Inhibition of monoamine oxidase (MAO) by β-carbolines and their interactions in live neuronal (PC12) and liver (HuH-7 and MH1C1) cells

Toxicology in Vitro

Volumn 28, Issue 3, 2014, Pages 403-410

  Santillo, Michael F ^a   Liu, Yitong ^a   Ferguson, Martine ^a   Vohra, Sanah N ^a   Wiesenfeld, Paddy L ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

Botanical; Cell assay; Combination index; Harmaline; Harmine; Methylene blue

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME A; AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME B; BETA CARBOLINE DERIVATIVE; HARMALINE; HARMALOL; HARMAN; HARMINE; KYNURAMINE; METHYLENE BLUE;

ANIMAL CELL; ARTICLE; CELL ASSAY; CELL INTERACTION; CELL LYSATE; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HEPATOMA CELL; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; NONHUMAN; PC12 CELL; PHEOCHROMOCYTOMA CELL; RAT;

BOTANICAL; CELL ASSAY; COMBINATION INDEX; HARMALINE; HARMINE; METHYLENE BLUE;

ALKALOIDS; ANIMALS; CARBOLINES; CELL LINE; CELL LINE, TUMOR; HUMANS; LIVER; MODELS, BIOLOGICAL; MONOAMINE OXIDASE; MONOAMINE OXIDASE INHIBITORS; PC12 CELLS; RATS; SPECIES SPECIFICITY;

EID: 84892453839     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2013.12.006     Document Type: Article

References (54)

1. Bland J.M., Altman D.G. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1986, 327:307-310. 10.1016/S0140-6736(86)90837-8.
2. Bland J.M., Altman D.G. Measuring agreement in method comparison studies. Stat. Meth. Med. Res. 1999, 8:135-160. 10.1177/096228029900800204.
3. Boyer E.W., Shannon M. The serotonin syndrome. New Engl. J. Med. 2005, 352:1112-1120. 10.1056/NEJMra041867.
4. Brown H.S., Wilby A.J., Alder J., Houston J.B. Comparative use of isolated hepatocytes and hepatic microsomes for cytochrome P450 inhibition studies: transporter-enzyme interplay. Drug Metabol. Dispos. 2010, 38:2139-2146. 10.1124/dmd.110.035824.
5. Brush D.E., Bird S.B., Boyer E.W. Monoamine oxidase inhibitor poisoning resulting from internet misinformation on illicit substances. Clin. Toxicol. 2004, 42:191-195. 10.1081/clt-120030949.
6. Callaway J.C., Raymon L.P., Hearn W.L., McKenna D.J., Grob C.S., Brito G.S., Mash D.C. Quantitation of N, N-dimethyltryptamine and harmala alkaloids in human plasma after oral dosing with ayahuasca. J. Anal. Toxicol. 1996, 20:492-497. 10.1093/jat/20.6.492.
7. Callaway J.C., McKenna D.J., Grob C.S., Brito G.S., Raymon L.P., Poland R.E., Andrade E.N., Andrade E.O., Mash D.C. Pharmacokinetics of Hoasca alkaloids in healthy humans. J. Ethnopharmacol. 1999, 65:243-256. 10.1016/S0378-8741(98)00168-8.
8. Chou T.-C. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol. Rev. 2006, 58:621-681. 10.1124/pr.58.3.10.
9. Coecke S., Eskes C., Gartlon J., Kinsner A., Price A., van Vliet E., Prieto P., Boveri M., Bremer S., Adler S., Pellizzer C., Wendel A., Hartung T. The value of alternative testing for neurotoxicity in the context of regulatory needs. Environ. Toxicol. Pharmacol. 2006, 21:153-167. 10.1016/j.etap.2005.07.006.
10. Dhawan K., Dhawan S., Sharma A. Passiflora: a review update. J. Ethnopharmacol. 2004, 94:1-23. 10.1016/j.jep.2004.02.023.
11. Disanto A.R., Wagner J.G. Pharmacokinetics of highly ionized drugs II: methylene blue-absorption, metabolism, and excretion in man and dog after oral administration. J. Pharm. Sci. 1972, 61:1086-1090. 10.1002/jps.2600610710.
12. Douglas K.T., Sharma R.K., Walmsley J.F., Hider R.C. Ionization processes of some harmala alkaloids. Mol. Pharmacol. 1983, 23:614-618.
13. Fisher A.A., Purcell P., Le Couteur D.G. Toxicity of Passiflora incarnata L. Clin. Toxicol. 2000, 38:63-66. 10.1081/CLT-100100919.
14. Frison G., Favretto D., Zancanaro F., Fazzin G., Ferrara S.D. A case of β-carboline alkaloid intoxication following ingestion of Peganum harmala seed extract. For. Sci. Intl. 2008, 179:e37-e43. 10.1016/j.forsciint.2008.05.003.
15. Gable R.S. Risk assessment of ritual use of oral dimethyltryptamine (DMT) and harmala alkaloids. Addiction 2007, 102:24-34. 10.1111/j.1360-0443.2006.01652.x.
16. Gillman P.K. CNS toxicity involving methylene blue: the exemplar for understanding and predicting drug interactions that precipitate serotonin toxicity. J. Psychopharmacol. 2011, 25:429-436. 10.1177/0269881109359098.
17. Ginovart N., Meyer J.H., Boovariwala A., Hussey D., Rabiner E.A., Houle S., Wilson A.A. Positron emission tomography quantification of [11C]-harmine binding to monoamine oxidase-A in the human brain. J. Cereb. Blood Flow Metab. 2005, 26:330-344. 10.1038/sj.jcbfm.9600197.
18. Greene L.A., Tischler A.S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. USA 1976, 73:2424-2428.
19. Guan Y., Louis E.D., Zheng W. Toxicokinetics of tremorogenic natural products, harmane and harmine, in male Sprague-Dawley rats. J. Toxicol. Environ. Health A 2001, 64:645-660. 10.1080/152873901753246241.
20. Herraiz T., Gonzalez D., Ancin-Azpilicueta C., Aran V.J., Guillen H. β-Carboline alkaloids in Peganum harmala and inhibition of human monoamine oxidase (MAO). Food Chem. Toxicol. 2010, 48:839-845. 10.1016/j.fct.2009.12.019.
21. Kalgutkar A.S., Dalvie D.K., Castagnoli N., Taylor T.J. Interactions of nitrogen-containing xenobiotics with monoamine oxidase (MAO) isozymes A and B: SAR studies on MAO substrates and inhibitors. Chem. Res. Toxicol. 2001, 14:1139-1162. 10.1021/tx010073b.
22. Krajl M. A rapid microfluorimetric determination of monoamine oxidase. Biochem. Pharmacol. 1965, 14:1684-1685. 10.1016/0006-2952(65)90025-0.
23. Lawrence K.R., Adra M., Gillman P.K. Serotonin toxicity associated with the use of linezolid: a review of postmarketing data. Clin. Infectious Diseases 2006, 42:1578-1583. 10.1086/503839.
24. Manly S. In vitro biochemical screening. J. Biomol. Screen. 1997, 2:197-199. 10.1177/108705719700200402.
25. Matsumoto T., Suzuki O., Furuta T., Asai M., Kurokawa Y., Nimura Y., Katsumata Y., Takahashi I. A sensitive fluorometric assay for serum monoamine oxidase with kynuramine as substrate. Clin. Biochem. 1985, 18:126-129. 10.1016/S0009-9120(85)80094-1.
26. McCabe-Sellers B.J., Staggs C.G., Bogle M.L. Tyramine in foods and monoamine oxidase inhibitor drugs: a crossroad where medicine, nutrition, pharmacy, and food industry converge. J. Food Composition Anal. 2006, 19:S58-S65. 10.1016/j.jfca.2005.12.008.
27. McKenna D.J., Towers G.H.N., Abbott F. Monoamine oxidase inhibitors in South American hallucinogenic plants: tryptamine and β-carboline constituents of ayahuasca. J. Ethnopharmacol. 1984, 10:195-223. 10.1016/0378-8741(84)90003-5.
28. Moncrieff J. Determination of pharmacological levels of harmane, harmine and harmaline in mammalian brain tissue, cerebrospinal fluid and plasma by high-performance liquid chromatography with fluorimetric detection. J. Chromatogr. B 1989, 496:269-278. 10.1016/S0378-4347(00)82576-1.
29. Moore K., Rees S. Cell-based versus isolated target screening: how lucky do you feel?. J. Biomol. Screen. 2001, 6:69-74. 10.1177/108705710100600202.
30. Morinan A., Garratt H.M. An improved fluorimetric assay for brain monoamine oxidase. J. Pharmacol. Meth. 1985, 13:213-223. 10.1016/0160-5402(85)90021-X.
31. Moroi K., Kuga T. Estimation of harmine and its derivatives by HPLC: correlation of brain harmine levels with jumping behavior in rats. Jpn. J. Pharmacol. 1987, 43:33-41. 10.1254/jjp.43.33.
32. Nakabayashi H., Taketa K., Miyano K., Yamane T., Sato J. Growth of human hepatoma cell lines with differentiated functions in chemically defined medium. Cancer Res. 1982, 42:3858-3863.
33. Ochiai Y., Itoh K., Sakurai E., Adachi M., Tanaka Y. Substrate selectivity of monoamine oxidase A, monoamine oxidase B, diamine oxidase, and semicarbazide-sensitive amine oxidase in COS-1 expression systems. Biol. Pharm. Bull. 2006, 29:2362-2366. 10.1248/bpb.29.2362.
34. Oz M., Lorke D.E., Hasan M., Petroianu G.A. Cellular and molecular actions of methylene blue in the nervous system. Med. Res. Rev. 2011, 31:93-117. 10.1002/med.20177.
35. Peter C., Hongwan D., Küpfer A., Lauterburg B.H. Pharmacokinetics and organ distribution of intravenous and oral methylene blue. Eur. J. Clin. Pharmacol. 2000, 56:247-250. 10.1007/s002280000124.
36. Riba J., Valle M., Urbano G., Yritia M., Morte A., Barbanoj M.J. Human pharmacology of Ayahuasca: subjective and cardiovascular effects, monoamine metabolite excretion, and pharmacokinetics. J. Pharmacol. Exp. Ther. 2003, 306:73-83. 10.1124/jpet.103.049882.
37. Richardson U.I., Tashjian A.H., Levine L. Establishment of a clonal strain of hepatoma cells which secrete albumin. J. Cell Biol. 1969, 40:236-247. 10.1083/jcb.40.1.236.
38. Salonen J.S., Nyman L., Boobis A.R., Edwards R.J., Watts P., Lake B.G., Price R.J., Renwick A.B., Gómez-Lechón M.-J., Castell J.V., Ingelman-Sundberg M., Hidestrand M., Guillouzo A., Corcos L., Goldfarb P.S., Lewis D.F.V., Taavitsainen P., Pelkonen O. Comparative studies on the cytochrome P450-associated metabolism and interaction potential of selegiline between human liver-derived in vitro systems. Drug Metabol. Dispos. 2003, 31:1093-1102. 10.1124/dmd.31.9.1093.
39. Saura J., Nadal E., van den Berg B., Vila M., Bombi J.A., Mahy N. Localization of monoamine oxidases in human peripheral tissues. Life Sci. 1996, 59:1341-1349. 10.1016/0024-3205(96)00459-6.
40. Shih J.C., Chen K., Ridd M.J. Monoamine oxidase: from genes to behavior. Ann. Rev. Neurosci. 1999, 22:197-217. 10.1146/annurev.neuro.22.1.197.
41. Shulman K.I., Walker S.E. Refining the MAOI diet: tyramine content of pizzas and soy products. J. Clin. Psychiat. 1999, 60:191-193.
42. Sklerov J., Levine B., Moore K.A., King T., Fowler D. A fatal intoxication following the ingestion of 5-methoxy-N, N-dimethyltryptamine in an ayahuasca preparation. J. Anal. Toxicol. 2005, 29:838-841. 10.1093/jat/29.8.838.
43. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., Fujimoto E.K., Goeke N.M., Olson B.J., Klenk D.C. Measurement of protein using bicinchoninic acid. Anal. Biochem. 1985, 150:76-85. 10.1016/0003-2697(85)90442-7.
44. Strolin Benedetti M., Tipton K.F., Whomsley R. Amine oxidases and monooxygenases in the invivo metabolism of xenobiotic amines in humans: has the involvement of amine oxidases been neglected?. Fund Clin. Pharmacol. 2007, 21:467-480. 10.1111/j.1472-8206.2007.00498.x.
45. Taavitsainen P., Anttila M., Nyman L., Karnani H., Salonen J.S., Pelkonen O. Selegiline metabolism and cytochrome P450 enzymes: in vitro study in human liver microsomes. Pharmacol. Toxicol. 2000, 86:215-221. 10.1034/j.1600-0773.2000.pto860504.x.
46. Thorne N., Auld D.S., Inglese J. Apparent activity in high-throughput screening: origins of compound-dependent assay interference. Curr. Opin. Chem. Biol. 2010, 14:315-324. 10.1016/j.cbpa.2010.03.020.
47. Tufvesson G. Fluorometric determination of amine oxidase activity in human blood serum with kynuramine as substrate. Scand. J. Clin. Lab Invest. 1970, 26:151-154. 10.3109/00365517009049227.
48. Valley M.P., Zhou W., Hawkins E.M., Shultz J., Cali J.J., Worzella T., Bernad L., Good T., Good D., Riss T.L., Klaubert D.H., Wood K.V. A bioluminescent assay for monoamine oxidase activity. Anal. Biochem. 2006, 359:238-246. 10.1016/j.ab.2006.09.035.
49. Youdim M.B.H., Heldman E., Pollard H.B., Fleming P., McHugh E. Contrasting monoamine oxidase activity and tyramine induced catecholamine release in PC12 and chromaffin cells. Neuroscience 1986, 19:1311-1318. 10.1016/0306-4522(86)90145-4.
50. Youdim M.B.H., Edmondson D., Tipton K.F. The therapeutic potential of monoamine oxidase inhibitors. Nat. Rev. Neurosci. 2006, 7:295-309. 10.1038/nrn1883.
51. Yuruktumen A., Karaduman S., Bengi F., Fowler J. Syrian rue tea: a recipe for disaster. Clin. Toxicol. 2008, 46:749-752. 10.1080/15563650701323205.
52. Zetler G., Back G., Iven H. Pharmacokinetics in the rat of the hallucinogenic alkaloids harmine and harmaline. Naunyn-Schmiedeberg's Arch. Pharmacol. 1974, 285:273-292. 10.1007/BF00498996.
53. Zhou M., Panchuk-Voloshina N. A one-step fluorometric method for the continuous measurement of monoamine oxidase activity. Anal. Biochem. 1997, 253:169-174. 10.1006/abio.1997.2392.
54. Zhou M., Diwu Z., Panchuk-Voloshina N., Haugland R.P. A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: Applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Anal. Biochem. 1997, 253:162-168. 10.1006/abio.1997.2391.