Home LiteratureArticle Details
PMID: 21952236 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Intrinsic sexually dimorphic expression of the principal human CYP3A4 correlated with suboptimal activation of GH/glucocorticoid-dependent transcriptional pathways in men.

Endocrinology ·Vol. 152 ·No. 12 ·2011-12-00 ·Pages 4813-24

Thangavel C, Boopathi E, Shapiro BH

Abstract

Cytochrome P450 (CYP)3A4 is the principal and most abundant human isoform of CYP responsible for the metabolism of more than 50% of all consumed drugs and innumerable endogenous compounds. Expression of CYP3A4 is sexually dimorphic and regulated by the combined actions of GH and glucocorticoids. In the case of the rat, nearly all of the CYPs are "intrinsically" or "inherently" sexually dimorphic, meaning that the expressed sex differences are permanent and irreversible. Using primary hepatocyte cultures derived from men and women exposed to physiologic-like levels of continuous GH (the feminine circulating profile) alone, dexamethasone alone, and the combined regimen, we observed a dramatic inherent CYP3A4 sexual dimorphism (women more than men) with all treatments. The molecular basis for this intrinsic sexually dimorphic expression of CYP3A4 appears to be due, at least in part, to a greater level of hormone-dependent activation and nuclear translocation of both hepatocyte nuclear factor-4α (HNF-4α) and pregnane X receptor in female hepatocytes. Furthermore, these transcription factors exhibited significantly higher DNA binding levels to their specific motifs on the CYP3A4 promoter in female hepatocytes, inferring a possible explanation for the elevated expression of CYP3A4 in women. Accordingly, experiments using HepG2 cells treated with small inhibitory RNA-induced knockdown of HNF-4α and/or transfected with luciferase reporter constructs containing a CYP3A4 promoter lacking HNF-4α-binding motifs demonstrated that GH, to a greater extent dexamethasone, and to the greatest extent the combine hormone regimen, stimulated HNF-4α and pregnane X receptor promoter transactivation, signifying enhanced transcription of CYP3A4 and, thus, identifying a molecular mechanism contributing to the intrinsic sexual dimorphic expression of human CYP3A4.

MeSH Terms
Biological Transport Cells, Cultured Cytochrome P-450 CYP3A/genetics Dexamethasone/pharmacology Glucocorticoids/metabolism Growth Hormone/metabolism Hepatocyte Nuclear Factor 4 Hepatocytes Human Growth Hormone/pharmacology Humans Male Sex Characteristics Sex Factors Transcription Factors/metabolism Transcription, Genetic
Chemicals
Glucocorticoids HNF4A protein, human Hepatocyte Nuclear Factor 4 Transcription Factors Human Growth Hormone Dexamethasone Growth Hormone Cytochrome P-450 CYP3A CYP3A4 protein, human
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Thangavel Chellappagounder
Laboratories of Biochemistry, School of Veterinary Medicine, University of Pennsylvania, 3800 Spruce Street, Philadelphia, Pennsylvania 19104-6009, USA.
Boopathi Ettickan
Shapiro Bernard H
References (56)
56 references, click to expand
  1. Long-term prospective study of body composition and lipid profiles during and after growth hormone (GH) treatment in children with GH deficiency: gender-specific metabolic effects.
    J Clin Endocrinol Metab. 1998 Nov;83(11):3890-6 PMID: 9814464
  2. Feminization of hepatic cytochrome P450s by nominal levels of growth hormone in the feminine plasma profile.
    Mol Pharmacol. 1996 Nov;50(5):1148-56 PMID: 8913346
  3. The human drug metabolizing cytochromes P450.
    J Pharmacokinet Biopharm. 1996 Oct;24(5):461-73 PMID: 9131485
  4. Preservation of hepatocyte nuclear factor-4alpha is associated with zinc protection against TNF-alpha hepatotoxicity in mice.
    Exp Biol Med (Maywood). 2007 May;232(5):622-8 PMID: 17463158
  5. Growth hormone secretion pattern is an independent regulator of growth hormone actions in humans.
    Am J Physiol Endocrinol Metab. 2002 Nov;283(5):E1008-15 PMID: 12376329
  6. Sexual dimorphism in the control of growth hormone secretion.
    Endocr Rev. 1985 Spring;6(2):128-50 PMID: 2861084
  7. The orphan nuclear receptor HNF4alpha determines PXR- and CAR-mediated xenobiotic induction of CYP3A4.
    Nat Med. 2003 Feb;9(2):220-4 PMID: 12514743
  8. Role of human hepatocyte nuclear factor 4alpha in the expression of drug-metabolizing enzymes and transporters in human hepatocytes assessed by use of small interfering RNA.
    Drug Metab Pharmacokinet. 2007 Aug;22(4):287-98 PMID: 17827783
  9. Thyroid hormones act indirectly to increase sex hormone-binding globulin production by liver via hepatocyte nuclear factor-4alpha.
    J Mol Endocrinol. 2009 Jul;43(1):19-27 PMID: 19336534
  10. Differential expression of gender-dependent hepatic isoforms of cytochrome P-450 by pulse signals in the circulating masculine episodic growth hormone profile of the rat.
    J Pharmacol Exp Ther. 2000 Jan;292(1):228-37 PMID: 10604952
  11. The far and distal enhancers in the CYP3A4 gene co-ordinate the proximal promoter in responding similarly to the pregnane X receptor but differentially to hepatocyte nuclear factor-4alpha.
    Biochem J. 2008 Jan 1;409(1):243-50 PMID: 17764444
  12. Transcriptional regulation and expression of CYP3A4 in hepatocytes.
    Curr Drug Metab. 2007 Feb;8(2):185-94 PMID: 17305497
  13. Gender differences in pharmacokinetics.
    Eur J Drug Metab Pharmacokinet. 1996 Apr-Jun;21(2):123-8 PMID: 8839685
  14. Marked gender differences in ambulatory morning growth hormone values in young adults.
    Clin Chem. 1998 Jun;44(6 Pt 1):1289-95 PMID: 9625055
  15. Sex-dependent genetic markers of CYP3A4 expression and activity in human liver microsomes.
    Pharmacogenomics. 2007 May;8(5):443-53 PMID: 17465708
  16. Interindividual differences in hepatic expression of CYP3A4: relationship to genetic polymorphism in the 5'-upstream regulatory region.
    Biochem Biophys Res Commun. 1999 May 27;259(1):201-5 PMID: 10334940
  17. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei.
    Nucleic Acids Res. 1983 Mar 11;11(5):1475-89 PMID: 6828386
  18. Pregnenolone 16 alpha-carbonitrile-inducible P-450 gene family: gene conversion and differential regulation.
    Mol Cell Biol. 1986 Aug;6(8):2969-76 PMID: 3785219
  19. Sex is a major determinant of CYP3A4 expression in human liver.
    Hepatology. 2003 Oct;38(4):978-88 PMID: 14512885
  20. Growth hormone treatment increases cytochrome P450-mediated antipyrine clearance in man.
    J Clin Endocrinol Metab. 1996 May;81(5):1999-2001 PMID: 8626872
  21. Evaluation of pulsatile patterns of growth hormone release in humans: A brief review.
    Am J Hum Biol. 1993;5(6):603-614 PMID: 28548364
  22. Use of human hepatocytes to study P450 gene induction.
    Methods Enzymol. 1996;272:388-401 PMID: 8791798
  23. Identification of a novel polymorphic enhancer of the human CYP3A4 gene.
    Mol Pharmacol. 2004 Feb;65(2):326-34 PMID: 14742674
  24. Sexually dimorphic regulation of hepatic isoforms of human cytochrome p450 by growth hormone.
    J Pharmacol Exp Ther. 2006 Jan;316(1):87-94 PMID: 16160083
  25. Characterization of Phase I and Phase II hepatic drug metabolism activities in a panel of human liver preparations.
    Chem Biol Interact. 1999 Apr 1;118(2):151-69 PMID: 10359459
  26. Summary of information on human CYP enzymes: human P450 metabolism data.
    Drug Metab Rev. 2002 Feb-May;34(1-2):83-448 PMID: 11996015
  27. An amplitude-specific divergence in the pulsatile mode of growth hormone (GH) secretion underlies the gender difference in mean GH concentrations in men and premenopausal women.
    J Clin Endocrinol Metab. 1996 Jul;81(7):2460-7 PMID: 8675561
  28. Liver-enriched transcription factors in liver function and development. Part I: the hepatocyte nuclear factor network and liver-specific gene expression.
    Pharmacol Rev. 2002 Mar;54(1):129-58 PMID: 11870262
  29. Control of pancreas and liver gene expression by HNF transcription factors.
    Science. 2004 Feb 27;303(5662):1378-81 PMID: 14988562
  30. A molecular basis for the sexually dimorphic response to growth hormone.
    Endocrinology. 2007 Jun;148(6):2894-903 PMID: 17332060
  31. Intrinsic sex differences determine expression of growth hormone-regulated female cytochrome P450s.
    Mol Cell Endocrinol. 2004 May 31;220(1-2):31-9 PMID: 15196697
  32. Inherent sexually dimorphic expression of hepatic CYP2C12 correlated with repressed activation of growth hormone-regulated signal transduction in male rats.
    Drug Metab Dispos. 2008 Sep;36(9):1884-95 PMID: 18559485
  33. Interindividual variations in human liver cytochrome P-450 enzymes involved in the oxidation of drugs, carcinogens and toxic chemicals: studies with liver microsomes of 30 Japanese and 30 Caucasians.
    J Pharmacol Exp Ther. 1994 Jul;270(1):414-23 PMID: 8035341
  34. Effects of growth hormone deficiency and rhGH replacement therapy on the 6beta-hydroxycortisol/free cortisol ratio, a marker of CYP3A activity, in growth hormone-deficient children.
    Eur J Clin Pharmacol. 2004 Oct;60(8):559-64 PMID: 15365655
  35. Dexamethasone induces pregnane X receptor and retinoid X receptor-alpha expression in human hepatocytes: synergistic increase of CYP3A4 induction by pregnane X receptor activators.
    Mol Pharmacol. 2000 Aug;58(2):361-72 PMID: 10908304
  36. Gene structure of CYP3A4, an adult-specific form of cytochrome P450 in human livers, and its transcriptional control.
    Eur J Biochem. 1993 Dec 1;218(2):585-95 PMID: 8269949
  37. Separate and interactive regulation of cytochrome P450 3A4 by triiodothyronine, dexamethasone, and growth hormone in cultured hepatocytes.
    J Clin Endocrinol Metab. 1998 Jul;83(7):2411-6 PMID: 9661620
  38. Phenobarbital induction of hepatic CYP2B1 and CYP2B2: pretranscriptional and post-transcriptional effects of gender, adult age, and phenobarbital dose.
    Mol Pharmacol. 1996 Mar;49(3):523-31 PMID: 8643092
  39. Growth hormone (GH)-deficient men are more responsive to GH replacement therapy than women.
    J Clin Endocrinol Metab. 1997 Feb;82(2):550-5 PMID: 9024252
  40. Insulin-like growth factor I levels during growth hormone (GH) replacement in GH-deficient adults: a gender difference.
    Growth Horm IGF Res. 2004 Dec;14(6):436-41 PMID: 15519251
  41. Gender differences in the responsiveness of the sex-dependent isoforms of hepatic P450 to the feminine plasma growth hormone profile.
    Endocrinology. 1999 Mar;140(3):1245-54 PMID: 10067850
  42. Gender differences in rhGH-induced changes in body composition in GH-deficient adults.
    J Clin Endocrinol Metab. 2001 Sep;86(9):4161-5 PMID: 11549643
  43. CYP3A4 inducible model for in vitro analysis of human drug metabolism using a bioartificial liver.
    Hepatology. 2003 Mar;37(3):665-73 PMID: 12601364
  44. Gender differences in drug metabolism regulated by growth hormone.
    Int J Biochem Cell Biol. 1995 Jan;27(1):9-20 PMID: 7757886
  45. Attenuated expression of episodic growth hormone-induced CYP2C11 in female rats associated with suboptimal activation of the Jak2/Stat5B and other modulating signaling pathways.
    Drug Metab Dispos. 2007 Nov;35(11):2102-10 PMID: 17682071
  46. Substrates of human hepatic cytochrome P450 3A4.
    Toxicology. 1995 Dec 15;104(1-3):1-8 PMID: 8560487
  47. Cyclin-dependent kinase 2 negatively regulates human pregnane X receptor-mediated CYP3A4 gene expression in HepG2 liver carcinoma cells.
    J Biol Chem. 2008 Nov 7;283(45):30650-7 PMID: 18784074
  48. Epidermal growth factor regulation of female-dependent CYP2A1 and CYP2C12 in primary rat hepatocyte culture.
    Drug Metab Dispos. 2001 Feb;29(2):111-20 PMID: 11159799
  49. Regulation of cyp3a gene transcription by the pregnane x receptor.
    Annu Rev Pharmacol Toxicol. 2002;42:1-23 PMID: 11807162
  50. Gender differences in the effects of long term growth hormone (GH) treatment on bone in adults with GH deficiency.
    J Clin Endocrinol Metab. 1999 Jun;84(6):2002-7 PMID: 10372701
  51. Sex differences in the expression of hepatic drug metabolizing enzymes.
    Mol Pharmacol. 2009 Aug;76(2):215-28 PMID: 19483103
  52. Regulation of murine cytochrome c oxidase Vb gene expression during myogenesis: YY-1 and heterogeneous nuclear ribonucleoprotein D-like protein (JKTBP1) reciprocally regulate transcription activity by physical interaction with the BERF-1/ZBP-89 factor.
    J Biol Chem. 2004 Aug 20;279(34):35242-54 PMID: 15190078
  53. Transcription factor binding to a putative double E-box motif represses CYP3A4 expression in human lung cells.
    Mol Pharmacol. 2007 Sep;72(3):514-25 PMID: 17548528
  54. Hepatic steroid hydroxylating enzymes are controlled by the sexually dimorphic pattern of growth hormone secretion in normal and dwarf rats.
    FASEB J. 1992 Jan 6;6(2):711-8 PMID: 1537461
  55. Strain independent elevation of hepatic mono-oxygenase enzymes in female mice.
    Xenobiotica. 1987 Sep;17(9):1095-102 PMID: 3687065
  56. Gender as a risk factor for adverse events to medications.
    Drugs. 1995 Jul;50(1):1-6 PMID: 7588082
Article Info
Journal
Endocrinology
Abbr.
Endocrinology
ISSN
1945-7170
Published
2011-12-00
Epub
2011-00-27
Pages
4813-24
Language
English
Region
United States
NLM ID
0375040
PMCID
PMC3230058
Subset
IM
Grants
NICHD NIH HHS · R01 HD061285 · United States
NICHD NIH HHS · HD-061285 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com