Intramolecular electron transfer between tryptophan radical and tyrosine in oligoproline-bridged model peptides and hen egg-white lysozyme

• Autorzy: Wierzchowski K. L.
• Języki publikacji: EN

Abstrakty

EN

Long range electron transfer (LRET) across protein matrix underlies all one-electron cellular redox reactions. Elucidation of molecular electron transfer pathways and parametrization of their relative efficiency is one of the most challenging problems in the studies on LRET in proteins. In this paper results of pulse radiolysis investigations on kinetics of LRET accompanying intramolecular radical transformation Trp. --> TyrO. in model peptides built of tryptophan and tyrosine bridged by an oligoproline fragment are reviewed, along with an interpretation of the observed distance dependence of the rate of LRET in terms of conformational properties of the peptides, and partitioning of LRET between electron transfer pathways through space and through peptide backbone. This review on model peptide systems is supplemented with recapitulation of similar studies on the same intramolecular transformation in hen egg-white lysozyme, which allowed to identify Trp./Tyr redox pairs and associated electron transfer pathways involved in LRET in this protein.

Słowa kluczowe

EN

pulse radiolysis; hen; transfer pathway; intramolecular electron; lysozyme; radical transformation; egg white; tryptophan; oligoproline peptide

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 1997
• Tom: 44
• Numer: 4
• Opis fizyczny: p.627-644,fig.

Twórcy

autor

Wierzchowski K. L.

• Polish Academy of Sciences, A.Pawinskiego 5a, 02-106 Warsaw, Poland

Bibliografia

• 1. Gray, H.B. & Winkler, J.R. (1996) Electron transfer in proteins. Annu. Rev. Biochem. 65, 537-561.
• 2. Moser, C.C., Keske, J.M., Warncke, K., Farid, R.S. & Dutton, P.L. (1992) Nature of biological electron transfer. Nature 355, 796-802.
• 3. Marcus, R.A. (1993J Electron transfer reac­tions in chemistry — Theory and experiment (Nobel Lecture). Angew. Chem. Intern. Edit. Engl. 32, 1111-1121.
• 4. Marcus, R.A. & Sutin, N. (1985) Electron transfers in chemistry and biology. Biochim. Biophys. Acta 811,265-322.
• 5. Hopfield, J.J. (1974) Electron transfer be­tween biological molecules by thermally acti­vated tunneling. Proc. Natl. Acad. Sci. U.S.A. 71, 3640-3644.
• 6. Newton, M.D. (1991) Quantum chemical probes of electron-transfer kinetics: The na­ture of donor-acceptor interactions. Chem. Rev. 91. 767-792.
• 7. Onuchic, J.N., Beratan, D.N., Winkler, J.R. & Gray, H.B. (1992) Pathway analysis of protein electron-transfer reactions. Annu. Rev. Bio- phys. Biomol. Struct. 21, 349-377.
• 8. Skourtis, S.S. & Beratan, D.N. (1997) High and low resolution theories of protein electron transfer. J. Biol. Inorg. Chem. 2. 378-386.
• 9. Priitz, W.A. & Land, E.J. (1979) Charge trans­fer in peptides. Pulse radiolysis investigation of one-clcctron reactions in dipetides of tryp­tophan and tyrosine. Int. J. Radiat. Biol. 36, 513-520.
• 10. Priitz, W.A., Land, E.J. & Sloper, R.W. (1981) Charge transfer in peptides. J.C.S. Faraday Trans. I 77, 281-292.
• 11. Prutz. W.A., Siebert, F., Butler. J., Land, E.J., Menez, A. & Garestier, T.M. (1982) Charge transfer in peptides. Intramolecular radical transformations involving methionine, tryp­tophan and tyrosine. Biochim. Biophys. Acta 705. 139-149.
• 12. Prutz, W.A., Butler, J. & Land, E.J. (1983) Phenol coupling initiated by one-electron oxi­dation of tyrosine units in peptides and his- tone. Int. J. Radiat. Biol. 44, 183-196.
• 13. Priitz, W.A., Butler, J. & Land, E.J. (1985) Methionyl-tyrosyl radical transition initiated by Br-2 in peptide model systems and ribonu- clease A. Int. J. Radiat. Biol. 47, 149-156.
• 14. Prutz, W.A., Butler, J., Land, E.J. & Swallow, A.J. (1986) Unpaired electron migration be­tween aromatic and sulphur peptide units. Free Radical Res. Commun. 2, 69-75.
• 15. Helbecque, N. & Loucheux-Lefebvre, M.H. (1982) Critical chain length for polyproline-ll structure formation in H-Gly-(Pro)n-OH. Int. J. Peptide Protein Res. 19, 94-101.
• 16. Wierzchowski, K.L., Majcher, K. & Poznański, J. (1995) CD investigations on conformation of H-X-(Pro)n-Y-OH peptides (X=Trp,- Tyr; Y=Tyr,Mct); models for intra­molecular long range electron transfer. Acta Biochim. Polon. 42, 259-268.
• 17. Isied, S.S. & Vassilian. A. (1984) Electron transfer across polypeptides. 3. Oligoproline bridging ligands. J. Am. Chem. Soc. 106, 1732-1736.
• 18. Isied, S.S., Vassilian, A., Magnuson, R. & Schwartz, H.A. (1985) Electron transfer across polypeptides. 5. Rapid rates of electron transfer between Os(II) and Co(III) in com­plexes with bridging oligoprolincs and other polypeptides. J. Am. Chem. Soc. 107, 7432- 7438.
• 19. Isied, S.S., Vassilian, A., Wishart, J.F., Cre- utz, C. & Schwartz, H.A. (1988) The distance dependence of intramolecular electron trans­fer rates: Importance of the nuclear factor. J. Am. Chem. Soc. 110. 635-637.
• 20. Vassilian, A., Wishart, J.F., Hemelryck, B., Schwartz, H. & Isied, S.S. (1990) Electron transfer across polypeptides. 6. I/)ng-range electron transfer in osmium-ruthenium binu- clear complexes bridged with oligoproline peptides. J. Am. Chem. Soc. 112. 7278-7286.
• 21. Isied, S.S., Ogawa, M.Y. & Wishart, J.F. (1992) Peptide-mediated intramolecular elec­tron transfer: Long range distance depend­ence. Chem. Rev. 92, 381-394.
• 22. Ogawa, M.Y., Wishart. J.F., Young, Z., Miller, J.R. & Isied, S.S. (1993) Distance dependence of intramolecular electron transfer across oli- goprolines in f(bpy)2RuU-L-(Pro)n-Coiri(N- H3)5]3+, n = 1-6: Different effects for helical and nonhelical polyproline II structures. J. Phys. Chem. 97, 11456-11463.
• 23. Ogawa, M.Y., Moreira, I., Wishart. J.F. & Isied, S.S. (1993) Long range electron transfer in helical polyproline II oligopeptides. Chem. Phys. 176, 589-600.
• 24. Isied. S.S., Moreira, I., Ogawa, M.Y., Vas­silian, A., Arbo, B. & Sun, J. (1994) New perspectives on long-range electron transfer in conformationally organized peptides and electron-transfer proteins: An experimental approach. J. Photochem. Photobiol., A: Chem. 82, 203-210.
• 25. Schanze, K. & Sauer, K. (1988) Photoinduced intramolecular electron transfer in peptide bridged molecules. J. Am. Chem. Soc. 110, 1180-1186.
• 26. Schanze, K.S. & Cabana, L.A. (1990) Distance dependence of photochemical electron trans­fer across peptide spacers. J. Phys. Chem. 94, 2740-2743.
• 27. Cabana, L.A. & Schanze, K.S. (1990 )Photoin- duced electron transfer across peptide spac­ers; in Electron Transfer in Biology and the Solid State (Johnson, M.K., King, R.B., Kurtz, D.M., Jr., Kutal, C., Norton, M.L. & Scott, R.A., eds.) pp. 101-123, American Chemical Society, Washington. D.C.
• 28. Bobrowski, K., Wierzchowski, K.L., Holcman, J. & Ciurak, M. (1987) Intramolecular charge transfer between tryptophan and tyrosine in peptides with bridging prolines. Studia bio- physica 122, 23-28.
• 29. Bobrowski, K., Wierzchowski, K.L., Holcman, J. & Ciurak, M. (1990) Intramolecular elec­tron transfer in peptides containing methion­ine, tryptophan and tyrosine: A pulse radi- olysis study. Int. J. Radiat. Biol. 57, 919-932.
• 30. Bobrowski, K., Holcman, J., Poznanski, J., Ciurak, M. & Wierzchowski, K.L. (1992) Pulse radiolysis studies of intramolecular electron transfer in model peptides and proteins. 5. Trp' - Tyr* radical transformation in H-Trp- (Pro)n-Tyr-OH series of peptides. J. Phys. Chem. 96, 10036-10043.
• 31. Bobrowski, K., Poznański, J., Holcman, J. & Wierzchowski, K.L. (1998) Long range elec­tron transfer between proline-bridged aro­matic amino acids; in Photochemistry and Radiation Chemistry (Nocera, D.G. & Wis- hart, J.F., eds.) pp. 131-143, American Che­mical Society .Washington, DC. (in presss).
• 32. Faraggi, M., DeFelippis, M.R. & Klapper, M.H. (1989) Long-range electron transfer l>e- tween tyrosine and tryptophan in peptides. J. Am. Chem. Soc. Ill, 5141-5145.
• 33. DeFelippis, M.R., Faraggi, M. & Klapper, M.H. (1990) Evidence for through-bond long- range electron transfer in peptides. J. Am. Chem. Soc. 112, 5640-5642.
• 34. Mishra, A.K., Chandrasekar, R., Faraggi, M. & Klapper, M.H. (1994) Long-range electron transfer in peptides. Tyrosine reduction of the indolyl radical: Reaction mechanism, modula­tion of reaction rate, and physiological consid­erations. J. Am. Chem. Soc. 116, 1414-1422.
• 35. Bobrowski, K., Wierzchowski, K.L., Holcman, J. & Ciurak, M. (1992) Pulse radiolysis stud­ies of intramolecular electron transfer in model peptides and proteins. 4. Met/S-Br- Tyr/O* radical transformation in aqueous so­lution of H-Tyr-(Pro)n-Met-OH peptides. Int. J. Radiat. Biol. 62, 507-516.
• 36. Stryer, L. & Haugland, R.P. (1982) Energy transfer: A spectroscopic ruler. Proc. Natl. Acad. Sci. U.S.A. 58, 719-726.
• 37. Land, E.J. & Prutz, W.A. (1979) Reaction of azide radicals with amino acids and proteins. Int. J. Radiat. Biol. 36, 75-83.
• 38. Butler, J., Land, E.J., Priitz, W.A. & Swallow, A.J. (1982) Charge transfer between trypto­phan and tyrosine in proteins. Biochim. Bio- phys. Acta 705, 150-162.
• 39. Prince, R.C. & George, G.N. (1990) Trypto­phan radicals. Trends Biochem. Sci. 15, 170- 172.
• 40. Sivaraja, M., Goodin, D.B., Smith, M. & Hoff­man, B.M. (1989) Identification by ENDOR of Trp 191 as the free-radical state in cytochrome c peroxidase compound ES. Science 245, 738-740.
• 41. Erman, J.E., Vitello, L.B., Mauro, J.M. & Kraut, J. (1989) Detection of an oxyferryl porphyrin ;r-cation radical intermediate in the reaction between hydrogen peroxide and a mutant yeast cytochrome c peroxidase. Bio­chemistry 28, 7992-7995.
• 42. Debus, R.J., Barry, B.A., Sithole, I., Babcock, G.T. & Mcintosh, L. (1988) Directed mutagen- sis indicates that the donor to P*680 in photo- system II is tyrosine-161 of the D1 polypep­tide. Biochemistry 27, 9071-9074.
• 43. Reichard, P. (1987) Regulation of deoxyri- botide synthesis. Biochemistry 26, 3245- 3248.
• 44. Karthein, R., Diet/., R., Nastainczyk, W. & Ruf, H.H. (1988) Higher oxidation states of prostaglandin H-EPR study of transient tyro- syl radical in the enzyme during the peroxy- dase reaction. Eur. J. Biochem. 171,313- 320.
• 45. Nordlund, P. & Eklund, H. (1993) Structure and function of the Escherichia coli ribonu­cleotide reductase protein R2. J. Mol. Biol. 232, 123-164.
• 46. Bobrowski, K., Holcman, J. & Wierzchowski, K.L. (1989) Temperature dependence of intra­molecular electron transfer as a probe for predenaturational changes in lysozyme. Free Radical Res. Commun. 6, 235-241.
• 47. Bobrowski, K., Holcman, J., Poznanski, J. & Wierzchowski, K.L. (1997) Pulse radiolysis studies of intramolecular electron transfer in model peptides and proteins. 7. Trp'-TyrO" radical transformation in hen egg-white lysozyme. Effects of pH, temperature. Trp62 oxidation and inhibitor binding. Biophys. Chem. 63, 153-166.
• 48. Poznanski, J. (1996) Conformational analysis of oligoproline-bridged peptides and its appli­cation in modeling of electron transfer be­tween terminal amino acids (Trp.Tyr,Met), Ph.D. Dissertation (in Polish), Institute of Biochemistry and Biophysics, Polish Acad­emy of Sciences, Warszawa
• 49. Poznanski, J., Ejchart, A., Wierzchowski, K.L. & Ciurak, M. (1993) 1H- and 13C-NMR inves­tigations on cis-trans isomerization of proline peptide bonds and conformation of aromatic side chains in H-Trp-(Pro)n-Tyr-OH peptides. Biopolymers 33, 781-795.
• 50. Sneddon, S.F. & Brooks, C.L.III (1992) The conformations of proline-linked donor-ac­ceptor systems. J. Am. Chem. Soc. 114, 8220-8225.
• 51. Ramachandran, G.N. & Sasisekharan, V. (1968) Conformation of polypeptides and pro­teins. Adv. Protein Chem. 23, 283-^37.
• 52. Jovanovic, S.V., Steenken, S. & Simic, M.G. (1991) Kinetics and energetics of one-elec­tron-transfer reactions involving tryptophan neutral and cation radicals. J. Phys. Chem. 95, 684-687.
• 53. DeFelippis, M.R., Murthy, C.P., Broitman, F., Weinraub, D., Faraggi, M. & Klapper, M.H. (1991) Electrochemical properties of tyrosine phenoxy and tryptophan indolyl radicals in peptides and amino acid analogues. J. Phys. Chem. 95, 3416-3419.
• 54. Harriman, A. (1987) Further comments on the redox potentials of tryptophan and tyro­sine. J. Phys. Chem. 91, 6102-6104.
• 55. Butler, J., Land, E.J., Prutz, W.A. & Swallow, A.J. (1986) Reversibility of charge transfer between tryptophan and tyrosine. J.C.S. Chem. Comm. 348-349.
• 56. Evenson, J.W. & Karplus, M. (1993) Effective coupling in biological electron transfer-expo­nential or complex distance dependence. Sci­ence 262, 1247-1249.
• 57. Inai, Y., Sisido, M. & Imanishi, Y. (1991) Photoinduced electron transfer on a single a-helical polypeptide chain. Evidence of a through-space mechanism. J. Phys. Chem. 95, 3847- 3851.
• 58. Lee, H., Faraggi. M. & Klapper. M.H. (1992) Long range electron transfer along an a-helix. Biochim. Biophys. Acta 1159, 286-294.
• 59. Faraggi, M. & Klapper, M.H. (1990) Intra­molecular electron transfer reactions in pep­tides and proteins; in Excess Electrons in Dielectric Media (Ferradini, C. & Jay-Cerin, J.-P., eds.) pp. 397-423, CRC Press, Boca Raton.
• 60. Weinstein, M., Alfassi, Z.B., DeFelippis, M.R., Klapper. M.H. & Faraggi, M. (1991) Long range electron transfer between tyrosine and tryptophan in hen egg-white lysozyme. Bio­chim. Biophys. Acta 1076. 173-178
• 61. Kuroda, J., Sakiyama, F. & Narita, K. (1975) Oxidation of tryptophan in lysozyme by ozone in aqueous solution. J. Biochem. 78, 641-665.
• 62. Sakiyama, F. & Natsuki, R. (1976) Identifica­tion of tryptophan 62 as an ozonization-sensi- tive residue in hen egg-white lysozyme. J. Biochem. 79, 225-228.
• 63. Delepierre, M., Dobson, C.M., Karplus, M., Poulsen, F.M., States, D.J. & Wedin, R.E. (1987) Electrostatic effects of hydrogen ex­change behaviour in proteins. The pH de- penedence of exchange rates in lysozyme. J. Mol. Biol. 197. 111-130
• 64. Wedin, R.E., Delepierre, M., Dobson, C.M. & Poulsen, F.M. (1982) Mechanisms of hydro­gen exchange in proteins from nuclear mag­netic resonance studies of individual trypto-phan indole NH hydrogens in lysozyme. Bio­chemistry 21, 1098-1103.
• 65. Pedersen, T.G., Thomson, N.K., Andersen, K.V., Madsen, J.C. & Poulsen, F.M. (1993) Determination of the rate constant-kl and constant-k2 of the Linderstrom-Lang model for protein amide hydrogen exchange — A study of the individual amides in hen egg- white lysozyme. J. Mol. Biol. 230, 651-660.
• 66. Imoto, T., Johnson, L.N., North, A.C.T., Phil­lips, D.C. & Rupley, J.A. (1972) Vertebrate lysozymes; in The Enzymes (Boyer, P.D., ed.) pp. 665-668, Academic Press, New York
• 67. Banerjee, S.K., Holler, E., Hess, G.P. & Ru­pley, J.A. (1975) Reaction of AT-acetylglu- cosamine oligosaccharides with lysozyme. J. Biol. Chem. 250, 4355-4367.
• 68. Beratan, D.N., Betts, J.N. & Onuchic, J.N. (1991) Protein electron transfer rates set by the bridging secondary and tertiary structure. Science 252, 1285-1288.
• 69. Betts, J.N., Beratan, D.N. & Onuchic, J.N. (1992) Mapping electron tunneling pathways. Algorithm that finds the "minimum length"/ maximum coupling pathway between elec­tron donors and acceptors in proteins. J. Am. Chem. Soc. 114, 4043-4046.
• 70. Beratan, D.N., Onuchic, J.N., Betts, J.N., Bowler, B.E. & Gray, H.B. (1990) Electron- tunneling pathways in ruthenated proteins. J. Am. Chem. Soc. 112, 7915-7921.
• 71. Ramanadham, M., Sieker, I#.C. & Jensen, L.H. (1990) Refinement of triclinic lysozyme: II. The method of stereochemical^ restrained last squares. Acta Crystallogr. B 46, 63-69.
• 72. Daizadeh, I., Medvedev, E.S. & Stuchebruk- hov, A.A. (1997) Effect of protein dynamics on biological electron transfer. Proc. Natl. Acad. Sei. U.S.A. 94, 3703-3708.
• 73. Ichiye, T. & Karplus, M. (1983) Fluorescence depolarization of tryptophan residues in pro­teins: A molecular dynamics study. Biochem­istry 22, 2884-2893.