Maternal obesity is associated with ovarian inflammation and upregulation of early growth response factor 1

Am J Physiol Endocrinol Metab. 2016 Jul 1;311(1):E269-77. doi: 10.1152/ajpendo.00524.2015. Epub 2016 Jun 7.

Abstract

Obesity impairs reproductive functions through multiple mechanisms, possibly through disruption of ovarian function. We hypothesized that increased adiposity will lead to a proinflammatory gene signature and upregulation of Egr-1 protein in ovaries from obese (OB; n = 7) compared with lean (LN; n = 10) female Sprague-Dawley rats during the peri-implantation period at 4.5 days postcoitus (dpc). Obesity was induced by overfeeding (40% excess calories for 28 days) via total enteral nutrition prior to mating. OB dams had higher body weight (P < 0.001), greater fat mass (P < 0.001), and reduced lean mass (P < 0.05) and developed metabolic dysfunction with elevated serum lipids, insulin, leptin, and CCL2 (P < 0.05) compared with LN dams. Microarray analyses identified 284 differentially expressed genes between ovaries from LN vs. OB dams (±1.3 fold, P < 0.05). RT-qPCR confirmed a decrease in expression of glucose transporters GLUT4 and GLUT9 and elevation of proinflammatory genes, including CCL2, CXCL10, CXCL11, CCR2, CXCR1, and TNFα in ovaries from OB compared with LN (P < 0.05). Protein levels of PI3K and phosphorylated Akt were significantly decreased (P < 0.05), whereas nuclear levels of Egr-1 (P < 0.05) were increased in OB compared with LN ovaries. Moreover, Egr-1 was localized to granulosa cells, with the highest expression in cumulus cells of preovulatory follicles. mRNA expression of VCAN, AURKB, and PLAT (P < 0.05) correlated with %visceral fat weight (r = 0.51, -0.77, and -0.57, respectively, P ≤ 0.05), suggesting alterations in ovarian function with obesity. In summary, maternal obesity led to an upregulation of inflammatory genes and Egr-1 expression in peri-implantation ovarian tissue and a concurrent downregulation of GLUTs and Akt and PI3K protein levels.

Keywords: early growth response factor 1; gene expression; inflammation; obesity; reproduction.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Aurora Kinase B / genetics
  • Case-Control Studies
  • Chemokine CCL2 / genetics
  • Chemokine CXCL10 / genetics
  • Chemokine CXCL11 / genetics
  • Early Growth Response Protein 1 / metabolism*
  • Female
  • Glucose Transporter Type 4 / genetics
  • Granulosa Cells / metabolism
  • Immunoblotting
  • Immunohistochemistry
  • Inflammation / genetics
  • Inflammation / metabolism
  • Monosaccharide Transport Proteins / genetics
  • Obesity / genetics*
  • Obesity / metabolism
  • Ovary / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphoproteins / metabolism
  • Pregnancy
  • Pregnancy Complications / genetics*
  • Pregnancy Complications / metabolism
  • Proto-Oncogene Proteins c-akt / metabolism
  • RNA, Messenger / metabolism
  • Rats, Sprague-Dawley
  • Real-Time Polymerase Chain Reaction
  • Receptors, CCR2 / genetics
  • Receptors, Interleukin-8A / genetics
  • Reverse Transcriptase Polymerase Chain Reaction
  • Tissue Array Analysis
  • Tissue Plasminogen Activator / genetics
  • Transcriptome
  • Tumor Necrosis Factor-alpha / genetics
  • Up-Regulation
  • Versicans / genetics

Substances

  • Ccl2 protein, rat
  • Ccr2 protein, rat
  • Chemokine CCL2
  • Chemokine CXCL10
  • Chemokine CXCL11
  • Cxcl10 protein, rat
  • Cxcl11 protein, rat
  • Early Growth Response Protein 1
  • Egr1 protein, rat
  • GLUT6 protein, rat
  • Glucose Transporter Type 4
  • Monosaccharide Transport Proteins
  • Phosphoproteins
  • RNA, Messenger
  • Receptors, CCR2
  • Receptors, Interleukin-8A
  • Slc2a4 protein, rat
  • Tumor Necrosis Factor-alpha
  • Versicans
  • Phosphatidylinositol 3-Kinases
  • Aurkb protein, rat
  • Aurora Kinase B
  • Proto-Oncogene Proteins c-akt
  • Tissue Plasminogen Activator