Sex steroid hormones regulate constitutive expression of Cyp2e1 in female mouse liver

American Journal of Physiology - Endocrinology and Metabolism

Volumn 304, Issue 10, 2013, Pages

  Konstandi, Maria ^a,b   Cheng, Jie ^b   Gonzalez, Frank J ^b  

^a UNIVERSITY OF IOANNINA   (Greece)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

17 estradiol; Cyp2e1; Estrous cycle; Mice; Progesterone

Indexed keywords

BETA CATENIN; CYTOCHROME P450 2E1; ESTRADIOL; ESTROGEN; GROWTH HORMONE; HEPATOCYTE NUCLEAR FACTOR 1ALPHA; PHOSPHATIDYLINOSITOL 3 KINASE; PROGESTERONE; PROTEIN KINASE B; SEX HORMONE; STAT5B PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TAMOXIFEN; TRANSCRIPTION FACTOR FKHR;

ANIMAL TISSUE; ARTICLE; ESTRUS; ESTRUS CYCLE; FEMALE; HORMONE BLOOD LEVEL; HORMONE SUBSTITUTION; LIVER; MALE; METESTRUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DIFFERENTIATION; SIGNAL TRANSDUCTION; UPREGULATION;

17Β-ESTRADIOL; CYP2E1; ESTROUS CYCLE; MICE; PROGESTERONE;

ANIMALS; BLOTTING, WESTERN; CYTOCHROME P-450 CYP2E1; ESTRADIOL; ESTROGEN ANTAGONISTS; ESTROUS CYCLE; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHOSPHATIDYLINOSITOL 3-KINASES; PROGESTERONE; PROTO-ONCOGENE PROTEINS C-AKT; REAL-TIME POLYMERASE CHAIN REACTION; RNA; STAT5 TRANSCRIPTION FACTOR; TAMOXIFEN;

EID: 84878532413     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00585.2012     Document Type: Article

References (84)

1. Assaf S, Hazard D, Pitel F, Morisson M, Alizadeh M, Gondret F, Diot C, Vignal A, Douaire M, Lagarrigue S. Cloning of cDNA encoding the nuclear form of chicken sterol response element binding protein-2 (SREBP-2), chromosomal localization, and tissue expression of chicken SREBP-1 and-2 genes. Poult Sci 82: 54-61, 2003.
2. Akiyama TE, Gonzalez FJ. Regulation of P450 genes by liver-enriched transcription factors and nuclear receptors. Biochim Biophys Acta 1619: 223-234, 2003.
3. Banerjee S, Shang TQ, Wilson AM, Moore AL, Strand SE, Gordon MP, Doty SL. Expression of functional mammalian P450 2E1 in hairy root cultures. Biotechnol Bioeng 77: 462-466, 2002.
4. Baynes JW, Dominiczak MH. Medical Biochemistry (2nd ed). Philadelphia, PA: Elsevier Mosby, p. 555, 2005.
5. Bebia Z, Buch SC, Wilson JW, Frye RF, Romkes M, Cecchetti A, Chaves-Gnecco D, Branch RA. Bioequivalence revisited: influence of age and sex on CYP enzymes. Clin Pharmacol Ther 76: 618-627, 2004.
6. Bellward GD, Chang T, Rodrigues B, McNeill JH, Maines S, Ryan DE, Levin W, Thomas PE. Hepatic cytochrome P-450j induction in the spontaneously diabetic BB rat. Mol Pharmacol 33: 140-143, 1988.
7. Bjornstrom L, Killic E, Norman M, Parker MG, Sjoberg M. Cross-talk between Stat5b and estrogen receptor-alpha and beta in mammary epithelial cells. J Mol Endocrinol 27: 93-106, 2001.
8. Bruckner JV, Ramanathan R, Lee KM, Muralidhara S. Mechanisms of circadian rhythmicity of carbon tetrachloride hepatotoxicity. J Pharmacol Exp Ther 300: 273-281, 2002.
9. Butura A, Nilsson K, Morgan K, Morgan TR, French SW, Johansson I, Schuppe-Koistinen I, Ingelman-Sundberg M. The impact of CYP2E1 on the development of alcoholic liver disease as studied in a transgenic mouse model. J Hepatol 50: 572-583, 2009.
10. Cederbaum AI. Cytochrome P450 2E1-dependent oxidant stress and upregulation of anti-oxidant defense in liver cells. J Gastroenterol Hepatol 21, Suppl 3: S22-S25, 2006.
11. Chen GF, Ronis MJ, Ingelman-Sundberg M, Badger TM. Hormonal regulation of microsomal cytochrome P4502E1 and P450 reductase in rat liver and kidney. Xenobiotica 29: 437-451, 1999.
12. Cheung C, Yu AM, Ward JM, Krausz KW, Akiyama TE, Feigenbaum L, Gonzalez FJ. The Cyp2e1-humanized transgenic mouse: role of Cyp2e1 in acetaminophen hepatotoxicity. Drug Metab Dispos 33: 449-457, 2005.
13. Choi HK, Waxman DJ. Growth hormone, but not prolactin, maintains, low-level activation of STAT5a and STAT5b in female rat liver. Endocrinology 140: 5126-5135, 1999.
14. Clodfelter KH, Holloway MG, Hodor P, Park SH, Ray WJ, Waxman DJ. Sex-dependent liver gene expression is extensive and largely dependent upon signal transducer and activator of transcription 5b (STAT5b): STAT5b-dependent activation of male genes and repression of female genes revealed by microarray analysis. Mol Endocrinol 20: 1333-1351, 2006.
15. Collom SL, Laddusaw RM, Burch AM, Kuzmic P, Perry Jn MD, Miller GP. CYP2E1 substrate inhibition: mechanistic interpretation through an effector site for monocyclic compounds. J Biol Chem 283: 3487-3496, 2008.
16. Deng QG, She H, Cheng JH, French SW, Koop DR, Xiong S, Tsukamoto H. Steatohepatitis induced by intragastric overfeeding in mice. Hepatology 42: 905-914, 2005.
17. Dong ZG, Hong JY, Ma QA, Li DC, Bullock J, Gonzalez FJ, Park SS, Gelboin HV, Yang CS. Mechanism of induction of cytochrome P-450ac (P-450j) in chemically induced and spontaneously diabetic rats. Arch Biochem Biophys 263: 29-35, 1988.
18. Doty SL, Shang TQ, Wilson AM, Tangen J, Westergreen AD, Newman LA, Strand SE, Gordon MP. Enhanced metabolism of halogenated hydrocarbons in transgenic plants containing mammalian cytochrome P450 2E1. Proc Natl Acad Sci USA 97: 6287-6291, 2000.
19. El-Mansoury AM, Morgan NG. Activation of protein kinase C modulates alpha2-adrenergic signalling in rat pancreatic islets. Cell Signal 10: 637-643, 1998.
20. Fata JE, Chaudhary V, Khokha R. Cellular turnover in the mammary gland is correlated with systemic levels of progesterone and not 17β-estradiol during the estrous cycle. Biol Reprod 65: 680-688, 2001.
21. Gergel D, Misik V, Riesz P, Cederbaum AI. Inhibition of rat and human cytochrome P4502E1 catalytic activity and reactive oxygen radical formation by nitric oxide. Arch Biochem Biophys 337: 239-250, 1997.
22. Gonzalez FJ. The 2006 Bernard B Brodie Award Lecture. Cyp2e1. Drug Metab Dispos 35: 1-8, 2007.
23. Guengerich FP, Kim DH, Iwasaki M. Role of human cytochrome P-450 IIE1 in the oxidation of many low molecular weight cancer suspects. Chem Res Toxicol 4: 168-4179, 1991.
24. Guengerich FP. Catalytic selectivity of human cytochrome P450 enzymes: relevance to drug metabolism and toxicity. Toxicol Lett 70: 133-138, 1994.
25. Hargreaves MB, Jones BC, Smith DA, Gescher A. Inhibition of pnitrophenol hydroxylase in rat liver microsomes by small aromatic and heterocyclic molecules. Drug Metab Dispos 22: 806-810, 1994.
26. Hel Z, Stringer E, Mestecky J. Sex steroid hormones, hormonal contraception, and the immunobiology of human immunodeficiency virus-1 infection. Endocr Rev 31: 79-97, 2010.
27. Holloway MG, Laz EV, Waxman DJ. Co-dependence of growth hormone-responsive, sexually dimorphic hepatic gene expression on signal transducer and activator of transcription 5b and hepatic nuclear factor 4-α. Mol Endocrinol 20: 647-660, 2006.
28. Hong JY, Ning SM, Ma BL, Lee MJ, Pan JM, Yang CS. Roles of pituitary hormones in the regulation of hepatic cytochrome P450IIE1 in rats and mice. Arch Biochem Biophys 281: 132-138, 1990.
29. Ingelman-Sundberg M. Pharmacogenetics of cytochrome P450 and its applications in drug therapy: the past, present and future. Trends Pharmacol Sci 25: 193-200, 2004.
30. Järveläinen HA, Fang C, Ingelman-Sundberg M, Lukkari TA, Sippel H, Lindros KO. Kupffer cell inactivation alleviates ethanol-induced steatosis and CYP2E1 induction but not inflammatory responses in rat liver. J Hepatol 32: 900-910, 2000.
31. Khatsenko O, Kikkawa Y. Nitric oxide differentially affects constitutive cytochrome P450 isoforms in rat liver. J Pharmacol Exp Ther 280: 1463-1470, 1997.
32. Kim SG, Novak RF. Cytochrome P450IIE1 metabolism of pyridines: evidence for production of a reactive intermediate which exhibits redoxcycling activity and causes DNA damage. Adv Exp Med Biol 283: 753-758, 1991.
33. Kim RB, O'Shea D. Interindividual variability of chlorzoxazone 6-hydroxylation in men and women and its relationship to CYP2E1 genetic polymorphisms. Clin Pharmacol Ther 57: 645-655, 1995.
34. Kim YC, Yim HK, Jung YS, Park JH, Kim SY. Hepatic injury induces contrasting response in liver and kidney to chemicals that are metabolically activated: role of male sex hormone. Toxicol Appl Pharmacol 223: 56-65, 2007.
35. Kohjima M, Enjoji M, Higuchi N, Kato M, Kotoh K, Yoshimoto T, Fujino T, Yada M, Yada R, Harada N, Takayanagi R, Nakamuta M. Re-evaluation of fatty acid metabolism-related gene expression in nonalcoholic fatty liver disease. Int J Mol Med 20: 351-358, 2007.
36. Koop DR. Hydroxylation of p-nitrophenol by rabbit ethanol-inducible cytochrome P-450 isozyme 3a. Mol Pharmacol 29: 399-404, 1986.
37. Konstandi M, Harkitis P, Kostakis D, Marselos M, Johnson EO, Lang MA. D2-receptor-linked signaling pathways regulate the expression of hepatic CYP2E1. Life Sci 82: 1-10, 2008.
38. Kouzmenko AP, Takeyama K, Ito S, Furutani T, Sawatsubashi S, Maki A, Suzuki E, Kawasaki Y, Akiyama T, Tabata T, Kato S. Wnt/beta-catenin and estrogen signaling converge in vivo. J Biol Chem 279: 40255-40258, 2004.
39. Lang MA, Gielen JE, Nebert DW. Genetic evidence for many unique liver microsomal P-450 mediated monoxygenase activities in heterogeneic stock mice. J Biol Chem 256: 12068-12075, 1981.
40. Leclercq IA, Farrell GC, Field J, Bell DR, Gonzalez FJ, Robertson GR. CYP2E1 and CYP4A as microsomal catalysts of lipid peroxides in murine nonalcoholic steatohepatitis. J Clin Invest 105: 1067-1075, 2000.
41. Li L, He D, Wilborn TW, Falany JL, Falany CN. Increased SULT1E1 activity in HepG2 hepatocytes decreases growth hormone stimulation of STAT5b phosphorylation. Steroids 74: 20-29, 2009.
42. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem 193: 265-275, 1951.
43. Massarweh S, Osborne CK, Creighton CJ, Qin L, Tsimelzon A, Huang S, Weiss H, Rimawi M, Schiff R. Tamoxifen resistance in breast tumors is driven by growth factor receptor signaling with repression of classic estrogen receptor genomic function. Cancer Res 68: 826-833, 2008.
44. Minamiyama Y, Takemura S, Imaoka S, Funae Y, Tanimoto Y, Inoue M. Irreversible inhibition of cytochrome P450 by nitric oxide. J Pharmacol Exp Ther 283: 1479-1485, 1997.
45. Mode A, Gustafsson JA. Sex and the liver-a journey through five decades. Drug Metab Rev 38: 197-207, 2006.
46. Moreira PI, Custódio JB, Nunes E, Moreno A, Seiça R, Oliveira CR, Santos MS. Estradiol affects liver mitochondrial function in ovariectomized and tamoxifen-treated ovariectomized female rats. Toxicol Appl Pharmacol 221: 102-110, 2007.
47. Mulholland DJ, Dedhar S, Coetzee GA, Nelson CC. Interaction of nuclear receptors with the Wnt/beta-catenin/Tcf signaling axis: Wnt you like to know? Endocr Rev 26: 898-915, 2005.
48. Nelson JF, Felicio LS, Osterburg HH, Finch CE. Altered profiles of estradiol and progesterone associated with prolonged estrous cycles and persistent vaginal cornification in aging C57BL/6J mice. Biol Reprod 24: 784-794, 1981.
49. Nelson LE, Sheridan MA. Regulation of somatostatins and their receptors in fish. Gen Comp Endocrinol 142: 117-133, 2005.
50. Ohe T, Hirobe M, Mashino T. Novel metabolic pathway of estrone and 17β-estradiol catalysed by cytochrome P-450. Drug Metab Dispos 28: 110-112, 2000.
51. Peng HM, Coon MJ. Regulation of rabbit P4502E1 expression in HepG2 cells by insulin and thyroid hormone. Mol Pharmacol 54: 740-747, 1998.
52. Persad S, Troussard AA, McPhee TR, Mulholland DJ, Dedhar S. Tumor suppressor PTEN inhibits nuclear accumulation of beta-catenin and T cell/lymphoid enhancer factor 1-mediated transcriptional activation. J Cell Biol 153: 1161-1174, 2001.
53. Reinke LA, Moyer MJ. p-Nitrophenol hydroxylation. A microsomal oxidation which is highly inducible by ethanol. Drug Metab Dispos 13: 548-552, 1985.
54. Roberts BJ, Song BJ, Soh Y, Park SS, Shoaf SE. Ethanol induces CYP2E1 by protein stabilization. Role of ubiquitin conjugation in the rapid degradation of CYP2E1. J Biol Chem 270: 29632-29635, 1995.
55. Robertson G, Leclercq I, Farrell GC. Nonalcoholic steatosis and steatohepatitis. II. Cytochrome P-450 enzymes and oxidative stress. Am J Physiol Gastrointest Liver Physiol 281: G1135-G1139, 2001.
56. Ronis M, Lindros KO, Ingelman-Sundberg M. In: Cytochromes P450, Metabolic and Toxicological Aspects. Boca Raton, FL: CRC, 1996, p. 211-239.
57. Rubí B, Ljubicic S, Pournourmohammadi S, Carobbio S, Armanet M, Bartley C, Maechler P. Dopamine D2-like receptors are expressed in pancreatic beta cells and mediate inhibition of insulin secretion. J Biol Chem 280: 36824-36832, 2005.
58. Santen RJ, Allred DC, Ardoin SP, Archer DF, Boyd N, Braunstein GD, Burger HG, Colditz GA, Davis SR, Gambacciani M, Gower BA, Henderson VW, Jarjour WN, Karas RH, Kleerekoper M, Lobo RA, Manson JE, Marsden J, Martin KA, Martin L, Pinkerton JV, Rubinow DR, Teede H, Thiboutot DM, Utian Endocrine Society WH. J Postmenopausal hormone therapy: an Endocrine Society scientific statement. Clin Endocrinol Metab 95, Suppl 1: S1-S66, 2010.
59. Scandlyn MJ, Stuart EC, Somers-Edgar TJ, Menzies AR, Rosengren RJ. A new role for tamoxifen in oestrogen receptor-negative breast cancer when it is combined with epigallocatechin gallate. Br J Cancer 99: 1056-1063, 2008.
60. Sekine S, Lan BY, Bedolli M, Feng S, Hebrok M. Liver-specific loss of beta-catenin blocks glutamine synthesis pathway activity and cytochrome p450 expression in mice. Hepatology 43: 817-825, 2006.
61. Sharma M, Chuang WW, Sun Z. Phosphatidylinositol 3-kinase/Akt stimulates androgen pathway through GSK3beta inhibition and nuclear beta-catenin accumulation. J Biol Chem 277: 30935-30941, 2002.
62. Sidhu JS, Fei L, Boyle SM, Omiecinski CJ. PI3k inhibitors reverse the Suppressive actions of insulin on CYP2E1 expression by activating stress-response pathways in primary rat hepatocytes. Mol Pharmacol 59: 1138-1146, 2001.
63. Song BJ, Matsunaga T, Hardwick JP, Park SS, Veech RL, Yang CS, Gelboin HV, Gonzalez FJ. Stabilization of cytochrome P450j messenger ribonucleic acid in the diabetic rat. Mol Endocrinol 1: 542-547, 1987.
64. Song BJ, Veech RL, Saenger P. Cytochrome P450IIE1 is elevated in lymphocytes from poorly controlled insulin-dependent diabetics. J Clin Endocrinol Metab 71: 1036-1040, 1990.
65. Thummel KE, Schenkman JB. Effects of testosterone and growth hormone treatment on hepatic microsomal P450 expression in the diabetic rat. Mol Pharmacol 37: 119-129, 1990.
66. Tsutsumi M, Matsuda Y, Takada A. Role of ethanol-inducible cytochrome P-450 2E1 in the development of hepatocellular carcinoma by the chemical carcinogen, N-nitrosodimethylamine. Hepatology 18: 1483-1489, 1993.
67. Veldhuis JD, Bowers CY. Sex-steroid modulation of growth hormone (GH) secretory control: three-peptide ensemble regulation under dual feedback restraint by GH and IGF-I. Endocrine 22: 25-40, 2003.
68. Verras M, Sun Z. Beta-catenin is involved in insulin-like growth factor 1-mediated transactivation of the androgen receptor. Mol Endocrinol 19: 391-398, 2005.
69. Walmer DK, Wrona MA, Hughes CL, Nelson KG. Lactoferrin expression in the mouse reproductive tract during the natural estrous cycle: correlation with circulating estradiol and progesterone. Endocrinology 131: 1458-1466, 1992.
70. Wauthier V, Sugathan A, Meyer RD, Dombkowski AA, Waxman DJ. Intrinsic sex differences in the early growth hormone responsiveness of sex-specific genes in mouse liver. Mol Endocrinol 24: 667-678, 2010.
71. Waxman DJ, Morrissey JJ, LeBlanc GA. Female-predominant rat hepatic P-450 forms j (IIE1) and 3 (IIA1) are under hormonal regulatory controls distinct from those of the sex-specific P-450 forms. Endocrinology 124: 2954-2966, 1989.
72. Waxman DJ. P450 gene induction by structurally diverse xenochemicals: central role of nuclear receptors CAR, PXR, and PPAR. Arch Biochem Biophys 369: 11-23, 1999.
73. Waxman DJ, Chang TKH. Hormonal regulation of liver cytochrome P450 enzymes. In: Cytochrome P450. Structure, Mechanism, and Biochemistry (edited by Ortiz de Montellano PR). New York: Kluwer Academic/ Plenum, 2005, p. 347-376.
74. Waxman DJ, O'Connor C. Growth hormone regulation of sex-dependent liver gene expression. Mol Endocrinol 20: 2613-2629, 2006.
75. Waxman DJ, Holloway MG. Sex differences in the expression of hepatic drug metabolizing enzymes. Mol Pharmacol 76: 215-228, 2009.
76. Williams MT, Simonet LC. Effects of growth hormone on cytochrome P-450j. Biochem Biophys Res Commun 155: 392-397, 1988.
77. Woodcroft KJ, Hafner MS, Novak RF. Insulin signaling in the transcriptional and posttranscriptional regulation of CYP2E1 expression. Hepatology 35: 263-273, 2002.
78. Wu WX, Owiny J, Zhang Q, Ma XH, Nathanielsz PW. Regulation of the estrogen receptor and its messenger ribonucleic acid in the ovariectomized sheep myometrium and endometrium: the role of estradiol and progesterone. Biol Reprod 55: 762-768, 1996.
79. Yamazaki H, Guo Z, Guengerich FP. Selectivity of cytochrome P4502E1 in chlorzoxazone 6-hydroxylation. Drug Metab Dispos 23: 438-440, 1995.
80. Yamazoe Y, Murayama N, Shimada M, Yamauchi K, Kato R. Cytochrome P450 in livers of diabetic rats: regulation by growth hormone and insulin. Arch Biochem Biophys 268: 567-575, 1989.
81. Yang CS, Yoo JS, Ishizaki H, Hong JY. Cytochrome P450IIE1: roles in nitrosamine metabolism and mechanisms of regulation. Drug Metab Rev 22: 147-159, 1990.
82. Yun YP, Casazza JP, Sohn DH, Veech RL, Song BJ. Pretranslational activation of cytochrome P450IIE during ketosis induced by a high fat diet. Mol Pharmacol 41: 474-479, 1992.
83. Zarrow MX. In: Experimental Endocrinology. A Sourcebook of Basic Techniques. New York and London: Academic, 1964, pp. 194 and 308.
84. Zeng T, Xie KQ. Ethanol and liver: recent advances in the mechanisms of ethanol-induced hepatosteatosis. Arch Toxicol 83: 1075-1081, 2009.