Long-Range Electron Transfer Between Proline-Bridged Aromatic Amino Acids

Abstract

Interpretation of the kinetic pulse radiolysis data for intramolecular Trp --> Tyr radical transformation in aqueous solutions of linear H-Trp-(Pro)n-Tyr-OH, n = 0-5, is presented in terms of the Marcus electron transfer theory, taking into account conformational dynamics of the molecules. For this purpose, for each peptide, representative sets of low-energy conformers were selected with the help of experimental methods ( 1 H and 13 C NMR, and circular dichroism) and modeling meth ods (molecular mechanics and dynamics ); and relative electron transfer rates averaged over all the conformers were calculated for two assumed competitive electron transfer pathways: through space (TS) and through the peptide backbone (TB). The TS rates were obtained by taking into account the overlap integrals of aromatic ring orbitals calu lated quantum mechanically. By fitting the calculated rates to the experi mental data for the rate constants for electron transfer, ket, with an exponential function appropriate for the two-pathway model, we have demonstrated that in linear short-bridged peptides (n = 0-2), electron transfer predominantly takes the TS pathway, which consists of van der Waals contacts between the aromatic rings, whereas in longer peptides (n = 3-5), it occurs exclusively by the TB pathway, which is made of a -(Pro)n-bridge in a helical conformation similar to that of all-trans poly-L-proline II. This pathway is characterized by a low value of the descriptor of the exponential distance dependence of the electron transfer rate, β ΤΒ = 2.5 ± 0.1 nm -1 , suggesting that helical segments in proteins can function as efficient channels of long-distance electron transfer.

Pulse Radiolysis Studies of Intramolecular Electron Transfer in Model Peptides and Proteins. 8. Trp[NH•+] → Tyr[O•] Radical Transformation in H-Trp-(Pro)n-Tyr-OH, n = 3−5, Series of Peptides

“…The kinetics of the observed electron-transfer reaction in the three peptides studied proved to be first-order over the whole pH (2)(3)(4)(5)(6)(7)(8) and temperature (278-328 K) ranges investigated. The rate of LRET, measured under pH conditions in which both reactions 1 and 2 can occur simultaneously, was the same whether followed by the decay of Trp[N • ] and Trp[NH •+ ] at 510 nm (isosbestic point) or solely by the decay of Trp[NH •+ ] at λ max ) 580 nm.…”

“…This similarity supports our earlier conclusion, based on comparison between Trp[N • ],Tyr[OH] and various metallic redox couples, that electron transferability of the helical PLPII type -(Pro) n -bridge is independent of the nature of the attached donor-acceptor pair. 8 This conclusion does not seem to apply, however, to peptide 3 for which the k 2 /k 1 ratio was found to be 3-fold lower.…”

“…Intramolecular one-electron oxidation of tyrosine, Tyr [OH], to phenoxyl radical, Tyr[O • ], by the tryptophan indolyl radical, Trp[N • ], involving long-range electron transfer (LRET), has been intensively studied by pulse radiolysis in model peptides [1][2][3][4][5][6][7][8][9][10][11] and proteins [12][13][14][15][16] because of the importance of the mechanism of free radical damage to proteins for understanding of freeradical-induced cell injury 17 and growing evidence for participation of Trp[N • ] and Tyr[O • ] radicals in the functioning of photosystem II and redox proteins. [18][19][20][21][22][23][24][25][26] The pulse radiolysis method allows us to trigger this reaction in a very short time (<1 µs) by selective oxidation of tryptophan, Trp[NH], to Trp-[N • ] by N 3 • (in neutral solution) or Br 2 •-(in acidic solution) radicals.…”

The Chemistry of Protein Oxidation in Food

“…These reactions may proceed as expected from the respective redox potentials (Table ). Intramolecular radical transfer from a tryptophanyl radical ( 18 ) to tyrosine leading to a phenoxyl radical ( 20 ) was described in a model study on lysozyme …”

Die Chemie der Proteinoxidation in Lebensmitteln

“…Diese Reaktionen können so ablaufen, wie es die entsprechenden Redoxpotentiale erwarten lassen (Tabelle ). Der intramolekulare Radikaltransfer von einem Tryptophanylradikal 18 (Schema ) zu einem Tyrosinrest unter Bildung eines Phenoxylradikals 20 wurde an Lysozym gezeigt …”