Inhibition of CYP1 by berberine, palmatine, and jatrorrhizine: Selectivity, kinetic characterization, and molecular modeling

Toxicology and Applied Pharmacology

Volumn 272, Issue 3, 2013, Pages 671-680

  Lo, Sheng Nan ^a,b   Chang, Yu Ping ^a   Tsai, Keng Chang ^a   Chang, Chia Yu ^a,d   Wu, Tian Shung ^c   Ueng, Yune Fang ^a,b,d  

^a NATIONAL RESEARCH INSTITUTE OF CHINESE MEDICINE   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^d TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Berberine; CYP1B1; Selective inhibition

Indexed keywords

7 ETHOXYCOUMARIN; ASPARAGINE; BENZO[A]PYRENE; BERBERINE; CYTOCHROME P450; CYTOCHROME P450 1A1; CYTOCHROME P450 1A1.1; CYTOCHROME P450 1A2; CYTOCHROME P450 1A2.1; CYTOCHROME P450 1B1; CYTOCHROME P450 1B1.1; CYTOCHROME P450 1B1.3; CYTOCHROME P450 1B1.4; JATRORRHIZINE; METHOXYRESORUFIN; PALMATINE; RESORUFIN DERIVATIVE; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; COMPARATIVE STUDY; COMPETITIVE INHIBITION; CONJUGATION; CONTROLLED STUDY; COPTIS CHINENSIS; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME KINETICS; HUMAN; HYDROGEN BOND; HYDROXYLATION; IC 50; MOLECULAR MODEL; SITE DIRECTED MUTAGENESIS; TISSUE DISTRIBUTION; WILD TYPE;

7-ETHOXYCOUMARIN O-DEETHYLATION; 7-ETHOXYRESORUFIN O-DEETHYLATION; 7-METHOXYRESORUFIN O-DEMETHYLATION; AHH; BENZO(A)PYRENE HYDROXYLASE; BERBERINE; CYP1B1; CYTOCHROME P450; ECOD; EROD; MROD; P450, CYP; SELECTIVE INHIBITION;

ARYL HYDROCARBON HYDROXYLASES; BERBERINE; BERBERINE ALKALOIDS; COMPUTER SIMULATION; CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 CYP1A2; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; MODELS, MOLECULAR; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84884709754     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2013.07.005     Document Type: Article

References (47)

1. Aklillu E., Oscarson M., Hidestrand M., Leidvik B., Otter C., Ingelman-Sundberg M. Functional analysis of six different polymorphic CYP1B1 enzyme variants found in an Ethiopian population. Mol. Pharmacol. 2002, 61:586-594.
2. Aklillu E., Øverbø S., Botnen I.V., Otter C., Ingelman-Sundberg M. Characterization of common CYP1B1 variants with different capacity for benzo(a)pyrene-7,8-dihydrodiol epoxide formation from benzo(a)pyrene. Cancer Res. 2005, 65:5105-5111.
3. Bailey L.R., Roodi N., Dupont W.D., Parl F.F. Association of cytochrome P450 1B1 (CYP1B1) polymorphism with steroid receptor status in breast cancer. Cancer Res. 1998, 58:5038-5041.
4. Chatterjee P., Franklin M.R. Human cytochrome P450 inhibition and metabolic-intermediate complex formation by goldenseal extract and its methylenedioxyphenyl components. Drug Metab. Dispos. 2003, 31:1391-1397.
5. Choudhary D., Jansson I., Stoilov I., Sarfarazi M., Schenkman J.B. Metabolism of retinoids and arachidonic acid by human and mouse cytochrome P450 1B1. Drug Metab. Dispos. 2004, 32:840-847.
6. Chu C.C., Pan K.L., Yao H.T., Hsu T.A. Development of a whole-cell screening system for evaluation of the human CYP1A2-mediated metabolism. Biotechnol. Bioeng. 2011, 108:2932-2940.
7. Chun Y.J., Oh Y.K., Kim S., Kim D., Lee S.K., Guengerich F.P. A new selective and potent inhibitor of human cytochrome P450 1B1 and its application to antimutagenesis. Cancer Res. 2001, 61:8164-8170.
8. Douglas J.A., Follett J.M., Parmenter G.A., Sansom C.E., Perry N.B., Littler R.A. Seasonal variation of biomass and bioactive alkaloid content of goldenseal, Hydrastis Canadensis. Fitoterapia 2010, 81:925-928.
9. Gajjar K., Martin-Hirsch P.L., Martin F.L. CYP1B1 and hormone-induced cancer. Cancer Lett. 2012, 324:13-30.
10. Greenlee W.F., Poland A. An improved assay of 7-ethoxycoumarin deethylase activity: induction of hepatic enzyme activity in C57BL/6J and DBA/2J mice by phenobarbital, 3-methylcholanthrene and 2,3,7,8-tetrachlorodibenzo-p-dioxin. J. Pharmacol. Exp. Ther. 1978, 205:596-605.
11. Grycova L., Dostal J., Marek R. Quaternary protoberberine alkaloids. Phytochemistry 2007, 68:150-157.
12. Guo Y., Chen Y., Tan Zr, Klaassen C.D., Zhou Hh. Repeated administration of berberine inhibits cytochromes P450 in humans. Eur. J. Clin. Pharmacol. 2012, 68:213-217.
13. Han Y.L., Yu H.L., Li D., Meng X.L., Zhou Z.Y., Yu Q., Zhang X.Y., Wang F.J., Guo C. In vitro inhibition of Huanglian[Rhizoma coptidis (L.)] and its six active alkaloids on six cytochrome P450 isoforms in human liver microsomes. Phytother. Res. 2011, 25:1660-1665.
14. Hanna I.H., Dawling S., Roodi N., Guengerich F.P., Parl F.F. Cytochrome P450 1B1 (CYP1B1) pharmacogenetics: association of polymorphisms with functional differences in estrogen hydroxylation activity. Cancer Res. 2000, 60:3440-3444.
15. Hevir N., Šinkovec J., Rižner T.L. Disturbed expression of phase I and phase II estrogen-metabolizing enzymes in endometrial cancer: lower levels of CYP1B1 and increased expression of S-COMT. Mol. Cell. Endocrinol. 2011, 331:158-167.
16. Jennings B.L., Sahan-Firat S., Estes A.M., Das K., Farjana N., Fang X.R., Gonzalez F.J., Malik K.U. Cytochrome P450 1B1 contributes to angiotensin II-induced hypertension and associated pathophysiology. Hypertension 2010, 56:667-674.
17. Jennings B.L., Anderson L.J., Estes A.M., Yaghini F.A., Fang X.R., Porter J., Gonzalez F.J., Campbell W.B., Malik K.U. Cytochrome P450 1B1 contributes to renal dysfunction and damage caused by angiotensin II in mice. Hypertension 2012, 59:348-354.
18. Jennings B.L., Anderson L.J., Estes A.M., Fang X.R., Song C.Y., Campbell W.B., Malik K.U. Involvement of cytochrome P-450 1B1 in renal dysfunction, injury, and inflammation associated with angiotensin II-induced hypertension in rats. Am. J. Physiol. Renal Physiol. 2012, 302:F408-F420.
19. Kang D.E., Sohn E.J., Kwon E.K., Han J.H., Oh H., Lee H.S. Effects of berberine on angiotensin-converting enzyme and NO/cGMP system in vessels. Vascul. Pharmacol. 2003, 39:281-286.
20. Kim T., Park H., Yue W., Wang J.P., Atkins K.A., Zhang Z., Rogan E.G., Cavalieri E.L., Mohammad K.S., Kim S., Santen R.J., Aiyar S.E. Tetra-methoxystilbene modulates ductal growth of the developing murine mammary gland. Breast Cancer Res. Treat. 2011, 126:779-789.
21. Kulkarni S.K., Dhir A. Berberine: a plant alkaloid with therapeutic potential for central nervous system disorders. Phytochemistry 2010, 24:317-324.
22. Lee H.S., Jin C., Park J., Kim D.H. Modulation of cytochrome P450 activities by 7,8-benzoflavone and its metabolites. Biochem. Mol. Biol. Int. 1994, 34:483-491.
23. Lee A.J., Cai M.J., Thomas P.E., Conney A.H., Zhu B.T. Characterization of the oxidative metabolites of 17β-estradiol and estrone formed by 15 selectively expressed human cytochrome P450 isoforms. Endocrinology 2003, 144:3382-3398.
24. Lewis D.F.V., Lake B.G., George S.G., Dickins M., Eddershaw P.J., Tarbit M.H., Beresford A.P., Goldfarb P.S., Guengerich F.P. Molecular modelling of CYP1 family enzymes CYP1A1, CYP1A2, CYP1A6 and CYP1B1 based on sequence homology with CYP102. Toxicology 1999, 139:53-79.
25. Li Y., Ren G., Wang Y.X., Kong W.J., Yang P., Wang Y.M., Li Y.H., Yi H., Li Z.R., Song D.Q., Jiang J.D. Bioactivities of berberine metabolites after transformation through P450 isoenzymes. J. Transl. Med. 2011, 9:62-71.
26. Liu J., Nguyen T.T., Dupart P.S., Sridhar J., Zhang X., Zhu Z., Stevens C.L.K., Foroozesh M. 7-Ethynylcoumarins: selective inhibitors of human cytochrome P450s 1A1 and 1A2. Chem. Res. Toxicol. 2012, 25:1047-1057.
27. Malik K.U., Jennings B.L., Yaghini F.A., Sahan-Firat S., Song C.Y., Estes A.M., Fang X.R. Contribution of cytochrome P450 1B1 to hypertension and associated pathophysiology: a novel target for antihypertensive agents. Prostaglandins Other Lipid Mediat. 2012, 98:69-74.
28. Mikstacka R., Rimando A.M., Dutkiewicz Z., Stefański T., Sobiak S. Design, synthesis and evaluation of the inhibitory selectivity of novel trans-resveratrol analogues on human recombinant CYP1A1, CYP1A2 and CYP1B1. Bioorg. Med. Chem. 2012, 20:5117-5126.
29. Nebert D.W., Gelboin H.V. Substrate-inducible microsomal aryl hydroxylase in mammalian cell culture. I. Assembly and properties of induced enzyme. J. Biol. Chem. 1968, 243:6242-6249.
30. Omura T., Sato R. The carbon monoxide-binding pigment of liver microsomes. l. Evidence for its hemeprotein nature. J. Biol. Chem. 1964, 239:2370-2379.
31. Paracchini V., Raimondi S., Gram I.T., Kang D., Kocabas N.A., Kristensen V.N., Li D., Parl F.F., Rylander-Rudqvist T., Souček P., Zheng W., Wedren S., Taioli E. Meta- and pooled analyses of the cytochrome P-450 1B1 Val432Leu polymorphism and breast cancer: a HuGE-GSEC review. Am. J. Epidemiol. 2007, 165:115-125.
32. Parikh A., Gillam E.M.J., Guengerich F.P. Drug metabolism by Escherichia coli expressing human cytochrome P450. Nat. Biotechnol. 1997, 15:784-788.
33. Phillips A.H., Langdon R.G. Hepatic triphosphopyridine nucleotide-cytochrome c reductase: isolation, characterization, and kinetic studies. J. Biol. Chem. 1962, 237:2652-2660.
34. Pohl R.J., Fouts J.R. A rapid method for assaying the metabolism of 7-ethoxyresorufin by microsomal subcellular fractions. Anal. Biochem. 1980, 107:150-155.
35. +-ATPase from Kluyveromyces lactis. Biochemistry 2007, 46:5616-5622.
36. Shimada T., Hayes C.L., Yamazaki H., Amin S., Hecht S.S., Guengerich F.P., Sutter T.R. Activation of chemically diverse procarcinogens by human cytochrome P-450 1B1. Cancer Res. 1996, 56:2979-2984.
37. Shimada T., Wunsch R.M., Hanna I.H., Sutter T.R., Guengerich F.P., Gillam E.M.J. Recombinant human cytochrome P450 1B1 expression in Escherichia coli. Arch. Biochem. Biophys. 1998, 357:111-120.
38. Shimada T., Yamazaki H., Foroozesh M., Hopkins N.E., Alworth W.L., Guengerich F.P. Selectivity of polycyclic inhibitors for human cytochrome P450s 1A1, 1A2, and 1B1. Chem. Res. Toxicol. 1998, 11:1048-1056.
39. Su C.R., Ueng Y.F., Dung N.X., Reddy V.B., Wu T.S. Cytochrome P450 3A4 inhibitors and other constituents of Fibraurea tinctoria. J. Nat. Prod. 2007, 70:1930-1933.
40. Sutter T.R., Tang Y.M., Hayes C.L., Wo Y.Y.P., Jabd E.W., Li X., Yin H., Cody C.W., Greenlee W.F. Complete cDNA sequence of a human dioxin-inducible mRNA identifies a new gene subfamily of cytochrome P450 that maps to chromosome 2. J. Biol. Chem. 1994, 269:13092-13099.
41. Tang J., Feng Y., Tsao S., Wang N., Cuttain R., Wang Y. Berberine and Coptidis Rhizoma as novel antineoplastic agents: a review of traditional use and biomedical investigations. J. Ethnopharmacol. 2009, 126:5-17.
42. Vrzal R., Zdarilova A., Ulrichova J., Blaha L., Giesy J.P., Dvorak Z. Activation of the aryl hydrocarbon receptor by berberine in HepG2 and H4IIE cells: biphasic effect on CYP1A1. Biochem. Pharmacol. 2005, 70:925-936.
43. *. J. Biol. Chem. 2011, 286:5736-5743.
44. Yao L., Fang F., Wu Q., Zhong Y., Yu L. No association between CYP1B1 Val432Leu polymorphism and breast cancer risk: a meta-analysis involving 40,303 subjects. Breast Cancer Res. Treat. 2010, 122:237-242.
45. Zan B., Wang T., Wu J., Ma Y., Cheng N. Simultaneous quantification of multiple active components from Xiexin decoction in rat plasma by LC-ESI-MS/MS: application in pharmacokinetics. Biomed. Chromatogr. 2011, 25:816-826.
46. Zeng X., Zeng X. Relationship between the clinical effects of berberine on severe congestive heart failure and its concentration in plasma studied by HPLC. Biomed. Chromatogr. 1999, 13:442-444.
47. Zhao Y., Hellum B.H., Liang A., Nilsen O.G. The in vitro inhibition of human CYP1A2, CYP2D6 and CYP3A4 by tetrahydropalmatine, neferine and berberine. Phytother. Res. 2012, 26:277-283.