Antioxidant properties of β-carboline alkaloids are related to their antimutagenic and antigenotoxic activities

Mutagenesis

Volumn 22, Issue 4, 2007, Pages 293-302

  Moura, Dinara Jaqueline ^a   Richter, Marc François ^b   Boeira, Jane Marlei ^c   Pêgas Henriques, João Antonio ^a,b   Saffi, Jenifer ^a,b,d  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b UNIVERSIDADE LUTERANA DO BRASIL   (Brazil)

^c DEPARTMENT OF FOOD ENGINEERING   (Brazil)

^d Programa de Pós Graduação em Genética   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALOID DERIVATIVE; ANTIMUTAGENIC AGENT; BETA CARBOLINE; DIHYDRONORHARMAN; HARMALINE; HARMALOL; HARMAN; HARMINE; HARMOL; HYDROXYL RADICAL; PARAQUAT; REACTIVE OXYGEN METABOLITE; SCAVENGER; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; COMET ASSAY; CONTROLLED STUDY; GENOTOXICITY; MUTAGENICITY; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; YEAST CELL;

ALKALOIDS; ANIMALS; ANTIMUTAGENIC AGENTS; ANTIOXIDANTS; CARBOLINES; CELL LINE; COMET ASSAY; CRICETINAE; CRICETULUS; GENES, FUNGAL; HYDROGEN PEROXIDE; MUTATION; SACCHAROMYCES CEREVISIAE;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 34547679653     PISSN: 02678357     EISSN: 14643804     Source Type: Journal    
DOI: 10.1093/mutage/gem016     Document Type: Article

References (73)

1. Allen, J. R. F. and Holmested, B. R. (1980) The simple β-carboline alkaloids. Phytochemistry, 19, 1573-1582.
2. Adachi, J., Mizoi, Y., Naito, T., Yamamota, K., Fujiwara, S. and Ninomiya, I. (1991) Determination of β-carboline in foodstuffs by high-performance liquid chromatography and high-performance liquid chromatography-mass spectrometry. J. Chromatogr., 538, 331-339.
3. Gross, G. A., Turesky, L. B., Fay, L. B., Stillwell, W. G., Skipper, P. L. and Tannenbaum, S. R. (1993) Heterocyclic aromatic amine formation in grilled bacon, beef and fish and rill scrapings. Carcinogenesis, 14, 2313-2318.
4. Callaway, J. C., Raymon, L. P., Hearn, W. L., McKenna, D. J., Grob, C. S., Brito, G. S. and Mash, D. C. (1996) Quantification of N,N-dimethyltryptamine and harmala alkaloids in human plasma after oral dosing with ayahuasca. J. Anal. Toxicol., 20, 492-497.
5. Totsuka, Y. H., Ushiyama, H., Ishihara, J., Sinha, R., Goto, S., Sugimura, T. and Wakabayashi, K. (1999) Quantification of the co-mutagenic beta-carboline, norharman and harman, in cigarette smoke condensates and cooked foods. Cancer Lett., 143, 139-143.
6. Zheng, W., Wang, S., Barnes, L. F., Guan, Y. and Louis, E. D. (2000) Determination of harmane and harmine in human blood using reverse-phase high performance liquid chromatography and fluorescence detection. Anal. Biochem., 279, 125-129.
7. Freedland, C. S. and Mansbach, R. S. (1999) Behavioral profile of constituents in ayahuasca, an Amazonian psychoactive plant mixture. Drug Alcohol Depend., 54, 183-194.
8. Boeira, J. M., Viana, A. F., Picada, J. N. and Henriques, J. A. P. (2002) Genotoxic and recombinogenic activities of the two beta-carboline alkaloids harman and harmine in Saccharomyces cerevisiae. Mutat. Res., 500, 39-48.
9. Tse, S. Y. H., Mak, I. T. and Dickens, B. F. (1991) Antioxidative properties of harmane and β-carboline alkaloids. Biochem. Pharmacol., 42, 459-464.
10. Rommelspacher, H., May, T. and Salewski, B. (1994) Harman (1-methyl-beta-carboline) is a natural inhibitor of monoamine oxidase type A in rats. Eur. J. Pharmacol., 252, 51-59.
11. Kim, H., Sablin, S. O. and Ramsay, R. R. (1997) Inhibition of monoamine oxidase A by β-carboline derivates. Arch. Biochem. Biophys., 337, 137-142.
12. Herraiz, T. and Chaparro, C. (2005) Human monoamine oxidase is inhibited by tobacco smoke: β-carboline alkaloids act as potent and reversible inhibitors. Biochem. Biophys. Res. Commun., 326, 378-386.
13. Pimpinella, G. and Palmery, M. (1995) Interaction of β-carbolines with central dopaminergic transmission in mice: structure-activity relationships. Neurosci. Lett., 189, 121-124.
14. Grella, B., Dukat, M., Young, R., Teitler, M., Davis, K. H., Gauthier, C. B. and Glennon, R. A. (1998) Investigation of hallucinogenic and related β-carbolines. Drug Alcohol Depend., 50, 99-107.
15. Glennon, R. A., Dukat, M., Grella, B. et al. (2000) Binding of β-carbolines and relating agents at serotonin (5-HT2 and 5-HT1A), dopamine (D2) and benzodiazepines receptors. Drug Alcohol Depend., 60, 121-132.
16. Husbands, S. M., Glennon, R. A., Gorgerat, S., Gough, R., Tyacke, R., Nutt, D. J., Lewis, J. W. and Hudson, A. L. (2001) β-Carboline binding to imidazole receptors. Drug Alcohol Depend., 64, 203-208.
17. Squires, E. P., Hills, C. E., Rogers, G. J., Garland, P., Farley, S. R. and Morgan, N. G. (2004) The putative imidazoline receptor agonist, harmane, promotes intracellular calcium mobilization in pancreatic β-cells. Eur. J. Pharmacol., 501, 31-39.
18. Loew, G. H., Nienow, J., Lawson, J. A., Toll, L. and Uyeno, E. T. (1985) Theoretical structure-activity studies of β-carbolines analogs. Requirements of benzodiazepine receptor affinity and antagonist activity. Mol. Pharmacol., 28, 17-31.
19. Barbaccia, M. L., Ravizza, L. and Costa, E. (1986) Maprotiline: an anti-depressant with an unusual pharmacology profile. J. Pharmacol. Exp. Ther., 236, 307-312.
20. Fuller, R. W., Wong, C. J. and Hemrick-Luecke, S. K. (1986) MD240928 and harmaline: opposite selectivity in antagonism of the inactivation of types A and B monoamino oxidase by paragyline in mice. Life Sci., 38, 409-412.
21. Taira, Z., Kansawas, S., Dohara, C., Ishida, S., Matsumoto, M. and Ohsawa, M. (1997) Intercalation of six beta-carboline derivatives into DNA. Jpn. J. Toxicol. Environ. Health, 43, 83-91.
22. Balon, M., Munoz, M. A., Carmona, C., Guardado, P. and Galan, M. (1999) A fluorescent study of the molecular interactions of harmane with the nucleobases, their nucleosides and mononucleotides. Biophys. Chem., 80, 41-52.
23. Funayama, Y., Nishio, K., Wakabayashi, K., Nagao, M., Shimoi, K., Ohira, T., Hasegawa, S. and Saijo, N. (1996) Effects of β-and γ-carboline derivatives on DNA topoisomerases activities. Mutat. Res., 349, 183-191.
24. Wehner, F. C., Thiel, P. G. and Van Rensburg, S. J. (1979) Mutagenicity of alkaloids in the Salmonella/microsome systems. Mutat. Res., 66, 187-190.
25. Oda, Y., Nakamura, S. I. and Oki, I. (1988) Harman and norharman induces SOS responses and frameshift mutation in bacteria. Mutat. Res., 208, 39-44.
26. Picada, J. N., Silva, K. V. C. L., Erdtmann, B., Henriques, A. T. and Henriques, J. A. P. (1997) Genotoxic effects of structurally related β-carboline alkaloids. Mutat. Res., 379, 135-149.
27. Nakayasu, M., Nakasato, F., Sakamoto, H., Terada, M. and Sugimura, T. (1987) Mutagenic activity of norharman and harman in Chinese lung cells in assay with diphteria toxin resistance as a marker. Cancer Lett., 17, 249-255.
28. Boeira, J. M., Silva, J., Erdtmann, B. and Henriques, J. A. P. (2001) Genotoxic effects of the alkaloids harman and harmine by comet assay and chromosome aberration test in mammalian cells in vitro. Pharmacol. Toxicol., 89, 287-294.
29. Madle, E., Obe, G., Hansen, J. and Ristow, H. (1981) Harman and norharman: induction of sister-chromatid exchanges in human peripheral lymphocytes in vitro and interaction with isolated DNA. Mutat. Res., 90, 433-442.
30. Wakabayashi, K., Yahagi, T., Nagao, M. and Sugimura, T. (1982) Co-mutagenic effect of norharman with amino pyridine derivatives. Mutat. Res., 105, 205-210.
31. Sasaki, Y. F. and Shirasu, Y. (1993) Suppressing effects of S phase post-treatment with carbolines on sister-chromatid exchange induced by mitomycin C in Chinese hamster cells. Mutat. Res., 302, 165-171.
32. Sasaki, Y. F., Yamada, H., Símio, K., Kinae, N., Tomita, I., Matsumura, H., Ohta, T. and Shirasu, Y. (1992) Enhancing effects of heterocyclic amines and β-carbolines on the induction of chromosome aberration in culture mammalian cells. Mutat. Res., 269, 79-95.
33. 2. Korean J. Pharmacol., 31, 345-353.
34. Kim, H. H., Jang, Y. Y., Han, E. S. and Lee, C. S. (1999) Differential antioxidant effects of ambroxol, rutin, glutathione and harmaline. J. Appl. Pharmacol., 7, 112-120.
35. Maher, P. and Davis, J. B. (1996) The role of monoamine metabolism in oxidative glutamate toxicity. J. Neurosci., 16, 6394-6401.
36. Lee, C. S., Han, E. S., Jang, Y. Y., Han, J. H., Ha, H. W. and Kim, D. E. (2000) Protective effect of harmalol and harmaline on MPTP neurotoxicity in the mouse and dopamine-induced damage of brain mitochondria and PC12 cell. J. Neurochem., 75, 521-531.
37. Kim, D. H., Jang, Y. Y., Han, E. S. and Lee, C. S. (2001) Protective effect of harmaline and harmalol against dopamine and 6-hydroxydopamine-induced oxidative damage of brains mitochondria and synaptosomes, and viability loss of PC12 cells. Eur. J. Neurosci., 13, 1861-1872.
38. Park, T. H., Kwon, O. S., Park, S. Y., Han, E. S. and Lee, C. S. (2003) N-methylated β-carbolines protect PC12 cells from cytotoxic effects of MPP+ by attenuation of mitochondrial membrane permeability change. Neurosci. Res., 46, 349-358.
39. Wiseman, H. and Halliwell, B. (1996) Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem. J., 313, 17-29.
40. Stadtman, E. R. and Berlett, B. S. (1997) Reactive oxygen-mediated protein oxidation in aging and disease. Chem. Res. Toxicol., 10, 485-494.
41. Valko, M., Izakovic, M., Mazur, M., Rhodes, C. J. and Telser, J. (2004) Role of oxygen radicals in DNA damage and cancer incidence. Mol. Cell. Biochem., 266, 37-56.
42. Borek, C. (2001) Antioxidant health effects of aged garlic extract. Nutrition, 131, 1010S-1015S.
43. Zhang, W., Guo, Y. W. and Gu, Y. (2006) Secondary metabolites from the South China Sea invertebrates: chemistry and biological activity. Curr. Med. Chem., 13, 2041-2090.
44. Burke, D., Dawson, D. and Stearns, T. (2000) Methods in Yeast Genetics. Cold Spring Harbor Laboratory Course Manual. CSH Laboratory Press, Plainview, New York, pp 171-205.
45. Longo, V. D., Gralla, E. B. and Valentine, J. S. (1996) Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevisiae. J. Biol. Chem., 271, 12275-12280.
46. Cyrne, L., Martins, L., Fernandes, L. and Marinho, H. S. (2003) Regulation of antioxidant enzymes gene expression in the yeast Saccharomyces cerevisiae during stationary phase. Free Radic. Biol. Med., 34, 385-393.
47. Brendel, M., Grey, M., Maris, A. et al. (1988) Low glutathione pools in the original pso3 mutant of Saccharomyces cerevisiae are responsible for its pleiotropic sensitivity phenotype. Curr. Genet., 33, 4-9.
48. Whelan, W. L., Gocke, E. and Manney, T. R. (1979) The CAN1 locus of Saccharomyces cerevisiae: fine-structure analysis and forward mutation rates. Genetics, 91, 35-51.
49. Speit, G., Habermeier, B. and Helbig, R. (1994) Differences in the responses to mutagens between two V79 sublines. Mutat. Res., 325, 105-111.
50. Singh, N. P., McCoy, M. T., Tice, R. R. and Schneider, E. L. (1998) A simple technique for quantification of low levels of DNA damage in individual cell. Exp. Cell Res., 175, 184-191.
51. Hartmann, A. and Speit, G. (1997) The contribution of cytotoxicity to DNA-effects in the single cell gel test (comet assay). Toxicol. Lett., 90, 183-188.
52. Nadin, S. B., Vargas-Roig, L. M. and Ciocca, D. R. (2001) A silver staining method for single-cell gel assay. J. Histochem. Cytochem., 49, 1183-1186.
53. Tice, R. R., Agurell, E., Anderson, D et al. (2000) Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ. Mol. Mutagen., 35, 206-221.
54. Collins, A. R. (2004) The comet assay for DNA damage and repair: principles, applications, and limitations. Mol. Biotechnol., 26, 249-261.
55. Owen, R. W., Wimonwatwatee, T., Spiegelhalder, B. and Bartsch, H. (1996) A high performance liquid chromatography method for quantification of hydroxyl radical formation by determination of dihydroxy benzoic acids. Eur. J. Cancer Prev., 5, 233-240.
56. Owen, R. W., Haubner, R., Mier, W., Giacosa, A., Hull, W. E., Spiegelhalder, B. and Bartsch, H. (2003) Isolation, structure elucitation and antioxidant potential of the major phenolic and flavonoid compounds in brined olive drupes. Food Chem. Toxicol., 41, 703-717.
57. Halliwell, B. and Gutteridge, J. M. C. (2000) Free Radicals in Biology and Medicine. 3rd ed. Oxford University Press, New York.
58. 2.- in the production of HO.: in vitro and in vivo. Free Radic. Biol. Med., 16, 29-33.
59. Freitas, J. M., Liba, A., Meneghini, R., Valentine, J. S. and Gralla, E. B. (1999) Yeast lacking Cu-Zn superoxide dismutase show altered iron homeostasis. J. Biol. Chem., 275, 11645-11649.
60. Bayliak, M., Semchyshyn, H. and Lushchak, V. (2006) Effect of hydrogen peroxide on antioxidant enzyme activities in Saccharomyces cerevisiae is strain-specific. Biochemistry (Mosc.), 71, 1013-1020.
61. Ikner, A. and Shiozaki, K. (2005) Yeast signaling pathways in the oxidative stress response. Mutat. Res., 569, 13-27.
62. Coleman, S. T., Epping, E. A., Steggerda, S. M. and Rowley, S. M. (1999) Yap1p activates gene transcription in an oxidant-specific fashion. Mol. Cell. Biol., 19, 8302-8313.
63. Ames, B. N. and Gold, L. S. (1991) Endogenous mutagens and the causes of aging and cancer. Mutat. Res., 250, 13-16.
64. Singal, P. K., Khaper, N., Palace, V. and Kumar, D. (1998) The role of oxidative stress in the genesis of heart disease. Cardiovasc. Res., 40, 426-432.
65. Dizdaroglu, M. (1991) Chemical determination of free radical-induced damage to DNA. Free Radic. Biol. Med., 10, 225-242.
66. Lee, D. H., O'Connor, T. R. and Pfeifer, G. P. (2002) Oxidative DNA damage induced by copper and hydrogen peroxide promotes CG-TT tandem mutations at methylated CpG dinucleotides in nucleotide excision repair-deficient cells. Nucleic Acids Res., 30, 3566-3573.
67. Fridovich, I. (1998) Oxygen toxicity: a radical explanation. J. Exp. Biol., 201, 1203-1209.
68. Zhao, C., Dodin, G., Yuan, C., Chen, H., Zheng, R., Jia, Z. and Fan, B. T. (2005) In vitro protection of DNA from Fenton reaction by plant polyphenol verbascoside. Biochim. Biophys. Acta, 1723, 114-123.
69. Uemura, T., Kanashiro, M., Hirai, K. and Miyazaki, N. (1988) Isolation structure and properties of the β-carboline alkaloids formed from 5-hydroxytryptamine by the superoxide anion-generating systems. J. Neurochem., 51, 710-717.
70. DeFelippis, M. R., Murthy, C. P., Faraggi, M. and Klapper, M. H. (1989) Pulse radiolytic measurement of redox potential: the tyrosine and tryptophan radical. Biochemistry, 28, 4847-4853.
71. Christen, S., Peterhans, E. and Stocker, R. (1990) Antioxidant activities of some tryptophan metabolites: possible implication for inflammatory disease. Proc Natl Acad Sci USA, 87, 2506-2510.
72. Hayashi, K., Nagao, M. and Sugimura, T. (1977) Interaction of norharman and harman with DNA. Nucleic Acids Res., 4, 3679-3685.
73. Duportail, G. and Lami, H. (1975) Studies of the interaction of the fluorophores harmine and harmaline with calf thymus DNA. Biochim. Biophys. Acta, 402, 20-30.