Dynamic, Sex-Differential STAT5 and BCL6 Binding to Sex-Biased, Growth Hormone-Regulated Genes in Adult Mouse Liver

REFERENCES

• Ayonrinde OT, et al. 2011. Gender-specific differences in adipose distribution and adipocytokines influence adolescent nonalcoholic fatty liver disease. Hepatology 53:800–809.
   PubMed Web of Science ®Google Scholar
• Baik M, Yu JH, Hennighausen L. 2011. Growth hormone-STAT5 regulation of growth, hepatocellular carcinoma, and liver metabolism. Ann. N. Y. Acad. Sci. 1229:29–37.
   PubMed Web of Science ®Google Scholar
• Bannister AJ, Kouzarides T. 2011. Regulation of chromatin by histone modifications. Cell Res. 21:381–395.
   PubMed Web of Science ®Google Scholar
• Bhadhprasit W, Sakuma T, Kawasaki Y, Nemoto N. 2011. Hepatocyte nuclear factor 4α regulates expression of the mouse female-specific Cyp3a41 gene in the liver. Drug Metab. Dispos 39:490–497.
   PubMedGoogle Scholar
• Chang CC, Ye BH, Chaganti RS, Dalla-Favera R. 1996. BCL-6, a POZ/zinc-finger protein, is a sequence-specific transcriptional repressor. Proc. Natl. Acad. Sci. U. S. A. 93:6947–6952.
   PubMed Web of Science ®Google Scholar
• Chen Y, et al. 2009. Computational and functional analysis of growth hormone (GH)-regulated genes identifies the transcriptional repressor B-cell lymphoma 6 (Bc16) as a participant in GH-regulated transcription. Endocrinology 150:3645–3654.
   PubMed Web of Science ®Google Scholar
• Chia DJ, Rotwein P. 2010. Defining the epigenetic actions of growth hormone: acute chromatin changes accompany GH-activated gene transcription. Mol. Endocrinol. 24:2038–2049.
   PubMedGoogle Scholar
• Chia DJ, Varco-Merth B, Rotwein P. 2010. Dispersed chromosomal Stat5b-binding elements mediate growth hormone-activated insulin-like growth factor-I gene transcription. J. Biol. Chem. 285:17636–17647.
   PubMedGoogle Scholar
• Choi HK, Waxman DJ. 1999. Growth hormone, but not prolactin, maintains, low-level activation of STAT5a and STAT5b in female rat liver. Endocrinology 140:5126–5135.
   PubMedGoogle Scholar
• Choi HK, Waxman DJ. 2000. Plasma growth hormone pulse activation of hepatic JAK-STAT5 signaling: developmental regulation and role in male-specific liver gene expression. Endocrinology 141:3245–3255.
   PubMed Web of Science ®Google Scholar
• Clodfelter KH, et al. 2006. 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.
   PubMedGoogle Scholar
• Clodfelter KH, et al. 2007. Role of STAT5a in regulation of sex-specific gene expression in female but not male mouse liver revealed by microarray analysis. Physiol. Genomics 31:63–74.
   PubMed Web of Science ®Google Scholar
• Davey HW, et al. 2001. STAT5b is required for GH-induced liver IGF-I gene expression. Endocrinology 142:3836–3841.
   PubMed Web of Science ®Google Scholar
• Delesque-Touchard N, Park SH, Waxman DJ. 2000. Synergistic action of hepatocyte nuclear factors 3 and 6 on CYP2C12 gene expression and suppression by growth hormone-activated STAT5b. Proposed model for female specific expression of CYP2C12 in adult rat liver. J. Biol. Chem. 275:34173–34182.
   PubMed Web of Science ®Google Scholar
• Dent AL, Shaffer AL, Yu X, Allman D, Staudt LM. 1997. Control of inflammation, cytokine expression, and germinal center formation by BCL-6. Science 276:589–592.
   PubMed Web of Science ®Google Scholar
• Diehl SA, et al. 2008. STAT3-mediated up-regulation of BLIMP1 is coordinated with BCL6 down-regulation to control human plasma cell differentiation. J. Immunol. 180:4805–4815.
   PubMed Web of Science ®Google Scholar
• Eleswarapu S, Gu Z, Jiang H. 2008. Growth hormone regulation of insulin-like growth factor-I gene expression may be mediated by multiple distal signal transducer and activator of transcription 5 binding sites. Endocrinology 149:2230–2240.
   PubMedGoogle Scholar
• Endo M, Takahashi Y, Sasaki Y, Saito T, Kamataki T. 2005. Novel gender-related regulation of CYP2C12 gene expression in rats. Mol. Endocrinol. 19:1181–1190.
   PubMed Web of Science ®Google Scholar
• Franconi F, Brunelleschi S, Steardo L, Cuomo V. 2007. Gender differences in drug responses. Pharmacol. Res. 55:81–95.
   PubMed Web of Science ®Google Scholar
• Gardmo C, Mode A. 2006. In vivo transfection of rat liver discloses binding sites conveying GH-dependent and female-specific gene expression. J. Mol. Endocrinol. 37:433–441.
   PubMed Web of Science ®Google Scholar
• Gingras H, Cases O, Krasilnikova M, Berube G, Nepveu A. 2005. Biochemical characterization of the mammalian Cux2 protein. Gene 344:273–285.
   PubMedGoogle Scholar
• Gorski K, Carneiro M, Schibler U. 1986. Tissue-specific in vitro transcription from the mouse albumin promoter. Cell 47:767–776.
   PubMed Web of Science ®Google Scholar
• Harris MB, Mostecki J, Rothman PB. 2005. Repression of an interleukin-4-responsive promoter requires cooperative BCL-6 function. J. Biol. Chem. 280:13114–13121.
   PubMedGoogle Scholar
• Hartatik T, et al. 2001. Binding of BAZF and Bc16 to STAT6-binding DNA sequences. Biochem. Biophys. Res. Commun. 284:26–32.
   PubMedGoogle Scholar
• Hennighausen L, Robinson GW. 2008. Interpretation of cytokine signaling through the transcription factors STAT5A and STAT5B. Genes Dev. 22:711–721.
   PubMed Web of Science ®Google Scholar
• Holloway MG, et al. 2007. Loss of sexually dimorphic liver gene expression upon hepatocyte-specific deletion of Stat5a-Stat5b locus. Endocrinology 148:1977–1986.
   PubMed Web of Science ®Google Scholar
• Holloway MG, Laz EV, Waxman DJ. 2006. Codependence of growth hormone-responsive, sexually dimorphic hepatic gene expression on signal transducer and activator of transcription 5b and hepatic nuclear factor 4α. Mol. Endocrinol. 20:647–660.
   PubMed Web of Science ®Google Scholar
• Holloway MG, Miles GD, Dombkowski AA, Waxman DJ. 2008. Liver-specific hepatocyte nuclear factor-4α deficiency: greater impact on gene expression in male than in female mouse liver. Mol. Endocrinol. 22:1274–1286.
   PubMed Web of Science ®Google Scholar
• Jansson JO, Eden S, Isaksson O. 1985. Sexual dimorphism in the control of growth hormone secretion. Endocr. Rev. 6:128–150.
   PubMed Web of Science ®Google Scholar
• Ji H, et al. 2008. An integrated software system for analyzing ChIP-chip and ChIP-seq data. Nat. Biotechnol. 26:1293–1300.
   PubMed Web of Science ®Google Scholar
• Kharroubi I, et al. 2006. BCL-6: a possible missing link for anti-inflammatory PPAR-delta signalling in pancreatic beta cells. Diabetologia 49:2350–2358.
   PubMed Web of Science ®Google Scholar
• Kumagai T, et al. 1999. The proto-oncogene Bc16 inhibits apoptotic cell death in differentiation-induced mouse myogenic cells. Oncogene 18:467–475.
   PubMedGoogle Scholar
• Lahuna O, et al. 1997. Expression of hepatocyte nuclear factor 6 in rat liver is sex-dependent and regulated by growth hormone. Proc. Natl. Acad. Sci. U. S. A. 94:12309–12313.
   PubMed Web of Science ®Google Scholar
• Lanning NJ, Carter-Su C. 2006. Recent advances in growth hormone signaling. Rev. Endocr. Metab. Disord. 7:225–235.
   PubMed Web of Science ®Google Scholar
• Laz EV, Holloway MG, Chen CS, Waxman DJ. 2007. Characterization of three growth hormone-responsive transcription factors preferentially expressed in adult female liver. Endocrinology 148:3327–3337.
   PubMed Web of Science ®Google Scholar
• Laz EV, Sugathan A, Waxman DJ. 2009. Dynamic in vivo binding of STAT5 to growth hormone-regulated genes in intact rat liver. Sex-specific binding at low- but not high-affinity STAT5 sites. Mol. Endocrinol. 23:1242–1254.
   PubMedGoogle Scholar
• Lemercier C, et al. 2002. Class II histone deacetylases are directly recruited by BCL6 transcriptional repressor. J. Biol. Chem. 277:22045–22052.
   PubMed Web of Science ®Google Scholar
• Lichanska AM, Waters MJ. 2008. How growth hormone controls growth, obesity and sexual dimorphism. Trends Genet. 24:41–47.
   PubMed Web of Science ®Google Scholar
• Ling G, Sugathan A, Mazor T, Fraenkel E, Waxman DJ. 2010. Unbiased, genome-wide in vivo mapping of transcriptional regulatory elements reveals sex differences in chromatin structure associated with sex-specific liver gene expression. Mol. Cell. Biol. 30:5531–5544.
   PubMed Web of Science ®Google Scholar
• Logarajah S, et al. 2003. BCL-6 is expressed in breast cancer and prevents mammary epithelial differentiation. Oncogene 22:5572–5578.
   PubMedGoogle Scholar
• Macisaac KD, et al. 2006. A hypothesis-based approach for identifying the binding specificity of regulatory proteins from chromatin immunoprecipitation data. Bioinformatics 22:423–429.
   PubMedGoogle Scholar
• Margueron R, Reinberg D. 2011. The Polycomb complex PRC2 and its mark in life. Nature 469:343–349.
   PubMed Web of Science ®Google Scholar
• Meyer RD, Laz EV, Su T, Waxman DJ. 2009. Male-specific hepatic Bcl6: growth hormone-induced block of transcription elongation in females and binding to target genes inversely coordinated with STAT5. Mol. Endocrinol. 23:1914–1926.
   PubMedGoogle Scholar
• Mode A, Gustafsson JA. 2006. Sex and the liver: a journey through five decades. Drug Metab. Rev. 38:197–207.
   PubMed Web of Science ®Google Scholar
• Ono M, et al. 2007. Signal transducer and activator of transcription (Stat) 5b-mediated inhibition of insulin-like growth factor binding protein-1 gene transcription: a mechanism for repression of gene expression by growth hormone. Mol. Endocrinol. 21:1443–1457.
   PubMedGoogle Scholar
• Park SH, Wiwi CA, Waxman DJ. 2006. Signalling cross-talk between hepatocyte nuclear factor 4α and growth-hormone-activated STAT5b. Biochem. J. 397:159–168.
   PubMedGoogle Scholar
• Pasqualucci L, et al. 2011. Inactivating mutations of acetyltransferase genes in B-cell lymphoma. Nature 471:189–195.
   PubMed Web of Science ®Google Scholar
• Rando G, Wahli W. 2011. Sex differences in nuclear receptor-regulated liver metabolic pathways. Biochim. Biophys. Acta 1812:964–973.
   PubMed Web of Science ®Google Scholar
• Ravaux L, et al. 2007. Inhibition of interleukin-1β-induced group IIA secretory phospholipase A2 expression by peroxisome proliferator-activated receptors (PPARs) in rat vascular smooth muscle cells: cooperation between PPARβ and the proto-oncogene BCL-6. Mol. Cell. Biol. 27:8374–8387.
   PubMedGoogle Scholar
• Scandlyn MJ, Stuart EC, Rosengren RJ. 2008. Sex-specific differences in CYP450 isoforms in humans. Expert Opin. Drug Metab. Toxicol. 4:413–424.
   PubMed Web of Science ®Google Scholar
• Schmidt D, et al. 2010. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 328:1036–1040.
   PubMedGoogle Scholar
• Schwartz JB. 2007. The current state of knowledge on age, sex, and their interactions on clinical pharmacology. Clin. Pharmacol. Ther. 82:87–96.
   PubMed Web of Science ®Google Scholar
• Seyfert VL, Allman D, He Y, Staudt LM. 1996. Transcriptional repression by the proto-oncogene BCL-6. Oncogene 12:2331–2342.
   PubMed Web of Science ®Google Scholar
• Shapiro BH, Agrawal AK, Pampori NA. 1995. Gender differences in drug metabolism regulated by growth hormone. Int. J. Biochem. Cell Biol. 27:9–20.
   PubMed Web of Science ®Google Scholar
• Su WL, et al. 2008. Exon and junction microarrays detect widespread mouse strain- and sex-bias expression differences. BMC Genomics 9:273.
   PubMedGoogle Scholar
• Subramanian A, et al. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U. S. A. 102:15545–15550.
   PubMed Web of Science ®Google Scholar
• Sugathan A, Laz EV, Rampersaud A, Waxman DJ. Role of histone-3 lysine 27 trimethylation (K27-me3) in repression of female-specific, growth hormone-regulated genes in male mouse liver. Endocr. Rev. 32:P2–P330.
   Google Scholar
• Takemoto N, et al. 2005. Sex-based molecular profiling of hepatitis C virus-related hepatocellular carcinoma. Int. J. Oncol. 26:673–678.
   PubMedGoogle Scholar
• Tannenbaum GS, Choi HK, Gurd W, Waxman DJ. 2001. Temporal relationship between the sexually dimorphic spontaneous GH secretory profiles and hepatic STAT5 activity. Endocrinology 142:4599–4606.
   PubMed Web of Science ®Google Scholar
• Vidal OM, et al. 2007. In vivo transcript profiling and phylogenetic analysis identifies suppressor of cytokine signaling 2 as a direct signal transducer and activator of transcription 5b target in liver. Mol. Endocrinol. 21:293–311.
   PubMedGoogle Scholar
• Wauthier V, Sugathan A, Meyer RD, Dombkowski AA, Waxman DJ. 2010. Intrinsic sex differences in the early growth hormone responsiveness of sex-specific genes in mouse liver. Mol. Endocrinol. 24:667–678.
   PubMedGoogle Scholar
• Wauthier V, Waxman DJ. 2008. Sex-specific early growth hormone response genes in rat liver. Mol. Endocrinol. 22:1962–1974.
   PubMedGoogle Scholar
• Waxman DJ, Holloway MG. 2009. Sex differences in the expression of hepatic drug metabolizing enzymes. Mol. Pharmacol. 76:215–228.
   PubMed Web of Science ®Google Scholar
• Waxman DJ, Pampori NA, Ram PA, Agrawal AK, Shapiro BH. 1991. Interpulse interval in circulating growth hormone patterns regulates sexually dimorphic expression of hepatic cytochrome P450. Proc. Natl. Acad. Sci. U. S. A. 88:6868–6872.
   PubMed Web of Science ®Google Scholar
• Waxman DJ, Ram PA, Park SH, Choi HK. 1995. Intermittent plasma growth hormone triggers tyrosine phosphorylation and nuclear translocation of a liver-expressed, Stat 5-related DNA binding protein. Proposed role as an intracellular regulator of male-specific liver gene transcription. J. Biol. Chem. 270:13262–13270.
   PubMed Web of Science ®Google Scholar
• Xu J, et al. 2011. Exploring endocrine GH pattern in mice using rank plot analysis and random blood samples. J. Endocrinol. 208:119–129.
   PubMed Web of Science ®Google Scholar
• Yang X, et al. 2006. Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res. 16:995–1004.
   PubMed Web of Science ®Google Scholar
• Zanger UM, Turpeinen M, Klein K, Schwab M. 2008. Functional pharmacogenetics/genomics of human cytochromes P450 involved in drug biotransformation. Anal. Bioanal Chem. 392:1093–1108.
   PubMed Web of Science ®Google Scholar
• Zhang Y, et al. 2011. Transcriptional profiling of human liver identifies sex-biased genes associated with polygenic dyslipidemia and coronary artery disease. PLoS One 6:e23506.
   PubMed Web of Science ®Google Scholar
• Zhang Y, et al. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9:R137.
   PubMed Web of Science ®Google Scholar
• Zhou YC, Waxman DJ. 1999. STAT5b down-regulates peroxisome proliferator-activated receptor alpha transcription by inhibition of ligand-independent activation function region-1 trans-activation domain. J. Biol. Chem. 274:29874–29882.
   PubMed Web of Science ®Google Scholar