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

José M Guzmán,Yoji Yamamoto,Penny Swanson,J Adam Luckenbach,Cheng-Guang Liang

doi:10.1371/journal.pone.0114176

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.

Highlights

Oogenesis is the developmental process by which an oogonium becomes a fullygrown, mature, and fertilizable egg
We demonstrated that follicle-stimulating hormone (Fsh) regulates the in vitro expression of a unique suite of genes involved in a number of ovarian processes mostly unexplored in fishes, like cell survival, proliferation, differentiation and growth, tissue and extracellular matrix (ECM) remodeling
Since most of these genes likely participate in ovarian processes mostly unexplored in fishes, the functional categories in which they are classified in the present study should be considered as only a guide

Summary

Introduction

Oogenesis is the developmental process by which an oogonium becomes a fullygrown, mature, and fertilizable egg. Coho salmon (Oncorhynchus kisutch) is a semelparous species (i.e., spawns only once in its life and dies) that exhibits synchronous follicle development. During vitellogenesis, plasma Fsh continues to rise until just prior to final maturation, at which point Fsh levels decline and Lh levels surge leading up to ovulation [8, 9]. These findings suggest that Fsh plays an important function from at least the onset of the early secondary oocyte growth until the completion of vitellogenesis, and this supposition is supported by data in other species [10, 11, 12, 13]

Methods

Results

Conclusion