Altered expression of small Heterodimer Partner Governs Cytochrome P450 (CYP) 2D6 induction during Pregnancy in CYP2D6-humanized mice

Journal of Biological Chemistry

Volumn 289, Issue 6, 2014, Pages 3105-3113

  Koh, Kwi Hye ^a   Pan, Xian ^b   Shen, Hong Wu ^c   Arnold, Samuel L M ^d   Yu, Ai Ming ^c   Gonzalez, Frank J ^e   Isoherranen, Nina ^d   Jeong, Hyunyoung ^a,b  

^a Department of Pharmacy Practice ^*  (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

^e NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME P450; DRUG METABOLISM; HNF4Α; PREGNANCY; RETINOID; SHP; TRANSGENIC MICE;

ANIMALS; ANTINEOPLASTIC AGENTS; CYTOCHROME P-450 CYP2D6; ENZYME INDUCTION; FEMALE; HEP G2 CELLS; HEPATOCYTE NUCLEAR FACTOR 4; HUMANS; LIVER; MICE; MICE, TRANSGENIC; PREGNANCY; PROMOTER REGIONS, GENETIC; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TRANSCRIPTIONAL ACTIVATION; TRETINOIN;

EID: 84893704468     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.526798     Document Type: Article

References (51)

1. Andrade, S. E., Gurwitz, J. H., Davis, R. L., Chan, K. A., Finkelstein, J. A., Fortman, K., McPhillips, H., Raebel, M. A., Roblin, D., Smith, D. H., Yood, M. U., Morse, A. N., and Platt, R. (2004) Prescription drug use in pregnancy. Am. J. Obstet. Gynecol. 191, 398-407
2. Glover, D. D., Amonkar, M., Rybeck, B. F., and Tracy, T. S. (2003) Prescription, over-the-counter, and herbal medicine use in a rural, obstetric population. Am. J. Obstet. Gynecol. 188, 1039-1045
3. Isoherranen, N., and Thummel, K. E. (2013) Drug metabolism and transport during pregnancy. How does drug disposition change during pregnancy and what are the mechanisms that cause such changes? Drug Metab. Dispos. 41, 256-262
4. Jover, R., Moya, M., and Gómez-Lechón, M. J. (2009) Transcriptional regulation of cytochrome p450 genes by the nuclear receptor hepatocyte nuclear factor 4-. Curr. Drug. Metab. 10, 508-519
5. Yu, A. M., Idle, J. R., and Gonzalez, F. J. (2004) Polymorphic cytochrome P450 2D6. Humanized mouse model and endogenous substrates. Drug Metab. Rev. 36, 243-277
6. Zanger, U. M., Raimundo, S., and Eichelbaum, M. (2004) Cytochrome P450 2D6. Overview and update on pharmacology, genetics, biochemistry. Naunyn Schmiedebergs Arch. Pharmacol. 369, 23-37
7. Yu, A. M., Idle, J. R., Byrd, L. G., Krausz, K. W., Küpfer, A., and Gonzalez, F. J. (2003) Regeneration of serotonin from 5-methoxytryptamine by polymorphic human CYP2D6. Pharmacogenetics 13, 173-181
8. Kurth, M. C., and Kurth, J. H. (1993) Variant cytochrome P450 CYP2D6 allelic frequencies in Parkinson's disease. Am. J. Med. Genet. 48, 166-168
9. Högstedt, S., Lindberg, B., Peng, D. R., Regardh, C. G., and Rane, A. (1985) Pregnancy-induced increase in metoprolol metabolism. Clin. Pharmacol. Ther. 37, 688-692
10. Wadelius, M., Darj, E., Frenne, G., and Rane, A. (1997) Induction of CYP2D6 in pregnancy. Clin. Pharmacol. Ther. 62, 400-407
11. Tracy, T. S., Venkataramanan, R., Glover, D. D., Caritis, S. N., and National Institute for Child Health and Human Development Network of Maternal-Fetal-Medicine Units (2005) Temporal changes in drug metabolism (CYP1A2, CYP2D6, and CYP3A activity) during pregnancy. Am. J. Obstet. Gynecol. 192, 633-639
12. Sit, D. K., Perel, J. M., Helsel, J. C., and Wisner, K. L. (2008) Changes in antidepressant metabolism and dosing across pregnancy and early postpartum. J. Clin. Psychiatry 69, 652-658
13. Dickmann, L. J., Tay, S., Senn, T. D., Zhang, H., Visone, A., Unadkat, J. D., Hebert, M. F., and Isoherranen, N. (2008) Changes in maternal liver Cyp2c and Cyp2d expression and activity during rat pregnancy. Biochem. Pharmacol. 75, 1677-1687
14. Koh, K. H., Xie, H., Yu, A. M., and Jeong, H. (2011) Altered cytochrome P450 expression in mice during pregnancy. Drug Metab. Dispos. 39, 165-169
15. Wilson, M. D., Barbosa-Morais, N. L., Schmidt, D., Conboy, C. M., Vanes, L., Tybulewicz, V. L., Fisher, E. M., Tavaré, S., and Odom, D. T. (2008) Species-specific transcription in mice carrying human chromosome 21. Science 322, 434-438
16. Corchero, J., Granvil, C. P., Akiyama, T. E., Hayhurst, G. P., Pimprale, S., Feigenbaum, L., Idle, J. R., and Gonzalez, F. J. (2001) The CYP2D6 humanized mouse. Effect of the human CYP2D6 transgene and HNF4-on the disposition of debrisoquine in the mouse. Mol. Pharmacol. 60, 1260-1267
17. Hayhurst, G. P., Lee, Y. H., Lambert, G., Ward, J. M., and Gonzalez, F. J. (2001) Hepatocyte nuclear factor 4-(nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis. Mol. Cell. Biol. 21, 1393-1403
18. Felmlee, M. A., Lon, H. K., Gonzalez, F. J., and Yu, A. M. (2008) Cytochrome P450 expression and regulation in CYP3A4/CYP2D6 double transgenic humanized mice. Drug Metab. Dispos. 36, 435-441
19. Fang, S., Miao, J., Xiang, L., Ponugoti, B., Treuter, E., and Kemper, J. K. (2007) Coordinated recruitment of histone methyltransferase G9a and other chromatin-modifying enzymes in SHP-mediated regulation of hepatic bile acid metabolism. Mol. Cell. Biol. 27, 1407-1424
20. Arnold, S. L., Amory, J. K., Walsh, T. J., and Isoherranen, N. (2012) A sensitive and specific method for measurement of multiple retinoids in human serum with UHPLC-MS/MS. J. Lipid Res. 53, 587-598
21. Lee, S. S., Cha, E. Y., Jung, H. J., Shon, J. H., Kim, E. Y., Yeo, C. W., and Shin, J. G. (2008) Genetic polymorphism of hepatocyte nuclear factor-4-influences human cytochrome P450 2D6 activity. Hepatology 48, 635-645
22. Cairns, W., Smith, C. A., McLaren, A. W., and Wolf, C. R. (1996) Characterization of the human cytochrome P4502D6 promoter. A potential role for antagonistic interactions between members of the nuclear receptor family. J. Biol. Chem. 271, 25269-25276
23. Sweeney, T. R., Moser, A. H., Shigenaga, J. K., Grunfeld, C., and Feingold, K. R. (2006) Decreased nuclear hormone receptor expression in the livers of mice in late pregnancy. Am. J. Physiol. Endocrinol. Metab. 290, E1313-E1320
24. Gonzalez, F. J. (2008) Regulation of hepatocyte nuclear factor 4-mediated transcription. Drug Metab. Pharmacokinet. 23, 2-7
25. Zhang, M., and Chiang, J. Y. (2001) Transcriptional regulation of the human sterol 12-hydroxylase gene (CYP8B1). Roles of heaptocyte nuclear factor 4-in mediating bile acid repression. J. Biol. Chem. 276, 41690-41699
26. Martinez-Jimenez, C. P., Kyrmizi, I., Cardot, P., Gonzalez, F. J., and Talianidis, I. (2010) Hepatocyte nuclear factor 4-coordinates a transcription factor network regulating hepatic fatty acid metabolism. Mol. Cell. Biol. 30, 565-577
27. Garrison, W. D., Battle, M. A., Yang, C., Kaestner, K. H., Sladek, F. M., and Duncan, S. A. (2006) Hepatocyte nuclear factor 4-is essential for embryonic development of the mouse colon. Gastroenterology 130, 1207-1220
28. Nikolaidou-Neokosmidou, V., Zannis, V. I., and Kardassis, D. (2006) Inhibition of hepatocyte nuclear factor 4 transcriptional activity by the nuclear factor-B pathway. Biochem. J. 398, 439-450
29. Nelson, B. R., Hartman, B. H., Ray, C. A., Hayashi, T., Bermingham-Mc-Donogh, O., and Reh, T. A. (2009) Acheate-scute like 1 (Ascl1) is required for normal delta-like (Dll) gene expression and notch signaling during retinal development. Dev. Dyn. 238, 2163-2178
30. Lee, Y. J., Han, D. H., Pak, Y. K., and Cho, S. H. (2012) Circadian regulation of low density lipoprotein receptor promoter activity by CLOCK/BMAL1, Hes1, and Hes6. Exp. Mol. Med. 44, 642-652
31. Malone, C. M., Domaschenz, R., Amagase, Y., Dunham, I., Murai, K., and Jones, P. H. (2011) Hes6 is required for actin cytoskeletal organization in differentiating C2C12 myoblasts. Exp. Cell Res. 317, 1590-1602
32. Sinal, C. J., Tohkin, M., Miyata, M., Ward, J. M., Lambert, G., and Gonzalez, F. J. (2000) Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell 102, 731-744
33. Milona, A., Owen, B. M., Cobbold, J. F., Willemsen, E. C., Cox, I. J., Boudjelal, M., Cairns, W., Schoonjans, K., Taylor-Robinson, S. D., Klomp, L. W., Parker, M. G., White, R., van Mil, S. W., and Williamson, C. (2010) Raised hepatic bile acid concentrations during pregnancy in mice are associated with reduced farnesoid X receptor function. Hepatology 52, 1341-1349
34. Goodwin, B., Watson, M. A., Kim, H., Miao, J., Kemper, J. K., and Kliewer, S. A. (2003) Differential regulation of rat and human CYP7A1 by the nuclear oxysterol receptor liver X receptor-. Mol. Endocrinol. 17, 386-394
35. Lu, T. T., Makishima, M., Repa, J. J., Schoonjans, K., Kerr, T. A., Auwerx, J., and Mangelsdorf, D. J. (2000) Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors. Mol. Cell 6, 507-515
36. Cai, S. Y., He, H., Nguyen, T., Mennone, A., and Boyer, J. L. (2010) Retinoic acid represses CYP7A1 expression in human hepatocytes and HepG2 cells by FXR/RXR-dependent and independent mechanisms. J. Lipid Res. 51, 2265-2274
37. Choi, S. Y., Koh, K. H., and Jeong, H. (2013) Isoform-specific Regulation of Cytochromes P450 Expression by Estradiol and Progesterone. Drug Metab. Dispos. 41, 263-269
38. Dickmann, L. J., and Isoherranen, N. (2013) Quantitative prediction of CYP2B6 induction by estradiol during pregnancy. Potential explanation for increased methadone clearance during pregnancy. Drug Metab. Dispos. 41, 270-274
39. Chanda, D., Park, J. H., and Choi, H. S. (2008) Molecular basis of endocrine regulation by orphan nuclear receptor small heterodimer partner. Endocr. J. 55, 253-268
40. Shimamoto, Y., Ishida, J., Yamagata, K., Saito, T., Kato, H., Matsuoka, T., Hirota, K., Daitoku, H., Nangaku, M., Yamagata, K., Fujii, H., Takeda, J., and Fukamizu, A. (2004) Inhibitory effect of the small heterodimer partner on hepatocyte nuclear factor-4 mediates bile acid-induced repression of the human angiotensinogen gene. J. Biol. Chem. 279, 7770-7776
41. Bagamasbad, P., Ziera, T., Borden, S. A., Bonett, R. M., Rozeboom, A. M., Seasholtz, A., and Denver, R. J. (2012) Molecular basis for glucocorticoid induction of the Kruppel-like factor 9 gene in hippocampal neurons. Endocrinology 153, 5334-5345
42. Xie, X., Liao, H., Dang, H., Pang, W., Guan, Y., Wang, X., Shyy, J. Y., Zhu, Y., and Sladek, F. M. (2009) Down-regulation of hepatic HNF4-gene expression during hyperinsulinemia via SREBPs. Mol. Endocrinol. 23, 434-443
43. Boulias, K., Katrakili, N., Bamberg, K., Underhill, P., Greenfield, A., and Talianidis, I. (2005) Regulation of hepatic metabolic pathways by the orphan nuclear receptor SHP. EMBO J. 24, 2624-2633
44. Rizzo, G., Renga, B., Antonelli, E., Passeri, D., Pellicciari, R., and Fiorucci, S. (2005) The methyl transferase PRMT1 functions as co-Activator of farnesoid X receptor (FXR)/9-cis retinoid X receptor and regulates transcription of FXR responsive genes. Mol. Pharmacol. 68, 551-558
45. Topletz, A. R., Le, H. N., Lee, N., Chapman, J. D., Kelly, E. J., Wang, J., and Isoherranen, N. (2013) Hepatic Cyp2d and Cyp26a1 mRNAs and activities are increased during mouse pregnancy. Drug Metab. Dispos. 41, 312-319
46. Thatcher, J. E., and Isoherranen, N. (2009) The role of CYP26 enzymes in retinoic acid clearance. Expert Opin. Drug Metab. Toxicol. 5, 875-886
47. Lai, K., Harnish, D. C., and Evans, M. J. (2003) Estrogen receptor-regulates expression of the orphan receptor small heterodimer partner. J. Biol. Chem. 278, 36418-36429
48. Heikkinen, J., Mäentausta, O., Ylöstalo, P., and Jänne, O. (1981) Changes in serum bile acid concentrations during normal pregnancy, in patients with intrahepatic cholestasis of pregnancy, and in pregnant women with itching. Br. J. Obstet. Gynaecol. 88, 240-245
49. Temesvári, M., Kóbori, L., Paulik, J., Sárvá ry, E., Belic, A., and Monostory, K. (2012) Estimation of drug-metabolizing capacity by cytochrome P450 genotyping and expression. J Pharmacol. Exp. Ther. 341, 294-305
50. Carcillo, J. A., Adedoyin, A., Burckart, G. J., Frye, R. F., Venkataramanan, R., Knoll, C., Thummel, K., Roskos, L., Wilson, J. W., Sereika, S., Romkes, M., Bebia, Z., and Branch, R. A. (2003) Coordinated intrahepatic and extrahepatic regulation of cytochrome p4502D6 in healthy subjects and in patients after liver transplantation. Clin. Pharmacol. Ther. 73, 456-467
51. Ohtsuki, S., Schaefer, O., Kawakami, H., Inoue, T., Liehner, S., Saito, A., Ishiguro, N., Kishimoto, W., Ludwig-Schwellinger, E., Ebner, T., and Terasaki, T. (2012) Simultaneous absolute protein quantification of transporters, cytochromes P450, and UDP-glucuronosyltransferases as a novel approach for the characterization of individual human liver. Comparison with mRNA levels and activities. Drug Metab. Dispos. 40, 83-92