OATP1A/1B Transporters Affect Irinotecan and SN-38 pharmacokinetics and carboxylesterase expression in knockout and humanized transgenic mice

Molecular Cancer Therapeutics

Volumn 13, Issue 2, 2014, Pages 492-503

  Iusuf, Dilek ^a   Ludwig, Marion ^a   Elbatsh, Ahmed ^a   Van Esch, Anita ^a   Van De Steeg, Evita ^a   Wagenaar, Els ^a   Van Der Valk, Martin ^b   Lin, Fan ^a   Van Tellingen, Olaf ^a   Schinkel, Alfred H ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b Departments of Animal Pathology   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CAMPTOTHECIN; CARBOXYLESTERASE; CARBOXYLESTERASE 1, MOUSE; IRINOTECAN; OATP1A1 PROTEIN, MOUSE; ORGANIC ANION TRANSPORTER; ORGANIC CATION TRANSPORTER; PRODRUG; SLCO1B2 PROTEIN, MOUSE;

ANALOGS AND DERIVATIVES; ANIMAL; APOPTOSIS; AREA UNDER THE CURVE; BLOOD; DRUG EFFECTS; FEMALE; GENE EXPRESSION; GENETICS; HUMAN; KNOCKOUT MOUSE; LIVER; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMALL INTESTINE; THYMUS; TRANSGENIC MOUSE; UPREGULATION;

ANIMALS; APOPTOSIS; AREA UNDER CURVE; CAMPTOTHECIN; CARBOXYLIC ESTER HYDROLASES; FEMALE; GENE EXPRESSION; HUMANS; INTESTINE, SMALL; LIVER; MICE, KNOCKOUT; MICE, TRANSGENIC; ORGANIC ANION TRANSPORTERS, SODIUM-INDEPENDENT; ORGANIC CATION TRANSPORT PROTEINS; PRODRUGS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THYMUS GLAND; UP-REGULATION;

EID: 84894124093     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-13-0541     Document Type: Article

References (49)

1. Hagenbuch B, Meier PJ. Organic anion transporting polypeptides of the OATP/SLC21 family: phylogenetic classification as OATP/SLCO superfamily, new nomenclature and molecular/functional properties. Pflugers Arch 2004;447:653-65.
2. Kalliokoski A, Niemi M. Impact of OATP transporters on pharmacokinetics. Br J Pharmacol 2009;158:693-705.
3. Iusuf D, van de Steeg E, Schinkel AH. Functions of OATP1A and 1B transporters in vivo: insights from mouse models. Trends Pharmacol Sci 2012;33:100-8.
4. van de Steeg E, van Esch A, Wagenaar E, Kenworthy KE, Schinkel AH. Influence of human OATP1B1, OATP1B3, and OATP1A2 on the pharmacokinetics of methotrexate and paclitaxel in humanized transgenic mice. Clin Cancer Res 2013;19:821-32.
5. Mathijssen RH, Loos WJ, Verweij J, Sparreboom A. Pharmacology of topoisomerase I inhibitors irinotecan (CPT-11) and topotecan. Curr Cancer Drug Targets 2002;2:103-23.
6. Innocenti F, Kroetz DL, Schuetz E, Dolan ME, Ramirez J, Relling M, et al. Comprehensive pharmacogenetic analysis of irinotecan neutropenia and pharmacokinetics. J Clin Oncol 2009;27:2604-14.
7. Nozawa T, Minami H, Sugiura S, Tsuji A, Tamai I. Role of organic anion transporter OATP1B1 (OATP-C) in hepatic uptake of irinotecan and its active metabolite, 7-ethyl-10-hydroxycamptothecin: in vitro evidence and effect of single nucleotide polymorphisms. Drug Metab Dispos 2005;33:434-9.
8. Oostendorp RL, van de Steeg E, van der Kruijssen CM, Beijnen JH, Kenworthy KE, Schinkel AH, et al. Organic anion-transporting polypeptide 1B1 mediates transport of Gimatecan and BNP1350 and can be inhibited by several classic ATP-binding cassette (ABC) B1 and/or ABCG2 inhibitors. Drug Metab Dispos 2009;37:917-23.
9. Yamaguchi H, Kobayashi M, Okada M, Takeuchi T, Unno M, Abe T, et al. Rapid screening of antineoplastic candidates for the human organic anion transporter OATP1B3 substrates using fluorescent probes. Cancer Lett 2008;260:163-9.
10. Mathijssen RH, van Alphen RJ, Verweij J, Loos WJ, Nooter K, Stoter G, et al. Clinical pharmacokinetics and metabolism of irinotecan (CPT- 11). Clin Cancer Res 2001;7:2182-94.
11. Smith NF, Figg WD, Sparreboom A. Pharmacogenetics of irinotecan metabolism and transport: an update. Toxicol In Vitro 2006;20:163-75.
12. Hu ZY, Yu Q, Zhao YS. Dose-dependent association between UGT1A1-28 polymorphism and irinotecan-induced diarrhoea: a meta-analysis. Eur J Cancer 2010;46:1856-65.
13. Han JY, Lim HS, Shin ES, Yoo YK, Park YH, Lee JE, et al. Influence of the organic anion-transporting polypeptide 1B1 (OATP1B1) polymorphisms on irinotecan-pharmacokinetics and clinical outcome of patients with advanced non-small cell lung cancer. Lung Cancer 2008;59:69-75.
14. Takane H, Miyata M, Burioka N, Kurai J, Fukuoka Y, Suyama H, et al. Severe toxicities after irinotecan-based chemotherapy in a patient with lung cancer: a homozygote for the SLCO1B1-15 allele. Ther Drug Monit 2007;29:666-8.
15. Xiang X, Jada SR, Li HH, Fan L, Tham LS, Wong CI, et al. Pharmacogenetics of SLCO1B1 gene and the impact of-1b and-15 haplotypes on irinotecan disposition in Asian cancer patients. Pharmacogenet Genomics 2006;16:683-91.
16. Takane H, Kawamoto K, Sasaki T, Moriki K, Moriki K, Kitano H, et al. Life-threatening toxicities in a patient with UGT1A1-6/-28 and SLCO1B1-15/-15 genotypes after irinotecan-based chemotherapy. Cancer Chemother Pharmacol 2009;63:1165-9.
17. Pasanen MK, Neuvonen PJ, Niemi M. Global analysis of genetic variation in SLCO1B1. Pharmacogenomics 2008;9:19-33.
18. van de Steeg E, Stranecky V, Hartmannova H, Noskova L, Hrebicek M, Wagenaar E, et al. Complete OATP1B1 and OATP1B3 deficiency causes human Rotor syndrome by interrupting conjugated bilirubin reuptake into the liver. J Clin Invest 2012;122: 519-28.
19. Iusuf D, van de Steeg E, Schinkel AH. Hepatocyte hopping of OATP1B substrates contributes to efficient hepatic detoxification. Clin Pharmacol Ther 2012;92:559-62.
20. Morton CL, Wierdl M, Oliver L, Ma MK, Danks MK, Stewart CF, et al. Activation of CPT-11 in mice: identification and analysis of a highly effective plasma esterase. Cancer Res 2000;60:4206-10.
21. Schoemaker NE, Rosing H, Jansen S, Schellens JH, Beijnen JH. Highperformance liquid chromatographic analysis of the anticancer drug irinotecan (CPT-11) and its active metabolite SN-38 in human plasma. Ther Drug Monit 2003;25:120-4.
22. van Waterschoot RA, Lagas JS, Wagenaar E, van der Kruijssen CM, van Herwaarden AE, Song JY, et al. Absence of both cytochrome P450 3A and P-glycoprotein dramatically increases docetaxel oral bioavailability and risk of intestinal toxicity. Cancer Res 2009;69: 8996-9002.
23. Guemei AA, Cottrell J, Band R, Hehman H, Prudhomme M, Pavlov MV, et al. Human plasma carboxylesterase and butyrylcholinesterase enzyme activity: correlations with SN-38 pharmacokinetics during a prolonged infusion of irinotecan. Cancer Chemother Pharmacol 2001; 47:283-90.
24. Heymann E, Krisch K. [Phosphoric acid-bis-(p-nitro-phenylester), a new inhibitor of microsomal carboxylesterases] Phosphorsaure-bis- (p-nitro-phenylester), ein neuer Hemmstoff mikrosomaler Carboxylesterasen. Hoppe Seylers Z Physiol Chem 1967;348:609-19.
25. Fukami T, Takahashi S, Nakagawa N, Maruichi T, Nakajima M, Yokoi T. In vitro evaluation of inhibitory effects of antidiabetic and antihyperlipidemic drugs on human carboxylesterase activities. Drug Metab Dispos 2010;38:2173-8.
26. van Waterschoot RA, van Herwaarden AE, Lagas JS, Sparidans RW, Wagenaar E, van der Kruijssen CM, et al. Midazolam metabolism in cytochrome P450 3A knockout mice can be attributed to up-regulated CYP2C enzymes. Mol Pharmacol 2008;73: 1029-36.
27. Iusuf D, Sparidans RW, van Esch A, Hobbs M, Kenworthy KE, van de Steeg E, et al. Organic anion-transporting polypeptides 1a/1b control the hepatic uptake of pravastatin in mice. Mol Pharm 2012; 9:2497-504.
28. Innocenti F, Vokes EE, Ratain MJ. Irinogenetics: what is the right star? J Clin Oncol 2006;24:2221-4.
29. Holmes RS, Wright MW, Laulederkind SJ, Cox LA, Hosokawa M, Imai T, et al. Recommended nomenclature for five mammalian carboxylesterase gene families: human, mouse, and rat genes and proteins. Mamm Genome 2010;21:427-41.
30. Li B, Sedlacek M, Manoharan I, Boopathy R, Duysen EG, Masson P, et al. Butyrylcholinesterase, paraoxonase, and albumin esterase, but not carboxylesterase, are present in human plasma. Biochem Pharmacol 2005;70:1673-84.
31. Bahar FG, Ohura K, Ogihara T, Imai T. Species difference of esterase expression and hydrolase activity in plasma. J Pharm Sci 2012;101: 3979-88.
32. Shingyoji M, Takiguchi Y, Watanabe-Uruma R, Asaka-Amano Y, Matsubara H, Kurosu K, et al. In vitro conversion of irinotecan to SN-38 in human plasma. Cancer Sci 2004;95:537-40.
33. Humerickhouse R, Lohrbach K, Li L, Bosron WF, Dolan ME. Characterization of CPT-11 hydrolysis by human liver carboxylesterase isoforms hCE-1 and hCE-2. Cancer Res 2000;60:1189-92.
34. Zhang Y, Cheng X, Aleksunes L, Klaassen CD. Transcription factormediated regulation of carboxylesterase enzymes in livers of mice. Drug Metab Dispos 2012;40:1191-7.
35. Morton CL, Wadkins RM, Danks MK, Potter PM. The anticancer prodrug CPT-11 is a potent inhibitor of acetylcholinesterase but is rapidly catalyzed to SN-38 by butyrylcholinesterase. Cancer Res 1999;59:1458-63.
36. Iusuf D, van Esch A, Hobbs MJ, Taylor MA, Kenworthy KE, van de Steeg E, et al. Murine Oatp1a/1b uptake transporters control rosuvastatin systemic exposure without affecting its apparent liver exposure. Mol Pharmacol 2013;83:919-29.
37. Watanabe T, Kusuhara H, Maeda K, Shitara Y, Sugiyama Y. Physiologically based pharmacokinetic modeling to predict transportermediated clearance and distribution of pravastatin in humans. J Pharmacol Exp Ther 2009;328:652-62.
38. Hosokawa M, Furihata T, YaginumaY, Yamamoto N, Koyano N, Fujii A, et al. Genomic structure and transcriptional regulation of the rat, mouse, and human carboxylesterase genes. Drug Metab Rev 2007;39: 1-15.
39. Morton CL, Iacono L, Hyatt JL, Taylor KR, Cheshire PJ, Houghton PJ, et al. Activation and antitumor activity of CPT-11 in plasma esterasedeficient mice. Cancer Chemother Pharmacol 2005;56:629-36.
40. Satoh T, Hosokawa M. Structure, function and regulation of carboxylesterases. Chem Biol Interact 2006;162:195-211.
41. Lagas JS, Damen CW, van Waterschoot RA, Iusuf D, Beijnen JH, Schinkel AH. P-glycoprotein, multidrug-resistance associated protein 2, cyp3a, and carboxylesterase affect the oral availability and metabolism of vinorelbine. Mol Pharmacol 2012;82:636-44.
42. Sanghani SP, Sanghani PC, Schiel MA, Bosron WF. Human carboxylesterases: an update on CES1, CES2 and CES3. Protein Pept Lett 2009;16:1207-14.
43. Bellott R, Le Morvan V, Charasson V, Laurand A, Colotte M, Zanger UM, et al. Functional study of the 830C>Gpolymorphism of the human carboxylesterase 2 gene. Cancer Chemother Pharmacol 2008;61: 481-8.
44. Charasson V, Bellott R, Meynard D, Longy M, Gorry P, Robert J. Pharmacogenetics of human carboxylesterase 2, an enzyme involved in the activation of irinotecan into SN-38. Clin Pharmacol Ther 2004;76:528-35.
45. Kim SR, Nakamura T, Saito Y, Sai K, Nakajima T, Saito H, et al. Twelve novel single nucleotide polymorphisms in the CES2 gene encoding human carboxylesterase 2 (hCE-2). Drug Metab Pharmacokinet 2003;18:327-32.
46. Kim SR, Sai K, Tanaka-Kagawa T, Jinno H, Ozawa S, Kaniwa N, et al. Haplotypes and a novel defective allele of CES2 found in a Japanese population. Drug Metab Dispos 2007;35:1865-72.
47. Kubo T, Kim SR, Sai K, Saito Y, Nakajima T, Matsumoto K, et al. Functional characterization of three naturally occurring single nucleotide polymorphisms in the CES2 gene encoding carboxylesterase 2 (HCE-2). Drug Metab Dispos 2005;33:1482-7.
48. Sai K, Saito Y, Tatewaki N, Hosokawa M, Kaniwa N, Nishimaki- Mogami T, et al. Association of carboxylesterase 1A genotypes with irinotecan pharmacokinetics in Japanese cancer patients. Br J Clin Pharmacol 2010;70:222-33.
49. Wu MH, Yan B, Humerickhouse R, Dolan ME. Irinotecan activation by human carboxylesterases in colorectal adenocarcinoma cells. Clin Cancer Res 2002;8:2696-700.