Expression profiles of Fsh-regulated ovarian genes during oogenesis in coho salmon

PLoS One. 2014 Dec 8;9(12):e114176. doi: 10.1371/journal.pone.0114176. eCollection 2014.

Abstract

The function of follicle-stimulating hormone (Fsh) during oogenesis in fishes is poorly understood. Using coho salmon as a fish model, we recently identified a suite of genes regulated by Fsh in vitro and involved in ovarian processes mostly unexplored in fishes, like cell proliferation, differentiation, survival or extracellular matrix (ECM) remodeling. To better understand the role of these Fsh-regulated genes during oocyte growth in fishes, we characterized their mRNA levels at discrete stages of the ovarian development in coho salmon. While most of the transcripts were expressed at low levels during primary growth (perinucleolus stage), high expression of genes associated with cell proliferation (pim1, pcna, and mcm4) and survival (ddit4l) was found in follicles at this stage. The transition to secondary oocyte growth (cortical alveolus and lipid droplet stage ovarian follicles) was characterized by a marked increase in the expression of genes related to cell survival (clu1, clu2 and ivns1abpa). Expression of genes associated with cell differentiation and growth (wt2l and adh8l), growth factor signaling (inha), steroidogenesis (cyp19a1a) and the ECM (col1a1, col1a2 and dcn) peaked in vitellogenic follicles, showing a strong and positive correlation with transcripts for fshr. Other genes regulated by Fsh and associated with ECM function (ctgf, wapl and fn1) and growth factor signaling (bmp16 and smad5l) peaked in maturing follicles, along with increases in steroidogenesis-related gene transcripts. In conclusion, ovarian genes regulated by Fsh showed marked differences in their expression patterns during oogenesis in coho salmon. Our results suggest that Fsh regulates different ovarian processes at specific stages of development, likely through interaction with other intra- or extra-ovarian factors.

Publication types

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

MeSH terms

  • Animals
  • Databases, Genetic
  • Female
  • Follicle Stimulating Hormone / metabolism*
  • Gene Expression Profiling
  • Oncorhynchus kisutch / genetics*
  • Oncorhynchus kisutch / metabolism*
  • Oocytes / metabolism*
  • Oogenesis / genetics*
  • Receptors, FSH / genetics
  • Receptors, FSH / metabolism
  • Transcriptome*

Substances

  • Receptors, FSH
  • Follicle Stimulating Hormone

Grants and funding

This research was partially funded by NOAA Fisheries and by National Research Initiative Competitive Grant no. 2007-35203-18088 from the USDA National Institute of Food and Agriculture to PS, and postdoctoral fellowships from the Fundación Alfonso Martín Escudero (Spain) and The National Academy of Sciences (US) to JMG. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.