Characterization of human cytochrome P450 induction by pesticides

Toxicology

Volumn 294, Issue 1, 2012, Pages 17-26

  Abass, Khaled ^a,c   Lämsä, Virpi ^a   Reponen, Petri ^a   Küblbeck, Jenni ^b   Honkakoski, Paavo ^b   Mattila, Sampo ^a   Pelkonen, Olavi ^a   Hakkola, Jukka ^a  

^a UNIVERSITY OF OULU   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c MENOUFIA UNIVERSITY   (Egypt)

Author keywords

C3A, HepG2 and HepaRG cell lines; Human cytochrome P450; LC MS MS; Mouse primary hepatocytes; PXR and CAR; RT qPCR; Xenobiotic

Indexed keywords

CARBAMIC ACID; CARBAMIC ACID DERIVATIVE; CARBARIL; CARBENDAZIM; CARBOFURAN; CARBOSULFAN; CHLORPYRIFOS; CIPERMETHRIN; CONSTITUTIVE ANDROSTANE RECEPTOR; CYHALOTHRIN; CYTOCHROME P450; CYTOCHROME P450 2B6; DELTAMETHRIN; DIURON; FENITROTHION; FENVALERATE; ISOPROTURON; LUCIFERASE; MALATHION; MESSENGER RNA; METALAXYL; ORGANOPHOSPHATE PESTICIDE; PESTICIDE; PHENTHOATE; PREGNANE X RECEPTOR; PROFENOFOS; PYRETHROID; TEBUFENOZIDE; TRIAZINE; UNINDEXED DRUG;

ARTICLE; CELL LINE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION;

ANIMALS; CARBAMATES; CELL LINE; CYTOCHROME P-450 ENZYME SYSTEM; ENZYME INDUCTION; HEPATOCYTES; HUMANS; L-LACTATE DEHYDROGENASE; MALE; MICE; MICE, INBRED DBA; PESTICIDES; PYRETHRINS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, STEROID;

EID: 84857796387     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2012.01.010     Document Type: Article

References (67)

1. Abass K., Turpeinen M., Rautio A., Hakkola J., Pelkonen O. Metabolism of pesticides by human cytochrome P450 enzymes in vitro - a survey. Insecticides - Advances in Integrated Pest Managemen 2012, InTech, Austria. F. Perveen (Ed.).
2. Abass K., Reponen P., Jalonen J., Pelkonen O. In vitro metabolism and interaction of profenofos by human, mouse and rat liver preparations. Pestic. Biochem. Physiol. 2007, 87:238-247.
3. Abass K., Reponen P., Jalonen J., Pelkonen O. In vitro metabolism and interactions of the fungicide metalaxyl in human liver preparations. Environ. Toxicol. Pharmacol. 2007, 23:39-47.
4. Abass K., Reponen P., Mattila S., Pelkonen O. Metabolism of carbosulfan. II. Human interindividual variability in its in vitro hepatic biotransformation and the identification of the cytochrome P450 isoforms involved. Chem. Biol. Interact. 2010, 185:163-173.
5. Abass K., Reponen P., Mattila S., Pelkonen O. Metabolism of carbosulfan. I. Species differences in the in vitro biotransformation by mammalian hepatic microsomes including human. Chem. Biol. Interact. 2009, 181:210-219.
6. Abass K., Turpeinen M., Pelkonen O. An evaluation of the cytochrome P450 inhibition potential of selected pesticides in human hepatic microsomes. J. Environ. Sci. Health Part B: Pestic. Food Contam. Agric. Wastes 2009, 44:553.
7. Adgate J.L., Barr D.B., Clayton C.A., Eberly L.E., Freeman N.C.G., Lioy P.J., Needham L.L., Pellizzari E.D., Quackenboss J.J., Roy A., Sexton K. Measurement of children's exposure to pesticides: analysis of urinary metabolite levels in a probability-based sample. Environ. Health Perspect. 2001, 109:583-589.
8. Anderson L.E., Dring A.M., Hamel L.D., Stoner M.A. Modulation of constitutive androstane receptor (CAR) and pregnane X receptor (PXR) by 6-arylpyrrolo[2,1-d][1,5]benzothiazepine derivatives, ligands of peripheral benzodiazepine receptor (PBR). Toxicol. Lett. 2011, 202:148-154.
9. Aninat C., Piton A., Glaise D., Le Charpentier T., Langouet S., Morel F., Guguen-Guillouzo C., Guillouzo A. Expression of cytochromes P450, conjugating enzymes and nuclear receptors in human hepatoma HepaRG cells. Drug Metab. Dispos. 2006, 34:75-83.
10. Anthérieu S., Chesné C., Li R., Camus S., Lahoz A., Picazo L., Turpeinen M., Tolonen A., Uusitalo J., Guguen-Guillouzo C., Guillouzo A. Stable expression, activity, and inducibility of cytochromes P450 in differentiated HepaRG cells. Drug Metab. Dispos. 2010, 38:516-525.
11. Aprea C., Terenzoni B., De Angelis V., Sciarra G., Lunghini L., Borzacchi G., Vasconi D., Fani D., Quercia A., Salvan A., Settimi L. Evaluation of skin and respiratory doses and urinary excretion of alkylphosphates in workers exposed to dimethoate during treatment of olive trees. Arch. Environ. Contam. Toxicol. 2004, 48:127-134.
12. Arpiainen S., Järvenpää S., Manninen A., Viitala P., Lang M.A., Pelkonen O., Hakkola J. Coactivator PGC-1α regulates the fasting inducible xenobiotic-metabolizing enzyme CYP2A5 in mouse primary hepatocytes. Toxicol. Appl. Pharmacol. 2008, 232:135-141.
13. Baldwin W.S., Roling J.A. A concentration addition model for the activation of the constitutive androstane receptor by xenobiotic mixtures. Toxicol. Sci. 2009, 107:93-105.
14. Buratti F.M., D'Aniello A., Volpe M.T., Meneguz A., Testai E. Malathion bioactivation in the human liver liver: the contribution of different cytochrome P450 isoform. Drug Metab. Dispos. 2005, 33:295-302.
15. Buratti F.M., Testai E. Evidences for CYP3A4 autoactivation in the desulfuration of dimethoate by the human liver. Toxicology 2007, 241:33-46.
16. Buratti F.M., Volpe M.T., Fabrizi L., Meneguz A., Vittozzi L., Testai E. Kinetic parameters of OPT pesticide desulfuration by c-DNA expressed human CYPs. Environ. Toxicol. Pharmacol. 2002, 11:181-190.
17. Buratti F.M., Volpe M.T., Meneguz A., Vittozzi L., Testai E. CYP-specific bioactivation of four organophosphorothioate pesticides by human liver microsomes. Toxicol. Appl. Pharmacol. 2003, 186:143-154.
18. Butler A.M., Murray M. Biotransformation of parathion in human liver: participation of CYP3A4 and its inactivation during microsomal parathion oxidation. J. Pharmacol. Exp. Ther. 1997, 280:966-973.
19. Casabar R.C.T., Das P.C., DeKrey G.K., Gardiner C.S., Cao Y., Rose R.L., Wallace A.D. Endosulfan induces CYP2B6 and CYP3A4 by activating the pregnane X receptor. Toxicol. Appl. Pharmacol. 2010, 245:335-343.
20. Coumoul X., Diry M., Barouki R. PXR-dependent induction of human CYP3A4 gene expression by organochlorine pesticides. Biochem. Pharmacol. 2002, 64:1513-1519.
21. Croom E.L., Wallace A.D., Hodgson E. Human variation in CYP-specific chlorpyrifos metabolism. Toxicology 2010, 276:184-191.
22. Das P.C., Cao Y., Rose R.L., Cherrington N., Hodgson E. Enzyme induction and cytotoxicity in human hepatocytes by chlorpyrifos and N,N-diethyl-m-toluamide (DEET). Drug Metabol. Drug Interact. 2008, 23:237-260.
23. Das P.C., Streit T.M., Cao Y., Rose R.L., Cherrington N., Ross M.K., Wallace A.D., Hodgson E. Pyrethroids: cytotoxicity and induction of CYP isoforms in human hepatocytes. Drug Metabol. Drug Interact. 2008, 23:211.
24. Das P.C., Cao Y., Cherrington N., Hodgson E., Rose R.L. Fipronil induces CYP isoforms and cytotoxicity in human hepatocytes. Chem. Biol. Interact. 2006, 164:200-214.
25. Dayal M., Parmar D., Dhawan A., Ali M., Dwivedi U.N., Seth P.K. Effect of pretreatment of cytochrome P450 (P450) modifiers on neurobehavioral toxicity induced by deltamethrin. Food Chem. Toxicol. 2003, 41:431-437.
26. de Sousa G., Fontaine F., Pralavorio M., Botta-Fridlund D., Letreut Y., Rahmani R. Insecticide cytotoxicity and CYP1A1/2 induction in primary human and rat hepatocyte cultures. Toxicol. In Vitro 1997, 11:451-453.
27. Foxenberg R.J., McGarrigle B.P., Knaak J.B., Kostyniak P.J., Olson J.R. Human hepatic cytochrome P450-specific metabolism of parathion and chlorpyrifos. Drug Metab. Dispos. 2007, 35:189-193.
28. Gilden R.C., Huffling K., Sattler B. Pesticides and health risks. JOGNN 2010, 39:103-110.
29. Hodgson E., Rose R.L. Human metabolic interactions of environmental chemicals. J. Biochem. Mol. Toxicol. 2007, 21:182-186.
30. Honkakoski P., Negishi M. Regulation of cytochrome P450 (CYP) genes by nuclear receptors. Biochem. J. 2000, 347(Pt 2):321-337.
31. Jyrkkärinne J., Windshügel B., Mäkinen J., Ylisirniö M., Peräkylä M., Poso A., Sippl W., Honkakoski P. Amino acids important for ligand specificity of the human constitutive androstane receptor. J. Biol. Chem. 2005, 280:5960-5971.
32. Kanebratt K.P., Andersson T.B. Evaluation of HepaRG cells as an in vitro model for human drug metabolism studies. Drug Metab. Dispos. 2008, 36:1444-1452.
33. Kojima H., Sata F., Takeuchi S., Sueyoshi T., Nagai T. Comparative study of human and mouse pregnane X receptor agonistic activity in 200 pesticides using in vitro reporter gene assays. Toxicology 2011, 280:77-87.
34. Kretschmer X.C., Baldwin W.S. CAR and PXR: xenosensors of endocrine disrupters. Chem. Biol. Interact. 2005, 155:111-128.
35. Krieger R.I., Dinoff T.M. Malathion deposition, metabolite clearance, and cholinesterase status of date dusters and harvesters in California. Arch. Environ. Contam. Toxicol. 2000, 38:546-553.
36. Küblbeck J., Laitinen T., Jyrkkärinne J., Rousu T., Tolonen A., Abel T., Kortelainen T., Uusitalo J., Korjamo T., Honkakoski P., Molnár F. Use of comprehensive screening methods to detect selective human CAR activators. Biochem. Pharmacol. 2011, 82:1994-2007.
37. Lämsä V., Levonen A., Leinonen H., Ylaì̂-Herttuala S., Yamamoto M., Hakkola J. Cytochrome P450 2A5 constitutive expression and induction by heavy metals is dependent on redox-sensitive transcription factor Nrf2 in liver. Chem. Res. Toxicol. 2010, 23:977-985.
38. Lemaire G., de Sousa G., Rahmani R. A PXR reporter gene assay in a stable cell culture system: CYP3A4 and CYP2B6 induction by pesticides. Biochem. Pharmacol. 2004, 68:2347-2358.
39. Leoni C., Buratti F.M., Testai E. The participation of human hepatic P450 isoforms, flavin-containing monooxygenases and aldehyde oxidase in the biotransformation of the insecticide fenthion. Toxicol. Appl. Pharmacol. 2008, 233:343-352.
40. Lin J. CYP induction-mediated drug interactions: in vitro assessment and clinical implications. Pharm. Res. 2006, 23:1089-1116.
41. Long M., Laier P., Vinggaard A.M., Andersen H.R., Lynggaard J., Bonefeld-Jørgensen E.C. Effects of currently used pesticides in the AhR-CALUX assay: comparison between the human TV101L and the rat H4IIE cell line. Toxicology 2003, 194:77-93.
42. Mäkinen J., Reinisalo M., Niemi K., Viitala P., Jyrkkärinne J., Chung H., Pelkonen O., Honkakoski P. Dual action of oestrogens on the mouse constitutive androstane receptor. Biochem. J. 2003, 376:465-472.
43. Murray M., Cui P., Zhou F. Roles of mitogen-activated protein kinases in the regulation of CYP genes. Curr. Drug Metab. 2010, 11:850-858.
44. Mutch E., Daly A.K., Leathart J.B., Blain P.G., Williams F.M. Do multiple cytochrome P450 isoforms contribute to parathion metabolism in man?. Arch. Toxicol. 2003, 77:313-320.
45. Mutch E., Williams F.M. Diazinon, chlorpyrifos and parathion are metabolised by multiple cytochromes P450 in human liver. Toxicology 2006, 224:22-32.
46. Neal R.A. Microsomal metabolism of thiono-sulfur compounds: mechanisms and toxicological significance. Rev. Biochem. Toxicol. 1980, 2:131-171.
47. Neal R.A., Halpert J. Toxicology of thiono-sulfur compounds. Annu. Rev. Pharmacol. Toxicol. 1982, 22:321-339.
48. Nolan R.J., Rick D.L., Freshour N.L., Saunders J.H. Chlorpyrifos: pharmacokinetics in human volunteers. Toxicol. Appl. Pharmacol. 1984, 73:8-15.
49. Pelkonen O., Turpeinen M., Hakkola J., Honkakoski P., Hukkanen J., Raunio H. Inhibition and induction of human cytochrome P450 enzymes: current status. Arch. Toxicol. 2008, 82:667-715.
50. Poet T.S., Wu H., Kousba A.A., Timchalk C. In vitro rat hepatic and intestinal metabolism of the organophosphate pesticides chlorpyrifos and diazinon. Toxicol. Sci. 2003, 72:193-200.
51. Rigas M.L., Okino M.S., Quackenboss J.J. Use of a pharmacokinetic model to assess chlorpyrifos exposure and dose in children, based on urinary biomarker measurements. Toxicol. Sci. 2001, 61:374-381.
52. Rudzok S., Schmücking E., Graebsch C., Herbarth O., Bauer M. The inducibility of human cytochrome P450 1A by environmental-relevant xenobiotics in the human hepatoma derived cell line HepG2. Environ. Toxicol. Pharmacol. 2009, 28:370-378.
53. Sams C., Mason H.J., Rawbone R. Evidence for the activation of organophosphate pesticides by cytochromes P450 3A4 and 2D6 in human liver microsomes. Toxicol. Lett. 2000, 116:217-221.
54. Sinz M., Kim S., Zhu Z., Chen T., Anthony M., Dickinson K., David R. Evaluation of 170 xenobiotics as transactivators of human pregnane X receptor (hPXR) and correlation to known CYP3A4 drug interactions. Curr. Drug Metab. 2006, 7:375-388.
55. Song X., Li Y., Liu J., Mukundan M., Yan B. Simultaneous substitution of phenylalanine-305 and aspartate-318 of rat pregnane X receptor with the corresponding human residues abolishes the ability to transactivate the CYP3A23 promoter. J. Pharmacol. Exp. Ther. 2005, 312:571-582.
56. Takeuchi S., Iida M., Yabushita H., Matsuda T., Kojima H. In vitro screening for aryl hydrocarbon receptor agonistic activity in 200 pesticides using a highly sensitive reporter cell line, DR-EcoScreen cells, and in vivo mouse liver cytochrome P450-1A induction by propanil, diuron and linuron. Chemosphere 2008, 74:155-165.
57. Tang J., Cao Y., Rose R.L., Brimfield A.A., Dai D., Goldstein J.A., Hodgson E. Metabolism of chlorpyrifos by human cytochrome P450 isoforms and human, mouse, and rat liver microsomes. Drug Metab. Dispos. 2001, 29:1201-1204.
58. Tang J., Cao Y., Rose R.L., Hodgson E. In vitro metabolism of carbaryl by human cytochrome P450 and its inhibition by chlorpyrifos. Chem. Biol. Interact. 2002, 141:229-241.
59. Tolonen A., Petsalo A., Turpeinen M., Uusitalo J., Pelkonen O. In vitro interaction cocktail assay for nine major cytochrome P450 enzymes with 13 probe reactions and a single LC/MSMS run: analytical validation and testing with monoclonal anti-CYP antibodies. J. Mass Spectrom. 2007, 42:960-966.
60. Tolonen A., Turpeinen M., Uusitalo J., Pelkonen O. A simple method for differentiation of monoisotopic drug metabolites with hydrogen-deuterium exchange liquid chromatography/electrospray mass spectrometry. Eur. J. Pharm. Sci. 2005, 25:155-162.
61. Turpeinen M., Tolonen A., Chesne C., Guillouzo A., Uusitalo J., Pelkonen O. Functional expression, inhibition and induction of CYP enzymes in HepaRG cells. Toxicol. In Vitro 2009, 23:748-753.
62. Tzameli I., Pissios P., Schuetz E.G., Moore D.D. The xenobiotic compound 1,4-bis[2-(3,5-dichloropyridyloxy)]benzene is an agonist ligand for the nuclear receptor CAR. Mol. Cell. Biol. 2000, 20:2951-2958.
63. Usmani K.A., Hodgson E., Rose R.L. In vitro metabolism of carbofuran by human, mouse, and rat cytochrome P450 and interactions with chlorpyrifos, testosterone, and estradiol. Chem. Biol. Interact. 2004, 150:221-332.
64. Wei P., Zhang J., Dowhan D.H., Han Y., Moore D.D. Specific and overlapping functions of the nuclear hormone receptors CAR and PXR in xenobiotic response. Pharmacogenomics J. 2002, 2:117-126.
65. Wirdefeldt K., Adami H., Cole P., Trichopoulos D., Mandel J. Epidemiology and etiology of Parkinson's disease: a review of the evidence. Eur. J. Epidemiol. 2011, 26:1-58.
66. Wyde M.E., Bartolucci E., Ueda A., Zhang H., Yan B., Negishi M., You L. The environmental pollutant 1,1-dichloro-2,2-bis (p-chlorophenyl)ethylene induces rat hepatic cytochrome P450 2B and 3A expression through the constitutive androstane receptor and pregnane X receptor. Mol. Pharmacol. 2003, 64:474-481.
67. Yang D., Wang X., Chen Y., Deng R., Yan B. Pyrethroid insecticides: isoform-dependent hydrolysis, induction of cytochrome P450 3A4 and evidence on the involvement of the pregnane X receptor. Toxicol. Appl. Pharmacol. 2009, 237:49-58.