N-Acetylserotonin and 6-Hydroxymelatonin against Oxidative Stress: Implications for the Overall Protection Exerted by Melatonin

Journal of Physical Chemistry B

Volumn 119, Issue 27, 2015, Pages 8535-8543

  Álvarez Diduk, Ruslán ^a   Galano, Annia ^a   Tan, Dun Xian ^b   Reiter, Russel J ^b  

^a DEPARTAMENTO DE QUÍMICA   (Mexico)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLAVONOIDS; FREE RADICALS; HORMONES; OXIDATIVE STRESS; SOLUTIONS; SOLVENTS;

ABSOLUTE REACTIVITIES; FREE RADICAL SCAVENGING ACTIVITY; OH PRODUCTION; PEROXYL RADICAL; PHENOL MOIETY; RELATED COMPOUNDS; SCAVENGING ACTIVITIES; SOLVENT POLARITY;

DENSITY FUNCTIONAL THEORY;

6-HYDROXYMELATONIN; COPPER; HYDROXYL RADICAL; MELATONIN; N-ACETYLSEROTONIN; PERHYDROXYL RADICAL; PEROXIDE; SCAVENGER; SEROTONIN; SOLVENT; WATER;

ANALOGS AND DERIVATIVES; CHEMISTRY; DRUG EFFECTS; OXIDATIVE STRESS;

COPPER; FREE RADICAL SCAVENGERS; HYDROXYL RADICAL; MELATONIN; OXIDATIVE STRESS; PEROXIDES; SEROTONIN; SOLVENTS; WATER;

EID: 84937053699     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/acs.jpcb.5b04920     Document Type: Article

References (78)

1. Young, I. M.; Leone, R. M.; Francis, P.; Stovell, P.; Silman, R. E. Melatonin is metabolized to N-acetyl serotonin and 6-hydroxymelatonin in man J. Clin. Endocrinol. Metab. 1985, 60, 114-119
2. Zhou, H.; Wang, J.; Jiang, J.; Stavrovskaya, I. G.; Li, M.; Li, W.; Wu, Q.; Zhang, X.; Luo, C.; Zhou, S. et al. N-acetyl-serotonin offers neuroprotection through inhibiting mitochondrial death pathways and autophagic activation in experimental models of ischemic injury J. Neurosci. 2014, 34, 2967-2978
3. Jiang, J.; Yu, S.; Jiang, Z.; Liang, C.; Yu, W.; Li, J.; Du, X.; Wang, H.; Gao, X.; Wang, X. N-acetyl-serotonin protects hepg2 cells from oxidative stress injury induced by hydrogen peroxide Oxid. Med. Cell. Longev. 2014, 2014, 310504
4. Oxenkrug, G.; Requintina, P.; Bachurin, S. Antioxidant and antiaging activity of n-acetylserotonin and melatonin in the in vivo models Ann. N.Y. Acad. Sci. 2001, 939, 190-199
5. Bachurin, S.; Oxenkrug, G. F.; Lermontova, N.; Afanasiev, A.; Beznosko, B.; Vankin, G.; Shevtzova, E.; Mukhina, T.; Serkova, T. N-acetylserotonin, melatonin and their derivatives improve cognition and protect against β-amyloid-induced neurotoxicity Ann. N.Y. Acad. Sci. 1999, 890, 155-166
6. García, J. J.; Lõpez-Pingarrõn, L.; Almeida-Souza, P.; Tres, A.; Escudero, P.; García-Gil, F. A.; Tan, D. X.; Reiter, R. J.; Ramírez, J. M.; Bernal-Pérez, M. Protective effects of melatonin in reducing oxidative stress and in preserving the fluidity of biological membranes: A review J. Pineal Res. 2014, 56, 225-237
7. 2: Protection by melatonin and related molecules J. Pineal Res. 2000, 29, 54-61
8. Seeger, H.; Mueck, A. O.; Lippert, T. H. Effect of melatonin and metabolites on copper-mediated oxidation of low density lipoprotein Br. J. Clin. Pharmacol. 1997, 44, 283-284
9. Gozzo, A.; Lesieur, D.; Duriez, P.; Fruchart, J. C.; Teissier, E. Structure-activity relationships in a series of melatonin analogues with the low-density lipoprotein oxidation model Free Radical Biol. Med. 1999, 26, 1538-1543
10. Anderson, G.; Rodriguez, M. Multiple sclerosis: The role of melatonin and n-acetylserotonin Mult. Scler. Relat. Disord. 2015, 4, 112-123
11. García, J. J.; Reiter, R. J.; Karbownik, M.; Calvo, J. R.; Ortiz, G. G.; Tan, D. X.; Martínez-Ballarín, E.; Acua-Castroviejo, D. N-acetylserotonin suppresses hepatic microsomal membrane rigidity associated with lipid peroxidation Eur. J. Pharmacol. 2001, 428, 169-175
12. Longoni, B.; Pryor, W. A.; Marchiafava, P. Inhibition of lipid peroxidation by n-acetylserotonin and its role in retinal physiology Biochem. Biophys. Res. Commun. 1997, 233, 778-780
13. Wölfler, A.; Abuja, P. M.; Schauenstein, K.; Liebmann, P. M. N-acetylserotonin is a better extra- and intracellular antioxidant than melatonin FEBS Lett. 1999, 449, 206-210
14. Karbownik, M.; Gitto, E.; Lewiñski, A.; Reiter, R. J. Relative efficacies of indole antioxidants in reducing autoxidation and iron-induced lipid peroxidation in hamster testes J. Cell. Biochem. 2001, 81, 693-699
15. 2+ dependent lipid peroxidation of rod outer segment membranes of bovine retina J. Pineal Res. 2003, 35, 276-282
16. Maharaj, D. S.; Anoopkumar-Dukie, S.; Glass, B. D.; Antunes, E. M.; Lack, B.; Walker, R. B.; Daya, S. The identification of the uv degradants of melatonin and their ability to scavenge free radicals J. Pineal Res. 2002, 32, 257-261
17. Maharaj, D. S.; Walker, R. B.; Glass, B. D.; Daya, S. 6-hydroxymelatonin protects against cyanide induced oxidative stress in rat brain homogenates J. Chem. Neuroanat. 2003, 26, 103-107
18. Maharaj, D. S.; Maharaj, H.; Antunes, E. M.; Maree, D. M.; Nyokong, T.; Glass, B. D.; Daya, S. 6-hydroxymelatonin protects against quinolinic-acid-induced oxidative neurotoxicity in the rat hippocampus J. Pharm. Pharmacol. 2005, 57, 877-881
19. Maharaj, D. S.; Maharaj, H.; Daya, S.; Glass, B. D. Melatonin and 6-hydroxymelatonin protect against iron-induced neurotoxicity J. Neurochem. 2006, 96, 78-81
20. Maharaj, D. S.; Limson, J. L.; Daya, S. 6-hydroxymelatonin converts Fe(III) to Fe(II) and reduces iron-induced lipid peroxidation Life Sci. 2003, 72, 1367-1375
21. Pierrefiche, G.; Topall, G.; Courboin, G.; Henriet, I.; Laborit, H. Antioxidant activity of melatonin in mice Res. Commun. Chem. Pathol. Pharmacol. 1993, 80, 211-224
22. Tan, D. X.; Manchester, L. C.; Reiter, R. J.; Qi, W. B.; Karbownik, M.; Calvo, J. R. Significance of melatonin in antioxidative defense system: Reactions and products Biol. Signals Recept. 2000, 9, 137-159
23. Reiter, R. J.; Tan, D. X.; Galano, A. Melatonin: Exceeding expectations Physiology 2014, 29, 325-333
24. Zhang, H. M.; Zhang, Y. Melatonin: A well-documented antioxidant with conditional pro-oxidant actions J. Pineal Res. 2014, 57, 131-146
25. Galano, A. On the direct scavenging activity of melatonin towards hydroxyl and a series of peroxyl radicals Phys. Chem. Chem. Phys. 2011, 13, 7178-7188
26. Galano, A.; Tan, D. X.; Reiter, R. J. On the free radical scavenging activities of melatonin's metabolites, afmk and amk J. Pineal Res. 2013, 54, 245-257
27. Terpinc, P.; Abramovič, H. A kinetic approach for evaluation of the antioxidant activity of selected phenolic acids Food Chem. 2010, 121, 366-371
28. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A., et al. Gaussian 09, Gaussian, Inc.: Wallingford, CT, 2009.
29. Zhao, Y.; Schultz, N. E.; Truhlar, D. G. Design of density functionals by combining the method of constraint satisfaction with parametrization for thermochemistry, thermochemical kinetics, and noncovalent interactions J. Chem. Theory Comput. 2006, 2, 364-382
30. Marenich, A. V.; Cramer, C. J.; Truhlar, D. G. Universal solvation model based on solute electron density and on a continuum model of the solvent defined by the bulk dielectric constant and atomic surface tensions J. Phys. Chem. B 2009, 113, 6378-6396
31. Velez, E.; Quijano, J.; Notario, R.; Pabón, E.; Murillo, J.; Leal, J.; Zapata, E.; Alarcón, G. A computational study of stereospecifity in the thermal elimination reaction of menthyl benzoate in the gas phase J. Phys. Org. Chem. 2009, 22, 971-977
32. 2 from η-butanol-a simple yet exacting test for model chemistries? J. Comput. Chem. 2010, 31, 1236-1248
33. Furuncuoʇlu, T.; Uʇur, I.; Degirmenci, I.; Aviyente, V. Role of chain transfer agents in free radical polymerization kinetics Macromolecules 2010, 43, 1823-1835
34. Ando, H.; Fingerhut, B. P.; Dorfman, K. E.; Biggs, J. D.; Mukamel, S. Femtosecond stimulated raman spectroscopy of the cyclobutane thymine dimer repair mechanism: A computational study J. Am. Chem. Soc. 2014, 136, 14801-14810
35. Alves, T. V.; Alves, M. M.; Roberto-Neto, O.; Ornellas, F. R. Direct dynamics investigation of the reaction s(3p) + ch 4 → ch3 + sh(2π) Chem. Phys. Lett. 2014, 591, 103-108
36. Altarawneh, M.; Dlugogorski, B. Z. A mechanistic and kinetic study on the formation of pbdd/fs from pbdes Environ. Sci. Technol. 2013, 47, 5118-5127
37. Li, W.; Su, Z.; Hu, C. Mechanism of ketone allylation with allylboronates as catalyzed by zinc compounds: A dft study Chem.-Eur. J. 2013, 19, 124-134
38. Dargiewicz, M.; Biczysko, M.; Improta, R.; Barone, V. Solvent effects on electron-driven proton-transfer processes: Adenine-thymine base pairs Phys. Chem. Chem. Phys. 2012, 14, 8981-8989
39. Prasanthkumar, K. P.; Alvarez-Idaboy, J. R. An experimental and theoretical study of the kinetics and mechanism of hydroxyl radical reaction with 2-aminopyrimidine RSC Adv. 2014, 4, 14157-14164
40. Henao, D.; Murillo, J.; Ruiz, P.; Quijano, J.; Mejía, B.; Castañeda, L.; Notario, R. A computational study of the thermolysis of β-hydroxy ketones in gas phase and in m-xylene solution J. Phys. Org. Chem. 2012, 25, 883-887
41. Murillo, J.; Henao, D.; Vélez, E.; Castaño, C.; Quijano, J.; Gaviria, J.; Zapata, E. Thermal decomposition of 4-hydroxy-2-butanone in m-xylene solution: Experimental and computational study Int. J. Chem. Kinet. 2012, 44, 407-413
42. Galano, A.; Alvarez-Idaboy, J. R. Kinetics of radical-molecule reactions in aqueous solution: A benchmark study of the performance of density functional methods J. Comput. Chem. 2014, 35, 2019-2026
43. Zhao, Y.; Truhlar, D. G. How well can new-generation density functionals describe the energetics of bond-dissociation reactions producing radicals? J. Phys. Chem. A 2008, 112, 1095-1099
44. Okuno, Y. Theoretical investigation of the mechanism of the baeyer-villiger reaction in nonpolar solvents Chem.-Eur. J. 1997, 3, 212-218
45. Benson, S. W. The foundations of chemical kinetics. McGraw-Hill: San Francisco, CA, 1960.
46. Eyring, H. The activated complex in chemical reactions J. Chem. Phys. 1935, 3, 63-71
47. Evans, M. G.; Polanyi, M. Some applications of the transition state method to the calculation of reaction velocities, especially in solution Trans. Faraday Soc. 1935, 31, 875-894
48. Truhlar, D. G.; Garrett, B. C.; Klippenstein, S. J. Current status of transition-state theory J. Phys. Chem. 1996, 100, 12771-12800
49. Kuppermann, A.; Truhlar, D. G. Exact tunneling calculations J. Am. Chem. Soc. 1971, 93, 1840-1851
50. Galano, A.; Alvarez-Idaboy, J. R. A computational methodology for accurate predictions of rate constants in solution: Application to the assessment of primary antioxidant activity J. Comput. Chem. 2013, 34, 2430-2445
51. De Grey, A. D. N. J. Ho2·: The forgotten radical DNA Cell Biol. 2002, 21, 251-257
52. Belcastro, M.; Marino, T.; Russo, N.; Toscano, M. Structural and electronic characterization of antioxidants from marine organisms Theor. Chem. Acc. 2006, 115, 361-369
53. Leopoldini, M.; Russo, N.; Chiodo, S.; Toscano, M. Iron chelation by the powerful antioxidant flavonoid quercetin J. Agric. Food Chem. 2006, 54, 6343-6351
54. Leopoldini, M.; Rondinelli, F.; Russo, N.; Toscano, M. Pyranoanthocyanins: A theoretical investigation on their antioxidant activity J. Agric. Food Chem. 2010, 58, 8862-8871
55. Leopoldini, M.; Russo, N.; Toscano, M. The molecular basis of working mechanism of natural polyphenolic antioxidants Food Chem. 2011, 125, 288-306
56. Chiodo, S. G.; Leopoldini, M.; Russo, N.; Toscano, M. The inactivation of lipid peroxide radical by quercetin. A theoretical insight Phys. Chem. Chem. Phys. 2010, 12, 7662-7670
57. Leopoldini, M.; Chiodo, S. G.; Russo, N.; Toscano, M. Detailed investigation of the oh radical quenching by natural antioxidant caffeic acid studied by quantum mechanical models J. Chem. Theory Comput. 2011, 7, 4218-4233
58. Iuga, C.; Alvarez-Idaboy, J. R.; Russo, N. Antioxidant activity of trans-resveratrol toward hydroxyl and hydroperoxyl radicals: A quantum chemical and computational kinetics study J. Org. Chem. 2012, 77, 3868-3877
59. Perez-Gonzalez, A.; Munoz-Rugeles, L.; Alvarez-Idaboy, J. R. Tryptophan: Antioxidant or target of oxidative stress? A quantum chemistry elucidation RSC Adv. 2014, 4, 56128-56131
60. Galano, A.; Tan, D. X.; Reiter, R. J. Cyclic 3-hydroxymelatonin, a key metabolite enhancing the peroxyl radical scavenging activity of melatonin RSC Adv. 2014, 4, 5220-5227
61. Galano, A.; Medina, M. E.; Tan, D. X.; Reiter, R. J. Melatonin and its metabolites as copper chelating agents and their role in inhibiting oxidative stress: A physicochemical analysis J. Pineal Res. 2015, 58, 107-116
62. Weinstein, J.; Bielski, B. H. J. Kinetics of the interaction of ho2 and o2-radicals with hydrogen peroxide. The haber-weiss reaction J. Am. Chem. Soc. 1979, 101, 58-62
63. Brewer, G. J. Iron and copper toxicity in diseases of aging, particularly atherosclerosis and alzheimer's disease Exp. Biol. Med. 2007, 232, 323-335
64. Gaetke, L. M.; Chow, C. K. Copper toxicity, oxidative stress, and antioxidant nutrients Toxicology 2003, 189, 147-163
65. Aruoma, O. I.; Halliwell, B.; Gajewski, E.; Dizdaroglu, M. Copper-ion-dependent damage to the bases in DNA in the presence of hydrogen peroxide Biochem. J. 1991, 273, 601-604
66. Letelier, M. E.; Sánchez-Jofré, S.; Peredo-Silva, L.; Cortés-Troncoso, J.; Aracena-Parks, P. Mechanisms underlying iron and copper ions toxicity in biological systems: Pro-oxidant activity and protein-binding effects Chem. Biol. Interact. 2010, 188, 220-227
67. Bryantsev, V. S.; Diallo, M. S.; Goddard, W. A., III Computational study of copper(ii) complexation and hydrolysis in aqueous solutions using mixed cluster/continuum models J. Phys. Chem. A 2009, 113, 9559-9567
68. Ortega-Castro, J.; Adrover, M.; Frau, J.; Donoso, J.; Muñoz, F. Cu2+ complexes of some ages inhibitors Chem. Phys. Lett. 2009, 475, 277-284
69. Fujii, T.; Moynier, F.; Abe, M.; Nemoto, K.; Albarède, F. Copper isotope fractionation between aqueous compounds relevant to low temperature geochemistry and biology Geochim. Cosmochim. Acta 2013, 110, 29-44
70. Fulton, J. L.; Hoffmann, M. M.; Darab, J. G. An x-ray absorption fine structure study of copper(i) chloride coordination structure in water up to 325 °C Chem. Phys. Lett. 2000, 330, 300-308
71. Fulton, J. L.; Hoffmann, M. M.; Darab, J. G.; Palmer, B. J.; Stern, E. A. Copper(i) and copper(ii) coordination structure under hydrothermal conditions at 325 °C: An x-ray absorption fine structure and molecular dynamics study J. Phys. Chem. A 2000, 104, 11651-11653
72. Álvarez-Diduk, R.; Galano, A. Adrenaline and noradrenaline: Protectors against oxidative stress or molecular targets? J. Phys. Chem. B 2015, 119, 3479-3491
73. Halliwell, B.; Murcia, M. A.; Chirico, S.; Aruoma, O. I. Free radicals and antioxidants in food and in vivo: What they do and how they work Crit. Rev. Food Sci. Nutr. 1995, 35, 7-20
74. Halliwell, B.; Whiteman, M. Measuring reactive species and oxidative damage in vivo and in cell culture: How should you do it and what do the results mean? Br. J. Pharmacol. 2004, 142, 231-255
75. Alberto, M. E.; Russo, N.; Grand, A.; Galano, A. A physicochemical examination of the free radical scavenging activity of trolox: Mechanism, kinetics and influence of the environment Phys. Chem. Chem. Phys. 2013, 15, 4642-4650
76. Marino, T.; Galano, A.; Russo, N. Radical scavenging ability of gallic acid toward oh and ooh radicals. Reaction mechanism and rate constants from the density functional theory J. Phys. Chem. B 2014, 118, 10380-10389
77. León-Carmona, J. R.; Galano, A. Is caffeine a good scavenger of oxygenated free radicals? J. Phys. Chem. B 2011, 115, 4538-4546
78. Caicedo, C.; Iuga, C.; Castañeda-Arriaga, R.; Alvarez-Idaboy, J. R. Antioxidant activity of selected natural polyphenolic compounds from soybean via peroxyl radical scavenging RSC Adv. 2014, 4, 38918-38930