Pregnane × Receptor (PXR) expression in colorectal cancer cells restricts irinotecan chemosensitivity through enhanced SN-38 glucuronidation

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Raynal, Caroline ^a,b   Pascussi, Jean Marc ^a   Leguelinel, Géraldine ^a   Breuker, Cyril ^a   Kantar, Jovana ^c   Lallemant, Benjamin ^a,b   Poujol, Sylvain ^d   Bonnans, Caroline ^a   Joubert, Dominique ^a   Hollande, Frédéric ^a   Lumbroso, Serge ^a,b   Brouillet, Jean Paul ^a,b   Evrard, Alexandre ^a,b  

^a INSERM   (France)

^b NÎMES UNIVERSITY HOSPITAL   (France)

^c Faculté de Médecine   (France)

^d CENTRE VAL D AURELLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

7 ETHYL 10 HYDROXYCAMPTOTHECIN; FLUOROURACIL; GLUCURONOSYLTRANSFERASE 1A1; GLUCURONOSYLTRANSFERASE 1A10; GLUCURONOSYLTRANSFERASE 1A9; IRINOTECAN; LENTIVIRUS VECTOR; MESSENGER RNA; OXALIPLATIN; PREGNANE X RECEPTOR; SHORT HAIRPIN RNA; BILIRUBIN URIDINE DIPHOSPHOGLUCURONOSYL TRANSFERASE 1A1; BILIRUBIN URIDINE-DIPHOSPHOGLUCURONOSYL TRANSFERASE 1A1; CAMPTOTHECIN; DRUG DERIVATIVE; GLUCURONOSYLTRANSFERASE; RIFAMPICIN; SMALL INTERFERING RNA; SN38 GLU; SN38-GLU; STEROID RECEPTOR;

ARTICLE; CANCER CELL CULTURE; CANCER RESISTANCE; CELL VIABILITY; COLORECTAL CANCER; CONTROLLED STUDY; CYTOTOXICITY; DRUG GLUCURONIDATION; DRUG METABOLISM; DRUG RESPONSE; DRUG SENSITIVITY; HUMAN; HUMAN CELL; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; PREDICTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; CELL SURVIVAL; COLORECTAL TUMOR; DRUG EFFECT; DRUG RESISTANCE; DRUG SCREENING; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

LENTIVIRUS;

CAMPTOTHECIN; CELL LINE, TUMOR; CELL SURVIVAL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COLORECTAL NEOPLASMS; DRUG RESISTANCE, NEOPLASM; DRUG SCREENING ASSAYS, ANTITUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCURONOSYLTRANSFERASE; HUMANS; RECEPTORS, STEROID; RIFAMPIN; RNA, MESSENGER; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 77950521888     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-46     Document Type: Article

References (49)

1. Center MM, Jemal A, Ward E. International trends in colorectal cancer incidence rates. Cancer Epidemiol Biomarkers Prev 2009, 18:1688-1694. 10.1158/1055-9965.EPI-09-0090, 19505900.
2. de Gramont A, Tournigand C, Andre T, Larsen AK, Louvet C. Adjuvant therapy for stage II and III colorectal cancer. Semin Oncol 2007, 34:S37-40. 10.1053/j.seminoncol.2007.01.004, 17449351.
3. Anthony L. Irinotecan toxicity. Curr Opin Support Palliat Care 2007, 1:35-39. 10.1097/SPC.0b013e328133f2ad, 18660722.
4. Ma MK, McLeod HL. Lessons learned from the irinotecan metabolic pathway. Curr Med Chem 2003, 10:41-49. 10.2174/0929867033368619, 12570720.
5. Mathijssen RH, van Alphen RJ, Verweij J, Loos WJ, Nooter K, Stoter G, Sparreboom A. Clinical pharmacokinetics and metabolism of irinotecan (CPT-11). Clin Cancer Res 2001, 7:2182-2194.
6. Candeil L, Gourdier I, Peyron D, Vezzio N, Copois V, Bibeau F, Orsetti B, Scheffer GL, Ychou M, Khan QA, Pommier Y, Pau B, Martineau P, Del Rio M. ABCG2 overexpression in colon cancer cells resistant to SN38 and in irinotecan-treated metastases. Int J Cancer 2004, 109:848-854. 10.1002/ijc.20032, 15027118.
7. Jansen WJ, Hulscher TM, van Ark-Otte J, Giaccone G, Pinedo HM, Boven E. CPT-11 sensitivity in relation to the expression of P170-glycoprotein and multidrug resistance-associated protein. Br J Cancer 1998, 77:359-365. 2151280, 9472629.
8. Innocenti F, Ratain MJ. "Irinogenetics" and UGT1A: from genotypes to haplotypes. Clin Pharmacol Ther 2004, 75:495-500. 10.1016/j.clpt.2004.01.011, 15179404.
9. Mathijssen RH, Gurney H. Irinogenetics: how many stars are there in the sky?. J Clin Oncol 2009, 27:2578-2579. 10.1200/JCO.2008.21.2480, 19349537.
10. Yonemori K, Takeda Y, Toyota E, Kobayashi N, Kudo K. Potential interactions between irinotecan and rifampin in a patient with small-cell lung cancer. Int J Clin Oncol 2004, 9:206-209. 10.1007/s10147-004-0394-4, 15221608.
11. Mannel M. Drug interactions with St John's wort: mechanisms and clinical implications. Drug Saf 2004, 27:773-797. 10.2165/00002018-200427110-00003, 15350151.
12. Bertilsson G, Heidrich J, Svensson K, Asman M, Jendeberg L, Sydow-Backman M, Ohlsson R, Postlind H, Blomquist P, Berkenstam A. Identification of a human nuclear receptor defines a new signaling pathway for CYP3A induction. Proc Natl Acad Sci USA 1998, 95:12208-12213. 10.1073/pnas.95.21.12208, 22810, 9770465.
13. Willson TM, Kliewer SA. PXR, CAR and drug metabolism. Nat Rev Drug Discov 2002, 1:259-266. 10.1038/nrd753, 12120277.
14. Lehmann JM, McKee DD, Watson MA, Willson TM, Moore JT, Kliewer SA. The human orphan nuclear receptor PXR is activated by compounds that regulate CYP3A4 gene expression and cause drug interactions. J Clin Invest 1998, 102:1016-1023. 10.1172/JCI3703, 508967, 9727070.
15. Geick A, Eichelbaum M, Burk O. Nuclear receptor response elements mediate induction of intestinal MDR1 by rifampin. J Biol Chem 2001, 276:14581-14587. 10.1074/jbc.M010173200, 11297522.
16. Goodwin B, Moore LB, Stoltz CM, McKee DD, Kliewer SA. Regulation of the human CYP2B6 gene by the nuclear pregnane × receptor. Mol Pharmacol 2001, 60:427-431.
17. Gardner-Stephen D, Heydel JM, Goyal A, Lu Y, Xie W, Lindblom T, Mackenzie P, Radominska-Pandya A. Human PXR variants and their differential effects on the regulation of human UDP-glucuronosyltransferase gene expression. Drug Metab Dispos 2004, 32:340-347. 10.1124/dmd.32.3.340, 2652677, 14977869.
18. Teng S, Jekerle V, Piquette-Miller M. Induction of ABCC3 (MRP3) by pregnane × receptor activators. Drug Metab Dispos 2003, 31:1296-1299. 10.1124/dmd.31.11.1296, 14570758.
19. Ma X, Idle JR, Gonzalez FJ. The pregnane × receptor: from bench to bedside. Expert Opin Drug Metab Toxicol 2008, 4:895-908. 10.1517/17425255.4.7.895, 2535920, 18624678.
20. Chen Y, Nie D. Pregnane × receptor and its potential role in drug resistance in cancer treatment. Recent Pat Anticancer Drug Discov 2009, 4:19-27. 10.2174/157489209787002498, 19149685.
21. Wang T, Ma X, Krausz KW, Idle JR, Gonzalez FJ. Role of pregnane × receptor in control of all-trans retinoic acid (ATRA) metabolism and its potential contribution to ATRA resistance. J Pharmacol Exp Ther 2008, 324:674-684. 10.1124/jpet.107.131045, 2268525, 17962516.
22. Mensah-Osman EJ, Thomas DG, Tabb MM, Larios JM, Hughes DP, Giordano TJ, Lizyness ML, Rae JM, Blumberg B, Hollenberg PF, Baker LH. Expression levels and activation of a PXR variant are directly related to drug resistance in osteosarcoma cell lines. Cancer 2007, 109:957-965. 10.1002/cncr.22479, 17279585.
23. Zhou J, Liu M, Zhai Y, Xie W. The antiapoptotic role of pregnane × receptor in human colon cancer cells. Mol Endocrinol 2008, 22:868-880. 10.1210/me.2007-0197, 2276464, 18096695.
24. Qin XF, An DS, Chen IS, Baltimore D. Inhibiting HIV-1 infection in human T cells by lentiviral-mediated delivery of small interfering RNA against CCR5. Proc Natl Acad Sci USA 2003, 100:183-188. 10.1073/pnas.232688199, 140921, 12518064.
25. Moreau A, Teruel C, Beylot M, Albalea V, Tamasi V, Umbdenstock T, Parmentier Y, Sa-Cunha A, Suc B, Fabre JM, Navarro F, Ramos J, Meyer U, Maurel P, Vilarem MJ, Pascussi JM. A novel pregnane × receptor and S14-mediated lipogenic pathway in human hepatocyte. Hepatology 2009,
26. Evrard A, Cuq P, Ciccolini J, Vian L, Cano JP. Increased cytotoxicity and bystander effect of 5-fluorouracil and 5-deoxy-5-fluorouridine in human colorectal cancer cells transfected with thymidine phosphorylase. Br J Cancer 1999, 80:1726-1733. 10.1038/sj.bjc.6690589, 2363120, 10468288.
27. Poujol S, Pinguet F, Malosse F, Astre C, Ychou M, Culine S, Bressolle F. Sensitive HPLC-fluorescence method for irinotecan and four major metabolites in human plasma and saliva: application to pharmacokinetic studies. Clin Chem 2003, 49:1900-1908. 10.1373/clinchem.2003.023481, 14578322.
28. Pascussi JM, Jounaidi Y, Drocourt L, Domergue J, Balabaud C, Maurel P, Vilarem MJ. Evidence for the presence of a functional pregnane × receptor response element in the CYP3A7 promoter gene. Biochem Biophys Res Commun 1999, 260:377-381. 10.1006/bbrc.1999.0745, 10403778.
29. Jansen WJ, Zwart B, Hulscher ST, Giaccone G, Pinedo HM, Boven E. CPT-11 in human colon-cancer cell lines and xenografts: characterization of cellular sensitivity determinants. Int J Cancer 1997, 70:335-340. 10.1002/(SICI)1097-0215(19970127)70:3<335::AID-IJC15>3.0.CO;2-E, 9033637.
30. Arita D, Kambe M, Ishioka C, Kanamaru R. Induction ofp53-independent apoptosis associated with G2M arrest following DNA damage in human colon cancer cell lines. Jpn J Cancer Res 1997, 88:39-43.
31. McDonald AC, Brown R. Induction of p53-dependent andp53-independent cellular responses by topoisomerase 1 inhibitors. Br J Cancer 1998, 78:745-751. 2062955, 9743293.
32. Pascussi JM, Drocourt L, Gerbal-Chaloin S, Fabre JM, Maurel P, Vilarem MJ. Dual effect of dexamethasone on CYP3A4 gene expression in human hepatocytes. Sequential role of glucocorticoid receptor and pregnane × receptor. Eur J Biochem 2001, 268:6346-6358. 10.1046/j.0014-2956.2001.02540.x, 11737189.
33. Zhou C, Poulton EJ, Grun F, Bammler TK, Blumberg B, Thummel KE, Eaton DL. The dietary isothiocyanate sulforaphane is an antagonist of the human steroid and xenobiotic nuclear receptor. Mol Pharmacol 2007, 71:220-229. 10.1124/mol.106.029264, 17028159.
34. Morimitsu Y, Nakagawa Y, Hayashi K, Fujii H, Kumagai T, Nakamura Y, Osawa T, Horio F, Itoh K, Iida K, Yamamoto M, Uchida K. A sulforaphane analogue that potently activates the Nrf2-dependent detoxification pathway. J Biol Chem 2002, 277:3456-3463. 10.1074/jbc.M110244200, 11706044.
35. Xu C, Shen G, Chen C, Gelinas C, Kong AN. Suppression of NF-kappaB and NF-kappaB-regulated gene expression by sulforaphane and PEITC through IkappaBalpha, IKK pathway in human prostate cancer PC-3 cells. Oncogene 2005, 24:4486-4495. 10.1038/sj.onc.1208656, 15856023.
36. Masuyama H, Nakatsukasa H, Takamoto N, Hiramatsu Y. Down-regulation of pregnane × receptor contributes to cell growth inhibition and apoptosis by anticancer agents in endometrial cancer cells. Mol Pharmacol 2007, 72:1045-1053. 10.1124/mol.107.037937, 17636047.
37. Gupta E, Wang X, Ramirez J, Ratain MJ. Modulation of glucuronidation of SN-38, the active metabolite of irinotecan, by valproic acid and phenobarbital. Cancer Chemother Pharmacol 1997, 39:440-444. 10.1007/s002800050595, 9054958.
38. Crews KR, Stewart CF, Jones-Wallace D, Thompson SJ, Houghton PJ, Heideman RL, Fouladi M, Bowers DC, Chintagumpala MM, Gajjar A. Altered irinotecan pharmacokinetics in pediatric high-grade glioma patients receiving enzyme-inducing anticonvulsant therapy. Clin CancerRes 2002, 8:2202-2209.
39. de Jong FA, Bol JM, Mathijssen RH, Loos WJ, Mathot RA, Kitzen JJ, Bent MJ, Verweij J. Irinotecan chemotherapy during valproic acid treatment: pharmacokinetic interaction and hepatotoxicity. Cancer Biol Ther 2007, 6:1368-1374. 10.1158/1535-7163.MCT-05-0414, 17873515.
40. Cummings J, Boyd G, Ethell BT, Macpherson JS, Burchell B, Smyth JF, Jodrell DI. Enhanced clearance of topoisomerase I inhibitors from human colon cancer cells by glucuronidation. Biochem Pharmacol 2002, 63:607-613. 10.1016/S0006-2952(01)00812-7, 11992628.
41. Cummings J, Ethell BT, Jardine L, Boyd G, Macpherson JS, Burchell B, Smyth JF, Jodrell DI. Glucuronidation as a mechanism of intrinsic drug resistance in human colon cancer: reversal of resistance by food additives. Cancer Res 2003, 63:8443-8450.
42. Gupta E, Lestingi TM, Mick R, Ramirez J, Vokes EE, Ratain MJ. Metabolic fate of irinotecan in humans: correlation of glucuronidation with diarrhea. Cancer Res 1994, 54:3723-3725.
43. Mathijssen RH, Gurney H. Irinogenetics: How Many Stars Are There in the Sky?. J Clin Oncol 2009,
44. Bosch TM, Deenen M, Pruntel R, Smits PH, Schellens JH, Beijnen JH, Meijerman I. Screening for polymorphisms in the PXR gene in a Dutch population. Eur J Clin Pharmacol 2006, 62:395-399. 10.1007/s00228-006-0108-0, 16568343.
45. King CR, Xiao M, Yu J, Minton MR, Addleman NJ, Van Booven DJ, Kwok PY, McLeod HL, Marsh S. Identification of NR1I2 genetic variation using resequencing. Eur J Clin Pharmacol 2007, 63:547-554. 10.1007/s00228-007-0295-3, 17404718.
46. Moreau A, Vilarem MJ, Maurel P, Pascussi JM. Xenoreceptors CAR and PXR activation and consequences on lipid metabolism, glucose homeostasis, and inflammatory response. Mol Pharm 2008, 5:35-41. 10.1021/mp700103m, 18159929.
47. Takagi S, Nakajima M, Mohri T, Yokoi T. Post-transcriptional regulation of human pregnane × receptor by micro-RNA affects the expression of cytochrome P450 3A4. J Biol Chem 2008, 283:9674-9680. 10.1074/jbc.M709382200, 18268015.
48. Misawa A, Inoue J, Sugino Y, Hosoi H, Sugimoto T, Hosoda F, Ohki M, Imoto I, Inazawa J. Methylation-associated silencing of the nuclear receptor 1I2 gene in advanced-type neuroblastomas, identified by bacterial artificial chromosome array-based methylated CpG island amplification. Cancer Res 2005, 65:10233-10242. 10.1158/0008-5472.CAN-05-1073, 16288011.
49. Flexner C. Pharmacoecology: a new name for an old science. Clin Pharmacol Ther 2008, 83:375-379. 10.1038/sj.clpt.6100499, 18285779.