Structure and reactivity of the N-acetyl-cysteine radical cation and anion: Does radical migration occur?

Journal of the American Society for Mass Spectrometry

Volumn 22, Issue 10, 2011, Pages 1794-1803

  Osburn, Sandra ^a   Berden, Giel ^b   Oomens, Jos ^b,c   O'Hair, Richard A J ^d,e,f   Ryzhov, Victor ^a  

^a NORTHERN ILLINOIS UNIVERSITY   (United States)

^b FOM INSTITUTE DIFFER   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f Australian Government Australian Research Council   (Australia)

Author keywords

DFT calculations; Ion molecule reactions; IRMPD spectroscopy; N acetyl cysteine; Radical ions; Radical rearrangement

Indexed keywords

DFT CALCULATION; ION-MOLECULE REACTION; IRMPD SPECTROSCOPY; N-ACETYL-CYSTEINE; RADICAL IONS; RADICAL REARRANGEMENT;

ATOMIC SPECTROSCOPY; DENSITY FUNCTIONAL THEORY; MOLECULES; POSITIVE IONS; SULFUR;

AMINO ACIDS;

ACETYLCYSTEINE; ANION; CATION; NITRIC OXIDE; RADICAL; SULFUR;

ARTICLE; CONTROLLED STUDY; DENSITY FUNCTIONAL THEORY; ENZYME STRUCTURE; INFRARED MULTI PHOTON DISSOCIATION SPECTROSCOPY; MIGRATION; MOLECULAR DYNAMICS; MOLECULE; PROTEIN CLEAVAGE; SPECTROSCOPY; STRUCTURE ANALYSIS;

ACETYLCYSTEINE; ALLYL COMPOUNDS; ANIONS; CATIONS; DISULFIDES; MASS SPECTROMETRY; MOLECULAR CONFORMATION; SPECTROPHOTOMETRY, INFRARED; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 80755142776     PISSN: 10440305     EISSN: 18791123     Source Type: Journal    
DOI: 10.1007/s13361-011-0198-5     Document Type: Article

References (62)

1. Balagopalakrishna, C., Abugo, O., Horsky, J., Manoharan, P., Nagababu, E., Rifkind, J.: Superoxide produced in the heme pocket of the B-chain of hemogobin reacts with the B-93 cysteine to produce a thiyl radical. Biochemistry 37, 13194-13202 (1998) (Pubitemid 28449563)
2. Becker, A., Kabsch, W.: X-ray structure of pyruvate formate-lyase in complex with pyruvate and CoA: How the enzyme uses the Cys 418 thiyl radical for pyruvate cleavage. J. Biol. Chem. 277, 40036-40042 (2002) (Pubitemid 35190993)
3. Ehrenberg, A., Reichard, P.: Electron spin resonance of the ironcontaining protein B2 from ribonucleotide reductase. J. Biol. Chem. 247, 3485-3488 (1972)
4. Knauer, S., Buckel, W., Dobbek, H.: Structural basis for recutive radical formation and electron recycling in (R)-2-Hydroxyisocaproyl-CoA dehydratase. J. Am. Chem. Soc. (2011). doi:10.1021/ja1076537
5. Lepore, B., Ruzicka, F., Frey, P., Ringe, D.: The x-ray crystal structure of lysine-2, 3-aminomutase from Clostridium subterminale. Proc. Natl. Acad. Sci. USA 102, 13819-13824 (2005) (Pubitemid 41377662)
6. Logan, D., Andersson, J., Sjoberg, B.-M., Nordlund, P.: A glycyl radical site in the crystal structure of a class III ribonucleotide reductase. Science 283, 1499-1504 (1999)
7. Mozziconacci, O., Sharov, V., Williams, T., Kerwin, B., Schoneich, C.: Peptide cysteine thiyl radicals abstract hydrogen atoms from surrounding amino acids: The photolysis of a cystine containing model peptide. J. Phys. Chem. B 112, 9250-9257 (2008)
8. Nauser, T., Casi, G., Koppenol, W., Schoneich, C.: Reversible intramolecular hydrogen transfer between cysteine thiyl radicals and glycine and alanine in model peptides: Absolute rate constants derived from pulse radiolysis and laser flash photolysis. J. Phys. Chem. B 112, 15034-15044 (2008)
9. Reitzer, R., Gruber, K., Jogl, G., Wagner, U., Bothe, H., Buckel, W., Kratky, C.: Glutamate mutase from Clostridium cochlearium: The structure of a coenzyme B12-dependent enzyme provides new mechanistic insights. Structure 7, 891-902 (1999) (Pubitemid 29372511)
10. Sivaraja, M., Goodin, D., Smith, M., Hoffman, B.: Identification by ENDOR of Trp191 as the free-radical site in cytochrome c peroxidase compound ES. Science 245, 738-740 (1989) (Pubitemid 19214005)
11. Hioe, J., Savasci, G., Brand, H., Zipse, H.: The stability of Cα peptide radicals: Why glycyl radical enzymes? Chem. Eur. J. 17, 3781-3789 (2011)
12. Licht, S., Gerfen, G., Stubbe, J.: Thiyl radicals in ribonucleotide reductases. Science 271, 477-481 (1996) (Pubitemid 26044465)
13. Davies, M., Dean, R.: Radical-mediated protein oxidation. Oxford University Press, New York (1997)
14. Davies, M.: Protein and peptide alkoxyl radicals can give rise to C-terminal decarboxylation and backbone cleavage. Arch. Biochem. Biophys. 336, 163-172 (1996) (Pubitemid 26423763)
15. Davies, M.: Myeloperoxidase-derived oxidation: Mechanisms of bological damage and its prevention. J. Clin. Biochem. Nutr. 48, 8-19 (2011)
16. Headlam, H., Mortimer, A., Easton, C., Davies, M.: B-scission of C-3 (β-carbon) alkoxyl radicals on peptides and proteins: A novel pathway which results in the formation of a α-carbon radicals and the loss of amino acid side chains. Chem. Res. Toxicol. 13, 1087-1095 (2000)
17. Rauk, A., Armstrong, D.: Influence of B-sheet on the susceptibility of proteins to backbone oxidative damage: Preference for αC-centered radical formation at glycine residues of antiparallel β-sheets. J. Am. Chem. Soc. 122, 4185-4192 (2000) (Pubitemid 30304853)
18. Rauk, A., Yu, D., Armstrong, D.: Oxidative damage to and by cysteine proteins: An Ab initio study of the radical structures, C-H, S-H, and C-C bond dissociation energies, and transition structures for H abstraction by thiyl radicals. J. Am. Chem. Soc. 120, 8848-8855 (1998) (Pubitemid 28442923)
19. Schoneich, C.: Mechanisms of protein damage induced by cysteine thiyl radical formation. Chem. Res. Toxicol. 21, 1175-1179 (2008) (Pubitemid 351967380)
20. Hopkinson, A.: Radical cations of amino acids and peptides: Structures and stabilities. Mass Spectrom. Rev. 28, 655-671 (2009)
21. Sibrian-Vazquez, M., Escobedo, J., Lim, S., Samoei, G., Strongin, R.: Homocystamides promote free-radical and oxidative damage to proteins. Proc. Natl. Acad. Sci. USA 107, 551-554 (2010)
22. Andersson, C. O.: Mass spectrometric studies on amino acid and peptide derivatives. Acta Chem. Scand. 12, 1353 (1958)
23. Chu, I., Rodriquez, C., Lau, T.-C., Hopkinson, A. C., Siu, K. W. M.: Molecular radical cations of oligopeptides. J. Phys. Chem. B 104, 3393-3397 (2000)
24. Masterson, D., Yin, H., Chacon, A., Hachey, D., Norris, J., Porter, N.: Lysine peroxycarbamates: Free radical-promoted peptide cleavage. J. Am. Chem. Soc. 126, 720-721 (2004) (Pubitemid 38114348)
25. Yin, H., Chacon, A., Porter, N., Masterson, D.: Free radical-induced site-specific peptide cleavage in the gas phase: Low-energy collisioninduced dissociation in ESI-and MALDI mass spectrometry. J. Am. Soc. Mass Spectrom. 18, 807-816 (2007) (Pubitemid 46617276)
26. Chacon, A., Masterson, D., Yin, H., Liebler, D., Porter, N.: N-terminal amino acid side-chain cleavage of chemically modified peptides in the gas phase: A mass spectrometry technique for N-terminus identification. Bioorg. Med. Chem. 14, 6213-6222 (2006) (Pubitemid 44224084)
27. Wee, S., Mortimer, A., Moran, D., Wright, A., Barlow, C. K., O'Hair, R. A. J., Radom, L., Easton, C. J.: Gas-phase regiocontrolled generation of charged amino acid and peptide radicals. Chem. Commun. 4233-4235 (2006) (Pubitemid 44556368)
28. Barlow, C. K., Wright, A., Easton, C. J., O'Hair, R. A. J.: Gas-phase ionmolecule reactions using regioselectively generated radical cations to model oxidative damage and probe radical sites in peptides. Org. Biomol. Chem. 9, 3733-3745 (2011)
29. Liu, Z., Julian, R.: Deciphering the peptide iodination code: Influence on subsequent gas-phase radical generation with photodissociation ESI-MS. J. Am. Soc. Mass Spectrom. 20, 965-971 (2009)
30. Ly, T., Julian, R.: Residue-specific radical-directed dissociation of whole proteins in the gas phase. J. Am. Chem. Soc. 130, 351-358 (2008)
31. Diedrich, J., Julian, R.: Site-specific radical directed dissociation of peptides at phosphrylated residues. J. Am. Chem. Soc. 130, 12212-12213 (2008)
32. Ryzhov, V., Lam, A. K. Y., O'Hair, R. A. J.: Gas-phase fragmentation of long-lived cysteine radical cations formed via NO loss from protonated S-nitrosocysteine. J. Am. Soc. Mass Spectrom. 20, 985-995 (2009)
33. Steill, J., Zhao, J., Siu, C.-K., Ke, Y., Verkerk, U., Oomens, J., Dunbar, R., Hopkinson, A. C., Siu, K. W. M.: Structure of the observable histidine radical cation in the gas-phase: A captodative α-radical ion. Angew. Chem. 120, 154-156 (2008)
34. Sinha, R., Maitre, P., Piccirillo, S., Chiavarino, B., Crestoni, M., Fornarini, S.: Cysteine radical cation: A distonic structure probed by gas phase IR spectroscopy. Phys. Chem. Chem. Phys. 12, 9794-9800 (2010)
35. Osburn, S., Steill, J., Oomens, J., O'Hair, R. A. J., Van Stipdonk, M., Ryzhov, V.: Structure and reactivity of the cysteine methyl ester radical cation. Chem. Eur. J. 17, 873-879 (2010)
36. Zhao, J., Siu, K. W. M., Hopkinson, A. C.: The cysteine radical cation: Structures and fragmentation pathways. Phys. Chem. Chem. Phys. 10, 281-288 (2008)
37. Lam, A. K. Y., Ryzhov, V., O'Hair, R. A. J.: Mobile protons vs. mobile radicals: Gas-phase unimolecular chemistry of radical cations of cysteine-containing peptides. J. Am. Soc. Mass Spectrom. 21, 1296-1312 (2010)
38. Moore, B., Blanksby, S., Julian, R.: Ion-molecule reactions reveal facile radical migration in peptides. Chem. Commun. 10, 5015-5017 (2009)
39. Fu, M., Li, S., Archibold, E., Yurkovich, M., Nash, J., Kenttamaa, H.: Reactions of an aromatic σ, σ-biradical with amino acids and dipeptides in the gas phase. J. Am. Soc. Mass Spectrom. 21, 1737-1752 (2010)
40. Li, S., Fu, M., Habicht, S., Pates, G., Nash, J. J., Kenttamaa, H.: Phenyl Radical Induced Damage to Dipeptides. J. Org. Chem. 74, 7724-7732 (2009)
41. Kirk, B., Harman, D., Blanksby, S.: Direct observation of the gas phase reaction of the cyclohexyl radical with dioxygen using a distonic radical ion approach. J. Phys. Chem. A 114, 1446-1456 (2010)
42. Lam, C. N. W., Chu, I. K.: Formation of anionic peptide radicals in vacuo. J. Am. Soc. Mass Spectrom. 17, 1249-1257 (2006) (Pubitemid 44292009)
43. Laskin, J., Yang, Z., Lam, C., Chu, I. K.: Charge-remote fragmentation of odd-electron peptide ions. Anal. Chem. 79, 6607-6614 (2007) (Pubitemid 47395045)
44. Coon, J. J., Shabanowitz, J., Hunt, D. F., Syka, J. E. P.: Electron transfer dissociation of peptide anions. J. Am. Soc. Mass Spectrom. 16, 880-882 (2005) (Pubitemid 40725163)
45. Pompella, A., Visvikis, A., Paolicchi, A., De Tata, V., Casini, A.: The changing faces of glutathione, a cellular protagonist. Biochem. Pharmacol. 66, 1499-1503 (2003) (Pubitemid 38373339)
46. Pyatkivskyy, Y., Ryzhov, V.: Coupling of ion-molecule reactions to liquid chromatography on a quadrupole ion trap mass spectrometer. Rapid Commun. Mass Spectrom. 22, 1288-1294 (2008) (Pubitemid 351600779)
47. Oepts, D., Van der Meer, A., Van Amersfoort, P.: The free electron laser user facility FELIX. Infrared Phys. Technol. 36, 297-308 (1995)
48. Valle, J., Eyler, J., Oomens, J., Moore, D., Van der Meer, A., Von Helden, G., Meijer, G., Hendrickson, C., Marshall, A., Blakney, G.: Free electron laser-fourier transform ion cyclotron resonance mass spectrometry facility for obtaining infrared multiphoton dissociation spectra of gaseous ions. Rev. Sci. Instrum. 76, 023103 (2005)
49. Polfer, N., Oomens, J., Moore, D., Von Helden, G., Meijer, G., Dunbar, R.: Infrared spectroscopy of phenylalanine Ag (I) and Zn (II) complexes in the gas phase. J. Am. Chem. Soc. 128, 517-525 (2006) (Pubitemid 43157545)
50. Marshall, A., Hendrickson, C., Jackson, G.: Fourier transform ion cyclotron resonance mass spectrometry: A primer. Mass Spectrom. Rev. 17, 1-35 (1998) (Pubitemid 128629493)
51. Polfer, N., Oomens, J.: Reaction products in mass spectrometry elucidated with infrared spectroscopy. Phys. Chem. Chem. Phys. 9, 3804-3817 (2007)
52. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Montgomery Jr., J. A., Vreven, T., Kudin, K. N., Burant, J. C., Millam, J. M., Iyengar, S. S., Tomasi, J., Barone, V., Mennucci, B., Cossi, M., Scalmani, G., Rega, N., Petersson, G. A., Nakatsuji, H., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Klene, M., Li, X., Knox, J. E., Hratchian, H. P., Cross, J. B., Bakken, V., Adamo, C., Jaramillo, J., Gomperts, R., Stratmann, R. E., Yazyev, O., Austin, A. J., Cammi, R., Pomelli, C., Ochterski, J. W., Ayala, P. Y., Morokuma, K., Voth, G. A., Salvador, P., Dannenberg, J. J., Zakrzewski, V. G., Dapprich, S., Daniels, A. D., Strain, M. C., Farkas, O., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Ortiz, J. V., Cui, Q., Baboul, A. G., Clifford, S., Cioslowski, J., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Gonzalez, C., Pople, J. A.: GAUSSIAN 03 (Revision D.01). Gaussian Inc., Wallingford (2004)
53. Polfer, N., Oomens, J., Dunbar, R.: IRMPD spectroscopy of metal-ion/tryptophan complexes. Phys. Chem. Chem. Phys. 8, 2744-2751 (2006)
54. Polfer, N., Oomens, J., Dunbar, R.: Alkali metal complexes of the dipeptides PheAla and AlaPhe: IRMPD spectroscopy. Chem. Phys. Chem. 9, 579-589 (2008)
55. Chu, I., Zhao, J., Xu, M., Siu, S., Hopkinson, A. C., Siu, K. W. M.: Are the radical centers in peptide radical cations mobile? The generation, tautomerism, and dissociation of isomeric α-carbon-centered triglycine radical cations in the gas phase. J. Am. Chem. Soc. 130, 7862-7872 (2008) (Pubitemid 351875061)
56. Siu, C.-K., Zhao, J., Laskin, J., Chu, I., Hopkinson, A. C., Siu, K. W. M.: Kinetics for tautomerization and dissociations of triglycine radical cations. J. Am. Soc. Mass Spectrom. 20, 996-1005 (2009)
57. Bohme, D. K.: Proton transport in the catalyzed gas-phase isomerization of protonated molecules. Int. J. Mass Spectrom. Ion Processes 115, 95-110 (1992)
58. Mourgues, P., Chamot-Rooke, J., Nedev, H., Audier, H.-E.: Spontaneous and catalyzed isomerizations of the acetamide radical cation. J. Mass Spectrom. 36, 102-104 (2001)
59. Gauld, J. W., Audier, H. E., Fossey, J., Radom, L.: Water-catalysed interconversion of conventional and distonic radical cations: Methanol and methyleneoxonium radical cations. J. Am. Chem. Soc. 118, 6299-6300 (1996) (Pubitemid 26236869)
60. Viehe, H. G., Janousek, Z., Merenyi, R., Stella, L.: The captodative effect. Acc. Chem. Res. 18, 148-154 (1985)
61. Sustmann, R., Korth, H.-G.: The captodative effect. Adv. Phys. Org. Chem. 26, 131-178 (1991)
62. Easton, C. J.: Free-radical reactions in the synthesis of α-amino acids and derivatives. Chem. Rev. 97, 53-82 (1997) (Pubitemid 127662442)