Expression and methylation status of female-predominant GH-dependent liver genes are modified by neonatal androgenization in female mice

Molecular and Cellular Endocrinology

Volumn 382, Issue 2, 2014, Pages 825-834

  Ramirez, Maria Cecilia ^a   Zubeldía Brenner, Lautaro ^a   Wargon, Victoria ^a   Ornstein, Ana María ^a   Becu Villalobos, Damasia ^a  

^a Universidad Nacional de Río Cuarto Consejo Nacional de Investigaciones Científicas y Técnicas   (Argentina)

Author keywords

Cyps; DNA methylation; GH; Liver; Neonatal testosterone; Sexual differences

Indexed keywords

ANDROGEN; DNA; ENDOCRINE DISRUPTOR; GROWTH HORMONE; MESSENGER RNA; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CYP7B1 GENE; DNA METHYLATION; FEMALE; GENE EXPRESSION; HNF6 GENE; LIVER; MALE; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; SEX DIFFERENCE; SEX DIFFERENTIATION; SEXUAL DEVELOPMENT; SIGNAL TRANSDUCTION;

CYPS; DNA METHYLATION; GH; LIVER; NEONATAL TESTOSTERONE; SEXUAL DIFFERENCES;

ANDROGENS; ANIMALS; ANIMALS, NEWBORN; DNA METHYLATION; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH HORMONE; HEPATOCYTE NUCLEAR FACTOR 6; LIVER; MALE; MICE; PROMOTER REGIONS, GENETIC; SEX CHARACTERISTICS; SIGNAL TRANSDUCTION; STEROID HYDROXYLASES; TESTOSTERONE; VIRILISM;

EID: 84888416545     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.11.003     Document Type: Article

References (52)

1. Anderson G.D. Sex and racial differences in pharmacological response: where is the evidence? Pharmacogenetics, pharmacokinetics, and pharmacodynamics. J. Womens Health (Larchmt.) 2005, 14:19-29.
2. Arnold A.P., Gorski R.A. Gonadal steroid induction of structural sex differences in the central nervous system. Annu. Rev. Neurosci. 1984, 7:413-442.
3. Ayonrinde O.T., Olynyk J.K., Beilin L.J., Mori T.A., Pennell C.E., de Klerk N., Oddy W.H., Shipman P., Adams L.A. Gender-specific differences in adipose distribution and adipocytokines influence adolescent nonalcoholic fatty liver disease. Hepatology 2011, 53:800-809.
4. Becu-Villalobos D. Diferenciación sexual del cerebro. Genética vs. epigenética. Medicina 2007, 67:397-402.
5. Becu-Villalobos D., Libertun C. Development of GnRH neuron regulation in the female rat. Cell. Mol. Neurobiol. 1995, 15:165-176.
6. Becu-Villalobos D., Gonzalez Iglesias A., Diaz-Torga G.S., Libertun C. Sexual differentiation and gonadotropins secretion in the rat. Cell. Mol. Neurobiol. 1997, 17:699-715.
7. Bhadhprasit W., Sakuma T., Kawasaki Y., Nemoto N. Drug Metab Dispos. 2011, 39:490-497.
8. Boergesen M., Pedersen T.A., Gross B., van Heeringen S.J., Hagenbeek D., Bindesboll C., Caron S., Lalloyer F., Steffensen K.R., Nebb H.I., Gustafsson J.A., Stunnenberg H.G., Staels B., Mandrup S. Genome-wide profiling of liver X receptor, retinoid X receptor, and peroxisome proliferator-activated receptor alpha in mouse liver reveals extensive sharing of binding sites. Mol. Cell Biol. 2012, 32:852-867.
9. Cheriathundam E., Doi S.Q., Knapp J.R., Jasser M.Z., Kopchick J.J., Alvares A.P. Consequences of overexpression of growth hormone in transgenic mice on liver cytochrome P450 enzymes. Biochem. Pharmacol. 1998, 55:1481-1487.
10. Chowen J.A., Argente J., Gonzalez-Parra S., Garcia-Segura L.M. Differential effects of the neonatal and adult sex steroid environments on the organization and activation of hypothalamic growth hormone-releasing hormone and somatostatin neurons. Endocrinology 1993, 133:2792-2802.
11. Conforto T.L., Zhang Y., Sherman J., Waxman D.J. Impact of CUX2 on the female mouse liver transcriptome: activation of female-biased genes and repression of male-biased genes. Mol. Cell Biol. 2012, 32:4611-4627.
12. Cui J.Y., Renaud H.J., Klaassen C.D. Ontogeny of novel cytochrome P450 gene isoforms during postnatal liver maturation in mice. Drug Metab. Dispos. 2012, 40:1226-1237.
13. Dhir R.N., Thangavel C., Shapiro B.H. 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, 35:2102-2110.
14. Dorner G., Docke F., Gotz F., Rohde W., Stahl F., Tonjes R. Sexual differentiation of gonadotrophin secretion, sexual orientation and gender role behavior. J. Steroid Biochem. 1987, 27:1081-1087.
15. Garcia-Carpizo V., Ruiz-Llorente L., Fraga M., Aranda A. The growing role of gene methylation on endocrine function. J. Mol. Endocrinol. 2011, 47:R75-R89.
16. Garcia-Tornadu I., Rubinstein M., Gaylinn B.D., Hill D., Arany E., Low M.J., Diaz-Torga G., Becu-Villalobos D. GH in the dwarf dopaminergic D2 receptor knockout mouse: somatotrope population, GH release, and responsiveness to GH-releasing factors and somatostatin. J. Endocrinol. 2006, 190:611-619.
17. Holloway M.G., Laz E.V., Waxman D.J. Codependence of growth hormone-responsive, sexually dimorphic hepatic gene expression on signal transducer and activator of transcription 5b and hepatic nuclear factor 4alpha. Mol. Endocrinol. 2006, 20:647-660.
18. Ingman W.V., Robertson S.A. Transforming growth factor-beta1 null mutation causes infertility in male mice associated with testosterone deficiency and sexual dysfunction. Endocrinology 2007, 148:4032-4043.
19. Jansson J.O., Frohman L.A. Differential effects of neonatal and adult androgen exposure on the growth hormone secretory pattern in male rats. Endocrinology 1987, 120:1551-1557.
20. Lacau-Mengido I.M., Mejía M., Diaz-Torga G., Gonzalez Iglesias A., Formía N., Libertun C., Becu-Villalobos D. Endocrine studies in ivermectin-treated heifers from birth to puberty. J. Anim. Sci. 2000, 78:1-8.
21. Lahuna O., Rastegar M., Maiter D., Thissen J.P., Lemaigre F.P., Rousseau G.G. Involvement of STAT5 (signal transducer and activator of transcription 5) and HNF-4 (hepatocyte nuclear factor 4) in the transcriptional control of the hnf6 gene by growth hormone. Mol. Endocrinol. 2000, 14:285-294.
22. Landsman T., Waxman D.J. Role of the cytokine-induced SH2 domain-containing protein CIS in growth hormone receptor internalization. J. Biol. Chem. 2005, 280:37471-37480.
23. Lenz K.M., Nugent B.M., McCarthy M.M. Sexual differentiation of the rodent brain: dogma and beyond. Front. Neurosci. 2012, 6:26.
24. Leuenberger N., Pradervand S., Wahli W. Sumoylated PPARalpha mediates sex-specific gene repression and protects the liver from estrogen-induced toxicity in mice. J. Clin. Invest. 2009, 119:3138-3148.
25. Li Z., Tuteja G., Schug J., Kaestner K.H. Foxa1 and Foxa2 are essential for sexual dimorphism in liver cancer. Cell 2012, 148:72-83.
26. Liao D., Porsch-Hallstrom I., Gustafsson J.A., Blanck A. Sex differences at the initiation stage of rat liver carcinogenesis-influence of growth hormone. Carcinogenesis 1993, 14:2045-2049.
27. Livne I., Silverman A.J., Gibson M.J. Reversal of reproductive deficiency in the hpg male mouse by neonatal androgenization. Biol. Reprod. 1992, 47:561-567.
28. Morris J.A., Jordan C.L., Breedlove S.M. Sexual differentiation of the vertebrate nervous system. Nat. Neurosci. 2004, 7:1034-1039.
29. Mueller K.M., Themanns M., Friedbichler K., Kornfeld J.W., Esterbauer H., Tuckermann J.P., Moriggl R. Hepatic growth hormone and glucocorticoid receptor signaling in body growth, steatosis and metabolic liver cancer development. Mol. Cell Endocrinol. 2012, 361:1-11.
30. NgÔ V., Gourdji D., Laverrière J.N. Mol Cell Biol. 1996, 6:3245-3254.
31. Noain D., Perez-Millan M.I., Bello-Gay E., Luque G.M., Casas Cordero R., Gelman D., Peper M., Garcia-Tornadu I., Low M.J., Becu-Villalobos D., Rubinstein M. Central dopamine D2 receptors regulate growth hormone-dependent body growth and pheromone signaling to conspecific males. J. Neurosci. 2013, 33:5834-5842.
32. Noshiro M., Negishi M. Pretranslational regulation of sex-dependent testosterone hydroxylases by growth hormone in mouse liver. J. Biol. Chem. 1986, 261:15923-15927.
33. Nugent B.M., McCarthy M.M. Epigenetic underpinnings of developmental sex differences in the brain. Neuroendocrinology 2011, 93:150-158.
34. Odom D.T., Dowell R.D., Jacobsen E.S., Gordon W., Danford T.W., MacIsaac K.D., Rolfe P.A., Conboy C.M., Gifford D.K., Fraenkel E. Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nat. Genet. 2007, 39:730-732.
35. Ramirez M.C., Luque G.M., Ornstein A.M., Becu-Villalobos D. Differential neonatal testosterone imprinting of GH-dependent liver proteins and genes in female mice. J. Endocrinol. 2010, 207:301-308.
36. Ramirez M.C., Bourguignon N.S., Bonaventura M.M., Lux-Lantos V., Libertun C., Becu-Villalobos D. Neonatal xenoestrogen exposure alters growth hormone-dependent liver proteins and genes in adult female rats. Toxicol. Lett. 2012, 213:325-331.
37. Rothwell P.M., Coull A.J., Silver L.E., Fairhead J.F., Giles M.F., Lovelock C.E., Redgrave J.N., Bull L.M., Welch S.J., Cuthbertson F.C., Binney L.E., Gutnikov S.A., Anslow P., Banning A.P., Mant D., Mehta Z. Population-based study of event-rate, incidence, case fatality, and mortality for all acute vascular events in all arterial territories (Oxford Vascular Study). Lancet 2005, 366:1773-1783.
38. Sugathan A., Waxman D.J. Genome-wide analysis of chromatin states reveals distinct mechanisms of sex-dependent gene regulation in male and female mouse liver. Mol. Cell Biol. 2013, 33:3594-3610.
39. Takemoto N., Iizuka N., Yamada-Okabe H., Hamada K., Tamesa T., Okada T., Hashimoto K., Sakamoto K., Takashima M., Miyamoto T., Uchimura S., Hamamoto Y., Oka M. Sex-based molecular profiling of hepatitis C virus-related hepatocellular carcinoma. Int. J. Oncol. 2005, 26:673-678.
40. Thangavel C., Shapiro B.H. A molecular basis for the sexually dimorphic response to growth hormone. Endocrinology 2007, 148:2894-2903.
41. Thangavel C., Dworakowski W., Shapiro B.H. Inducibility of male-specific isoforms of cytochrome p450 by sex-dependent growth hormone profiles in hepatocyte cultures from male but not female rats. Drug Metab. Dispos. 2006, 34:410-419.
42. Wauthier V., Sugathan A., Meyer R.D., Dombkowski A.A., Waxman D.J. Intrinsic sex differences in the early growth hormone responsiveness of sex-specific genes in mouse liver. Mol. Endocrinol. 2010, 24:667-678.
43. Waxman D.J., Holloway M.G. Sex differences in the expression of hepatic drug metabolizing enzymes. Mol. Pharmacol. 2009, 76:215-228.
44. Waxman D.J., O'Connor C. Growth hormone regulation of sex-dependent liver gene expression. Mol. Endocrinol. 2006, 20:2613-2629.
45. Wiwi C.A., Gupte M., Waxman D.J. Sexually dimorphic P450 gene expression in liver-specific hepatocyte nuclear factor 4alpha-deficient mice. Mol. Endocrinol. 2004, 18:1975-1987.
46. Wong J.H., Dukes J., Levy R.E., Sos B., Mason S.E., Fong T.S., Weiss E.J. Sex differences in thrombosis in mice are mediated by sex-specific growth hormone secretion patterns. J. Clin. Invest. 2008, 118:2969-2978.
47. Wu Z., Chiang J.Y. Transcriptional regulation of human oxysterol 7 alpha-hydroxylase gene (CYP7B1) by Sp1. Gene 2001, 272:191-197.
48. Wu M.V., Manoli D.S., Fraser E.J., Coats J.K., Tollkuhn J., Honda S., Harada N., Shah N.M. Estrogen masculinizes neural pathways and sex-specific behaviors. Cell 2009, 139:61-72.
49. Yokomori N., Kobayashi R., Moore R., Sueyoshi T., Negishi M. A DNA methylation site in the male-specific P450 (Cyp 2d-9) promoter and binding of the heteromeric transcription factor GABP. Mol. Cell Biol. 1995, 15:5355-5362.
50. Yoshida Y., Hughes D.E., Rausa F.M., Kim I.M., Tan Y., Darlington G.J., Costa R.H. C/EBPalpha and HNF6 protein complex formation stimulates HNF6-dependent transcription by CBP coactivator recruitment in HepG2 cells. Hepatology 2006, 43:276-286.
51. Zhang Y., Klein K., Sugathan A., Nassery N., Dombkowski A., Zanger U.M., Waxman D.J. Transcriptional profiling of human liver identifies sex-biased genes associated with polygenic dyslipidemia and coronary artery disease. PLoS One 2011, 6:e23506.
52. Zhang Y., Laz E.V., Waxman D.J. Dynamic, sex-differential STAT5 and BCL6 binding to sex-biased, growth hormone-regulated genes in adult mouse liver. Mol. Cell Biol. 2012, 32:880-896.