1723–1726. doi: 10.1073/pnas.69.7.1723. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Horn L. W. A novel method for the observation of membrane transporter dynamics. Biophys J. 1993 Jan;64(1):281–289. doi: 10.1016/S0006-3495(93)81365-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kalmijn A. J. Electric and magnetic field detection in elasmobranch fishes. Science. 1982 Nov 26;218(4575):916–918. doi: 10.1126/science.7134985. [DOI] [PubMed] [Google Scholar]
- Liu D. S., Astumian R. D., Tsong T. Y. Activation of Na+ and K+ pumping modes of (Na,K)-ATPase by an oscillating electric field. J Biol Chem. 1990 May 5;265(13):7260–7267. [PubMed] [Google Scholar]
- Markin V. S., Liu D., Gimsa J., Strobel R., Rosenberg M. D., Tsong T. Y. Ion channel enzyme in an oscillating electric field. J Membr Biol. 1992 Mar;126(2):137–145. doi: 10.1007/BF00231912. [DOI] [PubMed] [Google Scholar]
- Markin V. S., Tsong T. Y. Frequency and concentration windows for the electric activation of a membrane active transport system. Biophys J. 1991 Jun;59(6):1308–1316. doi: 10.1016/S0006-3495(91)82345-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meyer T., Stryer L. Calcium spiking. Annu Rev Biophys Biophys Chem. 1991;20:153–174. doi: 10.1146/annurev.bb.20.060191.001101. [DOI] [PubMed] [Google Scholar]
- Robertson B., Astumian R. D. Interpretation of the effect of an oscillating electric field on membrane enzymes. Biochemistry. 1992 Jan 14;31(1):138–141. doi: 10.1021/bi00116a020. [DOI] [PubMed] [Google Scholar]
- Serpersu E. H., Tsong T. Y. Activation of electrogenic Rb+ transport of (Na,K)-ATPase by an electric field. J Biol Chem. 1984 Jun 10;259(11):7155–7162. [PubMed] [Google Scholar]
- Serpersu E. H., Tsong T. Y. Stimulation of a ouabain-sensitive Rb+ uptake in human erthrocytes with an external electric field. J Membr Biol. 1983;74(3):191–201. doi: 10.1007/BF02332123. [DOI] [PubMed] [Google Scholar]
- Tomchik K. J., Devreotes P. N. Adenosine 3',5'-monophosphate waves in Dictyostelium discoideum: a demonstration by isotope dilution--fluorography. Science. 1981 Apr 24;212(4493):443–446. doi: 10.1126/science.6259734. [DOI] [PubMed] [Google Scholar]
- Tsien R. W., Tsien R. Y. Calcium channels, stores, and oscillations. Annu Rev Cell Biol. 1990;6:715–760. doi: 10.1146/annurev.cb.06.110190.003435. [DOI] [PubMed] [Google Scholar]
- Tsong T. Y., Astumian R. D. Electroconformational coupling and membrane protein function. Prog Biophys Mol Biol. 1987;50(1):1–45. doi: 10.1016/0079-6107(87)90002-2. [DOI] [PubMed] [Google Scholar]
- Tsong T. Y. Deciphering the language of cells. Trends Biochem Sci. 1989 Mar;14(3):89–92. doi: 10.1016/0968-0004(89)90127-8. [DOI] [PubMed] [Google Scholar]
- Tsong T. Y. Electrical modulation of membrane proteins: enforced conformational oscillations and biological energy and signal transductions. Annu Rev Biophys Biophys Chem. 1990;19:83–106. doi: 10.1146/annurev.bb.19.060190.000503. [DOI] [PubMed] [Google Scholar]
- Tsong T. Y. Electroporation of cell membranes. Biophys J. 1991 Aug;60(2):297–306. doi: 10.1016/S0006-3495(91)82054-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tsong T. Y. Molecular recognition and processing of periodic signals in cells: study of activation of membrane ATPases by alternating electric fields. Biochim Biophys Acta. 1992 Mar 26;1113(1):53–70. doi: 10.1016/0304-4157(92)90034-8. [DOI] [PubMed] [Google Scholar]
- Weaver J. C., Astumian R. D. The response of living cells to very weak electric fields: the thermal noise limit. Science. 1990 Jan 26;247(4941):459–462. doi: 10.1126/science.2300806. [DOI] [PubMed] [Google Scholar]
- Westerhoff H. V., Tsong T. Y., Chock P. B., Chen Y. D., Astumian R. D. How enzymes can capture and transmit free energy from an oscillating electric field. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4734–4738. doi: 10.1073/pnas.83.13.4734. [DOI] [PMC free article] [PubMed] [Google Scholar]
