Lipid profiling and transcriptomic analysis reveals a functional interplay between estradiol and growth hormone in liver

PLoS One. 2014 May 9;9(5):e96305. doi: 10.1371/journal.pone.0096305. eCollection 2014.

Abstract

17β-estradiol (E2) may interfere with endocrine, metabolic, and gender-differentiated functions in liver in both females and males. Indirect mechanisms play a crucial role because of the E2 influence on the pituitary GH secretion and the GHR-JAK2-STAT5 signaling pathway in the target tissues. E2, through its interaction with the estrogen receptor, exerts direct effects on liver. Hypothyroidism also affects endocrine and metabolic functions of the liver, rendering a metabolic phenotype with features that mimic deficiencies in E2 or GH. In this work, we combined the lipid and transcriptomic analysis to obtain comprehensive information on the molecular mechanisms of E2 effects, alone and in combination with GH, to regulate liver functions in males. We used the adult hypothyroid-orchidectomized rat model to minimize the influence of internal hormones on E2 treatment and to explore its role in male-differentiated functions. E2 influenced genes involved in metabolism of lipids and endo-xenobiotics, and the GH-regulated endocrine, metabolic, immune, and male-specific responses. E2 induced a female-pattern of gene expression and inhibited GH-regulated STAT5b targeted genes. E2 did not prevent the inhibitory effects of GH on urea and amino acid metabolism-related genes. The combination of E2 and GH decreased transcriptional immune responses. E2 decreased the hepatic content of saturated fatty acids and induced a transcriptional program that seems to be mediated by the activation of PPARα. In contrast, GH inhibited fatty acid oxidation. Both E2 and GH replacements reduced hepatic CHO levels and increased the formation of cholesterol esters and triacylglycerols. Notably, the hepatic lipid profiles were endowed with singular fingerprints that may be used to segregate the effects of different hormonal replacements. In summary, we provide in vivo evidence that E2 has a significant impact on lipid content and transcriptome in male liver and that E2 exerts a marked influence on GH physiology, with implications in human therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Estradiol / pharmacology*
  • Estrogens / pharmacology
  • Fatty Acids / analysis
  • Gene Expression Profiling
  • Gene Expression Regulation / drug effects
  • Gene Regulatory Networks / drug effects
  • Growth Hormone / pharmacology*
  • Hypothyroidism / genetics
  • Lipid Metabolism / genetics*
  • Lipids / analysis
  • Lipids / blood
  • Liver / drug effects*
  • Liver / metabolism
  • Male
  • Models, Genetic
  • Oligonucleotide Array Sequence Analysis
  • Orchiectomy
  • Rats, Sprague-Dawley
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Transcriptome / genetics*

Substances

  • Estrogens
  • Fatty Acids
  • Lipids
  • Estradiol
  • Growth Hormone

Associated data

  • GEO/GSE50014

Grants and funding

The Spanish Ministry of Science and Innovation with the funding of European Regional Development Fund-European Social Fund supported this research by grants-in-aid to LF-P (SAF2003-02117; SAF2006-07824) and MD (SAF2010- 22114-C02-01). LF-P was also supported by grants-in-aid from ACIISI (PI2007/033; PI2010/0110) and Alfredo Martin-Reyes Foundation (Arehucas)-FICIC. D.I-G and A.F-M are supported by the Danish Council for Independent Research and the Novo Nordisk Foundation. R.S-F was recipient of a predoctoral fellowship from the MCYT (SAF2003-02117), ULPGC-ACIISI (ULPAPD-08/01-4), and ACIISI-FSE (SE ­-10/13). M.M-G is a recipient of predoctoral fellowship from ULPGC-MEC (AP2001-3499). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.