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Fig. 6.25 The nicotinic acetylcholine receptor in a membrane. The deciphering of the structure is based on X-ray diffraction and electron microscopy. (According to Kistler and coworkers) through the transverse tubules to the membrane of the sarcoplasmatic reticulum, increasing the permeability of the membrane for calcium ions by five orders within 1 millisecond, so that the concentration of Ca2+ ions in the sarcoplasm increases above 10~3 mol dm~3. This produces a relative shift of actin and myosin molecules and contraction of the muscle fibre. After disappearance of the spike, Ca2+-ATPase renews the original situation and the muscle is relaxed. 6.5.2 Membrane principles of bioenergetics The basic process by which living organisms obtain energy is photosynthesis in green plants, yielding carbonaceous substances (fuels) and oxidative phosphorylation in all organisms, in which the Gibbs energy obtained by oxidation of these carbonaceous substances with oxygen is converted into the energy of the polyphosphate bond in adenosinetriphosphate (ATP) through the reaction of adenosine diphosphate with dihydrogen phosphate ions (PinOrg)This process occurs in the mitochondria, organelles present in the cells of all multicellular organisms (see Figs 6.8 and 6.26). Mitochondria have two membranes. The invaginations of the internal membrane into the inner space of the organelle (matrix space) are termed crests (from the Latin, cristae). The oxidation of the carbonaceous substrate with oxygen cannot occur directly as the released energy would be converted into heat, but must proceed almost reversibly, through a number of poorly water-soluble redox
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outer membrane inner membrane matrix space intracristal space 8
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Fig. 6.26 Section of a mitochondrion
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systems forming an electron transfer chain located in the internal membrane of the mitochondrion. They include the system of the oxidized and reduced forms of nicotinamide adenine dinucleotide (NAD + /NADH), several flavoprotein systems, especially FMN (flavinmononucleotide), Fe-S proteins (where the iron ions are bound in a complex with inorganic sulphide, cystein and a protein), coenzyme Q (ubiquinone) and several cytochromes. These redox systems are bound to phospholipids and other molecules in several integrated systems depending on their redox potential (see Table 6.2). The redox potentials of these systems, measured in solution, can be quite different from the potentials in the mitochondrial membrane. The sequence of the redox components in this electron transfer permits the oxidation of the carbonaceous substrates to occur 'vectorially', i.e. the chemical change is oriented in space. The theory of the accumulation of the Gibbs energy of oxidation of carbonaceous substrates in the form of the bond of the phosphate ion to
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Table 6.2 Apparent formal redox potentials of systems present in the electrontransfer chain (pH = 7). It should be noted that the potential values were obtained in the homogeneous phase. Due to stabilization in a membrane, the oxidationreduction properties vary so that the data listed below are of orientation character only Oxidized form Cytochrome a3 (ox) Cytochrome c (ox) Cytochrome b (ox) Coenzyme Q Flavinadenindinucleotide (FAD) Fumarate Nicotinamide adenindinucleotide (NAD+) Reduced form
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Cytochrome a3 (red) Cytochrome c (red) Cytochrome b (red) Coenzyme QH2 FADH2 Succinate NADH
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466 adenosine diphosphate (oxidative phosphorylation) must explain the following facts: (a) A topologically closed vesicle (a cell or an organelle) which is not permeable to passively transported H + is always necessary for transformation of the chemical energy of the substrate to the chemical energy of ATP. (b) This process is connected with a change in the pH difference between the intracristal space and the matrix space of the mitochondrion as well as with a change in the membrane potential. (c) An artificially generated difference in the electrochemical potential of H 3 O + between the intracristal space and the matrix space can result in ATP synthesis. (d) Uncoupling of oxidative phosphorylation (i.e. the process in which the substrate is oxidized but no ATP is synthesized) occurs in the presence of certain proton and alkali metal ion carriers. P. Mitchell (Nobel Prize for Chemistry, 1978) explained these facts by his chemiosmotic theory.! This theory is based on the ordering of successive oxidation processes into reaction sequences called loops. Each loop consists of two basic processes, one of which is oriented in the direction away from the matrix surface of the internal membrane into the intracristal space and connected with the transfer of electrons together with protons. The second process is oriented in the opposite direction and is connected with the transfer of electrons alone. Figure 6.27 depicts the first Mitchell loop, whose first step involves reduction of NAD + (the oxidized form of nicotinamide adenosine dinucleotide) by the carbonaceous substrate, SH2. In this process, two electrons and two protons are transferred from the matrix space. The protons are accumulated in the intracristal space, while electrons are transferred in the opposite direction by the reduction of the oxidized form of the Fe-S protein. This reduces a further component of the electron transport chain on the matrix side of the membrane and the process is repeated. The final process is the reduction of molecular oxygen with the reduced form of cytochrome oxidase. It would appear that this reaction sequence includes not only loops but also a proton pump, i.e. an enzymatic system that can employ the energy of the redox step in the electron transfer chain for translocation of protons from the matrix space into the intracristal space. The energy obtained by oxidation of the substrate with oxygen through the electron transport chain is thus accumulated as a difference in the electrochemical potential for H + between the intracristal and matrix spaces.
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tThe term 'chemiosmotic' theory is not very suitable; 'electrochemical membrane theory' would probably be better, but the former has become accepted. Similarly, Mitchell's term 'protonmotive' force is rather unfortunate for the potential difference produced by the transfer of a proton across the mitochondrion membrane. Even this term, imitating 'electromotive' force (retained only because of tradition), seems rather awkward.
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2H* Fig. 6.27 An example of Mitchell's 'loops'. The substrate SH2 is oxidized by NAD+ (nicotinamideadeninedinucleotide) and the reduced form transports two protons and two electrons, of which two protons remain in the intracristal space and two electrons are transported back by the Fe-S protein to reduce FMN (flavinmononucleotide), the reduced form of which transports two protons and two electrons in the opposite direction
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This can be used in several ways. H+-ATPase plays a key role in oxidative phosphorylation (ATP synthesis) as it transfers protons back into the matrix space with simultaneous synthesis of ATP (with temporary enzyme phosphorylation, cf. page 451). In the presence of certain substances, oxidative phosphorylation is uncoupled, i.e. while the carbonaceous substrate is oxidized, ATP is not synthesized, but can even be hydrolysed to ADP and a phosphate ion. The uncouplers of oxidative phosphorylation belong to the two groups of ionophores, one of which transfers protons across the mitochondrial membrane and the other alkali metal ions. The first group includes the semihydrophobic anions of weak acids such as 2,4-dinitrophenolate, dicumurate, azide, etc. By resonance effects resulting in spreading of the negative charge over the whole structure of these anions, they can pass through the lipid part of the inner membrane of the mitochondrion in the direction of increasing electric potential into the intracristal space, with higher concentration of hydrogen ions. They are then converted into the undissociated form of the corresponding acid, which is transported in the opposite direction into the matrix space, where protons obtained in
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468 the intracristal space are dissociated. The transport of the anions and of the undissociated acid is passive and decreases both the membrane potential and the activity of hydrogen ions in the intracristal space, so that the energy obtained in the oxidation of the carbonaceous substrate is dissipated as heat. The decrease in the hydrogen ion activity in the intracristal space leads to the opposite function of H+-ATPase resulting in ATP hydrolysis. The second group of uncouplers includes macrocyclic complexing agents of the valinomycin type (see page 445), which have the strongest effect in the presence of potassium ions. The hydrophobic (lipophilic) ionophore freely diffuses through the lipid part of the mitochondrial membrane. It binds potassium ions on the intracristal side, which are then passively transported into the matrix space in the complex, simulating proton transport. The explanation of the effect of uncouplers strongly supports the Mitchell theory of oxidative phosphorylation. The difference in the hydrogen ion electrochemical potential, formed in bacteria similarly as in mitochondria, can be used not only for synthesis of ATP but also for the electrogenic (connected with net charge transfer) symport of sugars and amino acids, for the electroneutral symport of some anions and for the sodium ion/hydrogen ion antiport, which, for example, maintains a low Na+ activity in the cells of the bacterium Escherichia coli. It should be noted that, while the Mitchell theory explains some of the basic characteristics of oxidative phosphorylation, a number of phenomena connected with this process remain unclear from both the biochemical and the electrochemical points of view. Biochemical processes in the mitochondrial membrane are still far from being clarified completely. Although the Mitchell theory is called electrochemical, it is obvious that it was not formulated by an electrochemist. It employs only thermodynamic quantities and does not consider the kinetics of the individual steps. Charge balance is neglected in charge transfer across the mitochondrial membrane, although it is obvious that part of the transferred charge must be consumed in charging the electrical double layer at the membrane surface, which is very diversified; because of the presence of cristae the capacity of the double layer is large. The role of transferred protons in acid-base equilibria is also not clear. Nonetheless, the Mitchell theory has been a great step forward. The second basic bioenergetic process consists of consumption of solar radiation as a source of energy in the organisms. One of the ways of employing solar radiation energy in the organism has already been mentioned in connection with the explanation of the function of the purple membrane of Halobacterium halobium (page 450); however, a far more important means of employing this energy for bioenergetic purposes is photosynthesis
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