Targeted oxidation of Torpedo californica acetylcholinesterase by singlet oxygen: Identification of N-formylkynurenine tryptophan derivatives within the active-site gorge of its complex with the photosensitizer Methylene Blue

Biochemical Journal

Volumn 448, Issue 1, 2012, Pages 83-91

  Triquigneaux, Mathilde M ^a   Ehrenshaft, Marilyn ^a   Roth, Esther ^b   Silman, Israel ^b   Ashani, Yakov ^b   Mason, Ronald P ^a   Weiner, Lev ^b   Deterdin, Leesa J ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Acetylcholinesterase (AChE); Active site gorge; Mass spectrometry; N formylkynurenine; Singlet oxygen; Site specific photo oxidation

Indexed keywords

ACETYLCHOLINESTERASE; EDROPHONIUM; FORMYLKYNURENINE; KYNURENINE; METHYLENE BLUE; PROPIDIUM IODIDE; SINGLET OXYGEN; TRYPTOPHAN DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL MODIFICATION; CHEMICAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME INACTIVATION; ILLUMINATION; OXIDATION; PHOTOOXIDATION; PRIORITY JOURNAL; TORPEDO CALIFORNICA;

ACETYLCHOLINESTERASE; ANIMALS; BINDING, COMPETITIVE; CATALYTIC DOMAIN; CHOLINESTERASE INHIBITORS; EDROPHONIUM; ELECTRIC ORGAN; HYDROLYSIS; KYNURENINE; MASS SPECTROMETRY; METHYLENE BLUE; MODELS, MOLECULAR; OXIDATION-REDUCTION; PHOTOCHEMISTRY; PHOTOSENSITIZING AGENTS; PROPIDIUM; PROTEIN CONFORMATION; SINGLET OXYGEN; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; TORPEDO; TRYPTOPHAN; WATER;

EID: 84867792090     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120992     Document Type: Article

References (28)

1. Silman, I. and Sussman, J. L. (2005) Acetylcholinesterase: 'classical' and 'non-classical' functions and pharmacology. Curr. Opin. Pharmacol. 5, 293-302 (Pubitemid 40674253)
2. Hasinoff, B. B. (1982) Kinetics of acetylthiocholine binding to electric eel acetylcholinesterase in glycerol/water solvents of increased viscosity. Evidence for a diffusion-controlled reaction. Biochim. Biophys. Acta 704, 52-58
3. Koelle, G. B. (1963) Cholinesterases and Anticholinesterase Agents, pp. 187-298, Springer-Verlag, Berlin
4. Azevedo Marques, L., Giera, M., Lingeman, H. and Niessen, W. M. A. (2011) Analysis of acetylcholinesterase inhibitors: bioanalysis, degradation and metabolism. Biomed. Chromatogr. 25, 278-299
5. Schliebs, R. and Arendt, T. (2011) The cholinergic system in aging and neuronal degeneration. Behav. Brain Res. 221, 555-563
6. Bon, S., Vigny, M. and Massoulie, J. (1979) Asymmetric and globular forms of acetylcholinesterase in mammals and birds. Proc. Natl. Acad. Sci. U.S.A. 76, 2546-2550 (Pubitemid 9213904)
7. Sussman, J. L., Harel, M., Frolow, F., Oefner, C., Goldman, A., Toker, L. and Silman, I. (1991) Atomic structure of acetylcholinesterase from Torpedo californica : a prototypic acetylcholine-binding protein. Science 253, 872-879 (Pubitemid 21917225)
8. Dvir, H., Silman, I., Harel, M., Rosenberry, T. L. and Sussman, J. L. (2010) Acetylcholinesterase: from 3D structure to function. Chem. Biol. Interact. 187, 10-22
9. Colletier, J.-P., Fournier, D., Greenblatt, H. M., Stojan, J., Sussman, J. L., Zaccai, G., Silman, I. and Weik, M. (2006) Structural insights into substrate traffic and inhibition in acetylcholinesterase. EMBO J. 25, 2746-2756 (Pubitemid 43980382)
10. Harel, M., Schalk, I., Ehret-Sabatier, L., Bouet, F., Goeldner, M., Hirth, C., Axelsen, P. H., Silman, I. and Sussman, J. L. (1993) Quaternary ligand binding to aromatic residues in the active-site gorge of acetylcholinesterase. Proc. Natl. Acad. Sci. U.S.A. 90, 9031-9035 (Pubitemid 23306445)
11. Weiner, L., Roth, E. and Silman, I. (2011) Targeted oxidation of Torpedo californica acetylcholinesterase by singlet oxygen. Photochem. Photobiol. 87, 308-316
12. Allen, M. T., Lynch, M., Lagos, A., Redmond, R. W. and Kochevar, I. E. (1991) A wavelength dependent mechanism for rose bengal-sensitized photoinhibition of red cell acetylcholinesterase. Biochim. Biophys. Acta 1075, 42-49
13. Tomlinson, G., Cummings, D. and Hryshko, L. (1986) Photoinactivation of acetylcholinesterase by erythrosin B and related compounds. Biochem. Cell Biol. 64, 515-522 (Pubitemid 16076624)
14. Paz, A. (2009) Structural and Functional Studies on the Cytoplasmic Domains of Cholinesterase-like Adhesion Molecules. Ph.D. Thesis, Feinberg Graduate School, Weizmann Institute of Science, Rehovot, Israel
15. Paz, A., Roth, E., Ashani, Y., Xu, Y., Shnyrov, V. S., Sussman, J. L., Silman, I. and Weiner, L. (2012) Structural and functional characterization of the interaction of the photosensitizing probe methylene blue with Torpedo californica acetylcholinesterase. Protein Sci. 21, 1138-1152
16. Ehrenshaft, M., de Oliveira Silva, S., Perdivara, I., Bilski, P., Sik, R. H., Chignell, C. F., Tomer, K. B. and Mason, R. P. (2009) Immunological detection of N-formylkynurenine in oxidized proteins. Free Radical Biol. Med. 46, 1260-1266
17. Ehrenshaft, M., Zhao, B., Andley, U. P., Mason, R. P. and Roberts, J. E. (2011) Immunological detection of N-formylkynurenine in porphyrin-mediated photooxided lens α-crystallin. Photochem. Photobiol. 87, 1321-1329
18. Chakraborty, A. B., Berger, S. J. and Gebler, J. C. (2007) Use of an integrated MS: multiplexed MS/MS data acquisition strategy for high-coverage peptide mapping studies. Rapid Comm. Mass Spectrom. 21, 730-744 (Pubitemid 46340317)
19. Plumb, R. S., Johnson, K. A., Rainville, P., Smith, B. W., Wilson, I. D, Castro-Perez, J. M. and Nicholson, J. K. (2006) UPLC/MSE : a new approach for generating molecular fragment information for biomarker structure elucidation. Rapid Comm. Mass Spectrom. 20, 1989-1994 (Pubitemid 44024575)
20. Schey, K. L. and Finley, E. L. (2000) Identification of peptide oxidation by tandem mass spectrometry. Acc. Chem. Res. 33, 299-306
21. Todorovski, T., Fedorova, M. and Hoffmann, R. (2011) Mass spectrometric characterization of peptides containing different oxidized tryptophan residues. J. Mass Spectrom. 46, 1030-1038
22. Biemann, K. (1990) Sequencing of peptides by tandem mass spectrometry and high-energy collision-induced dissociation. Methods Enzymol. 193, 455-479
23. Seidler, J., Zinn, N., Boehm, M. E. and Lehmann, W. D. (2010) De novo sequencing of peptides by MS/MS. Proteomics 10, 634-649
24. Crank, J. (1975) The Mathematics of Diffusion. Oxford University Press, Oxford
25. Ogilby, P. R. (2010) Singlet oxygen: there is indeed something new under the sun. Chem. Soc. Rev. 39, 3181-3209
26. Harel, M., Quinn, D. M., Nair, H. K., Silman, I. and Sussman, J. L. (1996) The X-ray structure of a transition state complex reveals the molecular origin of the catalytic power and substrate specificity of acetylcholinesterase. J. Am. Chem. Soc. 118, 2340-2246
27. Roy, A., Carpentier, P., Bourgeois, D. and Field, M. (2010) Diffusion pathways of oxygen species in the phototoxic fluorescent protein KillerRed. Photochem. Photobiol. Sci. 9, 1342-1350
28. Dolmans, D. E., Fukumura, D. and Jain, R. K. (2003) Photodynamic therapy for cancer. Nat. Rev. Cancer 3, 380-387 (Pubitemid 37328858)