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Review Letter TRANSMEMBRANE ELECTROCHEMICAL H+-POTENTIAL AS a CONVERTIBLE ENERGY SOURCE for the LIVING CELL

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Review Letter TRANSMEMBRANE ELECTROCHEMICAL H+-POTENTIAL AS a CONVERTIBLE ENERGY SOURCE for the LIVING CELL View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Volume 74, number 1 FEBS LETTERS February 1977 ReviewLetter TRANSMEMBRANE ELECTROCHEMICAL H+-POTENTIAL AS A CONVERTIBLE ENERGY SOURCE FOR THE LIVING CELL Vladimir P. SKULACHEV Department of Bioenergetics, Laboratory of Bioorganic Chemistry, Moscow State University, Moscow II 7234, USSR Received 1 November 1976 Revised version received 5 January 1977 1. Introduction oxidative phosphorylation. Lardy et al. [3] found that the antibiotic oligomycin prevents energy transfer In 1941 Lipmann [l] put forward the idea that between X - Y and ATP. In the presence of oligo- ATP occupies the point of intersection of biological mycin, X - Y produced by the second and third energy transformation pathways. In the following energy coupling sites of the respiratory chain was 3.5 years, comprehensive experimental proof of the shown to be utilized to support reverse electron- validity of this postulate was furnished by a great transfer via the first energy coupling site. ‘X - Y’ many independent lines of study. The impressive was postulated to be discharged by uncouplers of success of the ATP concept gave rise to the opinion oxidative phosphorylation added to mitochondria in that the system of high-energy compounds is the only vitro [3] or formed in vivo, e.g., in response to convertible and transportable form of energy in the exposure of warm-blooded animals to cold. living cell. The latter conclusion was, certainly, no Further investigations revealed that X - Y energy more than a speculation requiring deeper insight into can be used to actuate Ca”-uptake by mitochondria bioenergetic mechanisms to be confirmed or rejected. [5] and energy-linked reduction of NADP’ by NADH The study of one of these mechanisms, namely [6] . All these observations pointed to X - Y being a oxidative phosphorylation, resulted in several pieces polyfunctional energy source in mitochondria. of evidence being accumulated which indicated that the cell possesses another form of unified energy, 2.2. Electrochemical fl-potential (AjiH) besides ATP and related chemical substances. In 1961-1966 Mitchell [7,8] developed a new (‘chemiosmotic’) theory of biological energy coupling, postulating the existence of a gradient of 2. ‘Non-phosphorylated intermediate’ and H+ potential electrochemical-potential of hydrogen ions (APH) across membranes competent in respiratory or photo- 2.1. ‘Non-phosphorylated intermediate’ of energy synthetic phosphorylation. coupling (X - Y) According to Mitchell the role of respiratory and T’he,first group of facts which were indicative of photosynthetic redox-chains in ATP-synthesis is the storage of oxidation-released energy in a form confined to the formation of AjIH. The latter, it is other than ATP, was obtained in experiments with suggested, is used to reverse the H’--ATPase reaction. mitochondria oxidizing substrates in the absence of For example, the mitochondrial respiratory-chain ADP and phosphate. Such studies prompted Slater would pump H’ from the mitochondrion to the cyto- [2] to suggest a ‘non-phosphorylated intermediate plasm, creating AjiH across the inner mitochondrial of oxidative phosphorylation’. He believed this to be membrane (negative and alkaline in the mitochondrial an unknown high-energy chemical compound (X - Y) matrix). Then H+-ions go back to the matrix down e.g., a thioester, functioning as an ATP-precursor in A,CiHthrough an H’-ATPase (ATP-synthetase) system North-Holland Publishing Company - Amsterdam 1 Volume 74, number 1 FEBS LETTERS February 1977 localized in the same membrane and ATP is formed phores associated with a planar membrane, to be from ADP and Pi [7,8,8a,b]. measured. Maximal values of A$ found were 240 mV The electrochemical-potential of H+-ions consists for bacteriorhodopsin from Halobacterium halobium, of an electrical component (transmembrane electric 215 mV for the light-dependent system of cyclic potential difference, A$) and a chemical component electron-transport from Rhodospirillum rubrum, (gradient of H+-concentration, ApH). Both A$ and 100 mV for cytochrome oxidase from beef heart ApH have been demonstrated across coupling mem- mitochondria, 70 mV for R. rubum pyrophosphatase branes of many types (inner mltochondrial membranes, and about 40 mV for mitochondrial and R. rubrum chloroplast thylakoid membranes and bacterial mem- H’--ATPases (at currents of 1 X lo-” -1 X lo-l2 A). branes). A method of universal applicability for the It was shown in several laboratories that electro- detection of A$ in intact organelles (mitochondria phoretic movement of any penetrating ion across a and chloroplasts) and bacterial cells or their particles coupling membrane, down an electrical potential has been developed by our group [9,10]. It was gradient, results in the conversion of A$ to ApH (for suggested by Dr E. A. Liberman and consists of reviews, see refs. [8,21,22]). The pH outside the measuring the transmembrane distribution of synthetic vesicles was measured with a sensitive pH-electrode penetrating ions. or using pH-dependent changes in the light absorption It was found that penetrating cations and anions or fluorescence of some non-penetrating dyes. Pene- differing strongly ln their structures move through trating pH-indicators and detergent treatment were coupling membranes ln opposite directions. This used to determine the pH inside the vesicles. process, defined as transmembrane electrophoresis [ 111, was found to be supported by electron-transfer 2.3. Identity of ‘non-phosphorylated intermediate’ via any of four energy coupling sites of the respiratory and H’-po ten tial (X - Y = w) chain as well as by ATP-hydrolysis. Similar relation- In the first detailed presentation of the chemios- ships were revealed in experiments with chloroplast motic theory, Mitchell [8] considered the following and bacterial membrane systems. In chloroplasts and ‘energy transfer chain’: e- transfer via the redox-chain photosynthetic bacteria, A$ was detected also by measuring electrochromic shifts in absorption spectra coupling site + AiiH + X N Y + ATP. of carotenoids and chlorophyll [ 12-141. A light- dependent All/ was observed by means of a micro- However, the inclusion of X - Y in this pathway electrode inserted into a chloroplast in vivo [ 151. was no more than a tribute to the traditional view of To exclude any possibility of the electrical events the mechanism of energy coupling. Later Mitchell across mitochondrial, chloroplast and bacterial mem- [23] and Glagolev [24] put forward schemes not branes being a secondary consequence of the energiza- involving X - Y. Indeed, there are no experimental tion of a complex system like the cell or organelle, observations indicating that ‘non-phosphorylated we attempted to demonstrate the electrogenic activity intermediate’ is a high-energy chemical compound. of purified lipoproteins incorporated into an artificial Any attempts to identify X - Y with known high- membrane [ 16-201. The lipoprotein was incorporated energy substances failed. Moreover, several pieces of into spherical phospholipid membrane vesicles and the evidence were obtained suggesting ATP to be the resulting proteoliposomes were associated with a only covalent high-energy compound in the ‘energy planar phospholipid membrane through Ca’+-ions. transfer chain’ (for review, see refs [25,25(a)]). On Addition of an appropriate energy source utilizable the other hand, AiiH seems to meet requirements for by the lipoprotein was shown to induce generation of the component whose place had previously been both an electrical potential difference and a current occupied by X - Y, because: across the planar membrane. These were measured (1) &H can be formed by the redox-chain in the with a conventional electrometer and macro-electrodes absence of ADP and Pi, the process being resistant immersed in the electrolyte solutions on both sides to oligomycin. of the planar membrane. A similar procedure allowed (ii) Interconversion between AjiH and ATP is electrical generation, by intact bacterial chromato- sensitive to oligomycin. 2 Volume 74, number 1 FEBS LETTERS February 1977 (iii) AjiH is a common product of the forward seems to be obvious that the level of AjiH, when it is electron-transfers via the four energy coupling sites mainly in the form of A$, requires some additional and can be responsible for energy-exchange between stabilizing mechanism when the activities of A,QH- these sites; it can be involved in the respiration-sup- producing and MH-consuming pathways are chang- ported reverse electron-transfer in an oligomycin- ing. In these conditions, AiiH-supported conversion resistant fashion. of Pi to PPi, which CXI be easily converted back to Pi me~~r~eIsI supports ion-transport through coupling and AjiH, might function as the A,%H-stabilizing mechanism. (v) AjiH runs down in the presence of protono- phorous uncouplers [22] . 4. Osmotic work by APH 3. A,UH-Supported chemical work Conversion of A,QH to concentration-gradients of compounds penetrating membranes can also act as a This includes synthesis of high-energy phosphates A,QH-buffer. If a decrease in activity of AiiH-generat- (ATP and PPi) and reduction of compounds of negative ing enzymes takes place, efflux of penetrating cations redox-potential by means of the reverse electron- from mitochondria, accumulated earlier in the matrix transfer in the redox chains. It was shown that systems down an electrical gradient, should prevent AiiH from
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