Respiratory Chain. The respiratory chain. Electron carriers. Prosthetic groups. flavins. Citric acid cycle. P. Frederix
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1 The respiratory chain Citric acid cycle Respiratory Chain P. Frederix Nicotinamide Adenine Dinucleotide Electron carriers (Ubi)Quinone Prosthetic groups Non-protein chemical compounds that are tightly bound to a protein and are required for the protein's biological activity flavins FMN (Flavin MonoNucleotide) FAD (Flavin Adenine Dinucleotide) Carbon as electron donor 1
2 17-hydroxyethylfarnesyl Prosthetic groups: Hemes Prosthetic groups: Iron-Sulfur clusters 1 1 Heme b histidine cystein Hemes a and b are generally coordinated by conserved amino acid side chains (XY): e.g. Heme b inside complex II, kept in place between 2 histidines Prosthetic groups chain versus catalytic site Spectroscopy for studying respiration Hemes have characteristic absorption spectra Hemes are the prothetic groups of Cytochromes α-peak was used to categorize heme a, b and c types SMP = submitochondrial particle Lower temperature: narrower peaks Page et al. 2003, Absorption spectrum cyt c (Lehninger, Biochemistry) 2
3 Spectroscopy for studying respiration Hemes have characteristic absorption spectra Spectroscopy for studying respiration Hemes have characteristic absorption spectra Detection of redox centers Iron-sulfur centers EPR spectroscopy Redox potentiometry E = hν = g e µ B B Signal is from unpaired electrons in: Fe 3+, Mn 2+, Cu 2+ Biological redox couple plus secondary redox mediator (1-100 µm) that has similar mid-point potential, e.g. ascorbate (E m,7 +60 mv). For this experiment the complex must be kept in solution with detergent or a bilayer permeant mediator must be used. To titrate a redox process, either an electron donor (reducing agent) like dithionite (E m,7-660 mv) or an electron acceptor (oxidizing agent) like ferricyanide (E m, mv) is added. Titration with small aliquots of dithionite makes the potential more negative, with ferricyanide more positive. 3
4 Redox potentiometry Example: Mixture of complex II & III in detergent To titrate the redox process the electron acceptor ferricyanide is added, and spectra are recorded at different potentials. Here 4 Spectra were recorded (-100mV, -10mV, 145mV, 180mV) and difference spectra are calculated, by substracted the next oxidized stage (giving a reduced-oxidized difference spectrum): i. Abs(145mV) Abs(180mV) ii. Abs(-10mV) Abs(145mV) iii. Abs(-100mV) Abs(-10mV) Question: Which prosthetic groups do we look at and in which range are their mid-point potentials under the experimental conditions? Electron transfer: Marcus theory If wavefunctions overlap, transfer is possible. Overlap is maximal when G=-λ (product curve crosses reactant curve at minimum) The reorganization energy λ is the energy required for all structural adjustments (in the reactants and in the surrounding solvent molecules) which are needed in order that A and D assume the configuration required for the transfer of the electron. Marcus, J Chem Phys 1956, Moser et al. Nature, 1992 Practical tunneling expression Frank-Condon factor λ Reorganization energy λ (ev) Dutton s plots Tunneling versus distance k ET ( G+ λ ) / λ Driving force G (ev) G can be adjusted using mutants with shifted mid-potentials Haffa, A.L., Lin, Su, Katilius, E., Williams, J.C., Taguchi, A.K. J. Phys. Chem B. 106: (2002) Gunner, M. R and Dutton P.L. J.A.C.S. 111: (1989) Moser, C. C. et al. Nature 355: (1992). Page, C. C. et al. Nature 402:47-52 (1999). Moser, C. C. et al. In Enzyme-Catalyzed Electron Radical Transfer (Scrutton, N. S.), pp 1-30 (Plenum, 2000) Page, C. C. et al Current Opinion 7:1-6 (2003) Moser et al., Nature
5 Dutton s Equations If the structure of the protein is not known, electron transfer rates are calculated based on the following equations: Electron tunneling in oxidation-reduction For exothermic (downhill) reactions ( G < 0): Log 10 k et = (R - 3.6) ( G + λ ) 2 / λ For endothermic (uphill) reactions ( G > 0): Log 10 k et = (R - 3.6) (- G + λ ) 2 / λ - G/0.06 The initial constant 13 is the rate at van der Waals contact distance (R = 3.6 Å). The second term describes an approximately exponential fall-off in electron tunneling rate with distance through the insulating barrier. R is the edge-to-edge distance. The third term is the quantized Frank-Condon factor at room temperature. G is free energy change and λ is reorganization energy, both in units of ev. The last term in the uphill reactions incorporates thermal excitation (kt 0.025eV). Page et al, Nature 1999 Experimental rate data compared with edge-toedge distances lie close to the G=-λ line Theoretical curves for exo/endothermic with previous equations Electron tunneling in oxidation-reduction Electron tunneling in oxidation-reduction at the catalytic site Proximity between redox centers in catalytic clusters allows rapid tunneling to endergonic radical intermediate states. Insertion of high energy intermediates is faster than no intermediate Heme a 3 and Cu B In complex IV Xanthine dehydrogenase Moving radical states into the thermally accessible regime Page et al, Nature 1999 Page et al, Nature
6 Summary I Enzymes can be studied by redox potentiometry, optical spectroscopy, EPR spectroscopy Mitochondrial: The respiratory chain: Cofactors Electrons tunnel from one to the next prosthetic group The mid-point potential of prosthetic groups depends on their direct environment Electron tunneling requires prosthetic groups to be precisely arranged (<14Å) Electrons are shuttled by electron carriers from one to the next complex Electron carriers (NADH, quinone, cytochrome c, oxygen) must have precise docking sites to accept/deliver electrons from/into the tunneling pathway. Uphill intermediate prosthetic groups are possible Note: The counterpart of Complex I in bacteria has generally only 14 subunits (13 in E. coli, where two are fused as one) Other names: Complex I: NADH-UQ oxidoreductase Complex II: Succinate-UQ oxidoreductase, Succinate dehydrogenase, SQR Complex III: UQ-cyt c oxidoreductase, cyt bc 1 complex Complex IV: ferrocytochrome c-o 2 oxidoreductase, cytochrome c oxidase, cytochrome aa 3 oxidase 6
7 7
8 8
9 Redox potential ladder drives electronflow E m,7, in non-respiring mammalian mitochondria E h,7, in state 4, depends on ratio of components There are four isopotential groups Potential gaps correspond to regions where proton translocation occurs µ H+ 9
10 Complex I Complex I catalyzes oxidation of NADH, with reduction of coenzyme Q. Complex I is the point of entry for the major fraction of electrons that traverse the respiratory chain, is L-shaped and includes (in mammals) ~ 45 unlike proteins (M r about 2 MDa). Coupled to the electron transfer, protons are pumped from the matrix side to the inter-membrane space of mitochondria. NADH + Q + H + + nh + in NAD + + QH 2 + nh + out (n=3-5) This enzyme complex contains a noncovalently-bound FMN molecule and 2 binuclear and 6 tetranuclear iron-sulfur clusters. The initial electron transfers are: NADH + H + + FMN NAD + + FMNH 2 FMNH 2 + (Fe-S)ox FMNH + (Fe-S)red + H + Thereafter Fe-S is reoxidized by transfer of the electron to the next iron-sulfur center in the pathway: FMNH + (Fe-S)ox FMN + (Fe-S)red + H+ Electrons pass through a series of iron-sulfur centers in complex I, and are eventually transferred to coenzyme Q. Coenzyme Q accepts 2 e and picks up 2 H + to yield the fully reduced QH 2. M. Lazarou et al. / Biochimica et Biophysica Acta 1793 (2009) Research on complex I has recently taken on greater significance since the finding that many human mitochondrial diseases involve structural and functional defects at the level of this enzyme complex. Isolated complex I deficiency is the most common cause of respiratory chain dysfunction (1 st sentence in abstract Lazarou et al.) Complex II Succinate Dehydrogenase from E. coli is packed as a trimer. The complex II prosthetic group FAD is reduced to FADH 2 during oxidation of succinate to fumarate. FADH 2 is reoxidized by transfer of electrons through a series of three Fe-S centers to Coenzyme Q, yielding QH 2. X-ray crystallographic analysis of related bacterial electron transfer complexes indicates a linear arrangement of these electron carriers across the membrane consistent with the predicted sequence of electron transfers: FAD FeScenter 1 FeScenter 2 FeScenter 3 CoQ There are other non-membrane bound complexes that fulfill similar tasks as complex II E. Coli complex II Yankovskaya et al., science 2003 Bacterial complex II analogue: (QFR) Menaquinol oxidation by Wolinella succinogenes QFR. The prosthetic groups of the W. succinogenes QFR dimer are displayed (PDB entry 1QLA). Distances between prosthetic groups are edge-to-edge distances in Å. Drawn in red is the side chain of Glu C66. Menaquinol binding (drawn in green) is modelled. The position of bound fumarate (Fum) is taken from PDB entry 1QLB. E. coli W. succinogenes Complex II Why is heme b present? Yankoskaya et al., science 2003 According to Lancaster, FEBS 2001 Calculate transfer rates using Duttons rule. ( MK = Menaquinone) E. Coli complex II Yankovskaya et al., science
11 Complex III (bc1 complex) Complex III (bc1 complex) Complex III accepts electrons from the coenzyme QH2 that is generated by electron transfer in complexes I and II. The pathway is called the "Q cycle and depends on: the mobility of CoQ within the lipid bilayer the existence of binding sites for CoQ within bc1 that stabilize the semiquinone radical, Q. matrix Q cycle: Electrons enter complex III via QH2, which binds at a site near the membrane surface facing the intermembrane space. QH2 gives up an e to the Rieske iron-sulfur center (Fe-S), which makes a conformational change, so Fe-S can be reoxidized by electron transfer to cytochrome c1, which passes the electron out of the complex to cytochrome c. Loss of one e to the Fe-S complex, and release of 2 H+ to the intermembrane space, generates a Q radical. Q becomes Q as it gives up the second electron that is transferred to the other side of the membrane via hemes bl and bh. It takes 2 cycles for CoQ, bound at a site near the matrix side of the membrane, to be reduced to QH2, as 2 electrons are transferred from the b hemes and 2 H+ are extracted from the matrix compartment. In 2 cycles, 2 QH2 enter the pathway, and one is regenerated. intermembrane space Complex III (bc1 complex) -77±11mV 51±7mV Complex III (bc1 complex) 257±4mV 1) 2) 3) 4) 5) Control + myxothiazol + antimycin + myxothiazol + antimycin + antimycin + ascorbate Berry et al., 1991, JBC, 266, Reducing titration (open symbols) and re-oxidation titration (closed symbols) give the mid-potential of the complex III heme groups. Berry et al., 1991, JBC, 266,
12 Complex III Three positions of the Rieske Fe/S protein in beef mytochondrial cyt. bc 1 complex Complex III From Ed Berry The net Q cycle reaction: QH 2 +2H + (matrix)+2 cyt c (Fe 3+ ) Q + 4 H + (out) + 2 cyt c (Fe 2+ ) Per 2e- transferred through the complex to cytochrome c, 4H+ are released to the intermembrane space. Fe/S protein in its cyt c1 positional state (1BE3) Fe/S protein in intermediate location (1BCC) Fe/S protein in its b positional state, close to Q P -site (1BGY) Bovine Complex IV (cytochrome c oxidase) Subunits I and II of 13 subunits in cytochrome oxidase (complex IV) contain the metal centers: Cu a (2 adjacent Cu-atoms) heme a heme a 3 Cu b Bovine Complex IV (cytochrome c oxidase) Structure is solved for mitochondrial and bacterial complex: Intramembrane domains of cytochrome oxidase (complex IV) consist mainly of transmembrane α-helices. Tsukihara et al. (1995) 12
13 Bacterial Complex IV Cytochrome oxidase (complex IV) carries out the following irreversible reaction: O H e 2 H 2 O. The four electrons are transferred into the complex one at a time from cytochrome c. Cytochrome oxidase viewed from the side. (Paracoccus denitrificans) Subunit I is yellow Subunit II is magenta Subunit III is blue Subunit IV is in green The cyan subunit is from the antibody used to aid crystallization of the complex. Complex IV O 2 reacts at a binuclear center, consisting of heme a 3 and Cu B. For cytochrome c oxidase, the overall reaction is: 4 ferrocyt c + 4H + N + 4H + N + O 2 4 ferricyt c + + 2H 2 O + 4H + P Since cytochrome c is in the P-phase, 8 charges are transfered from N- to P-phase per oxygen consumed. Iwata et al. (1995) Complex IV Summary II The respiratory chain is a nanoscale redox machine built of complex I to IV, which are embedded in a lipid bilayer. These enzymes convert the redox energy obtained from oxidation of carbohydrates into a proton gradient The energy liberated drives protons uphill against a concentration gradient and a potential. Whereas the structure of complex I is still missing, those of complex II- IV are now resolved to high resolution CO-bound heme a 3 -Cu B unit Yoshikawa et al., 1996, science 280, Azide-bound heme a 3 -Cu B unit (Sodium azide, NaN3 is often used to keep buffers free of bacteria) Structures from different states of the reaction cycles of complex II-IV help to understand the function Nanometer scale movements are associated with functional cycles Proton pathways are lined with water molecules, but mechanism in complex I and IV are still not proven 13
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