Insulin-like growth factor-binding protein (IGFBP)-1, -2, -3, -4, -5, and -6 and IGFBP-related protein 1 during rainbow trout postvitellogenesis and oocyte maturation: molecular characterization, expression profiles, and hormonal regulation

Endocrinology. 2006 May;147(5):2399-410. doi: 10.1210/en.2005-1570. Epub 2006 Jan 26.

Abstract

In the present study we report the full coding sequence of rainbow trout IGF-binding protein-1 (IGFBP1), -2, -3, -5, and -6 and IGFBP-related protein-1 (IGFBP-rP1) mRNAs as well as the partial coding sequence of IGFBP-4 mRNA. To our knowledge, this is the first report of IGFBP4, IGFBP6, and IGFBP-rP1 in a nonmammalian species. The tissue distribution of all mRNAs was studied, and the ovarian expression profiles of IGFBP2 to -6 and IGFBP-rP1 between late vitellogenesis and oocyte maturation were characterized. In addition, in vitro hormonal regulation by the maturation-inducing steroid 17,20beta-dihydroxy-4-pregnen-3-one (17,20betaP), gonadotropin, and estradiol were studied. We observed that besides IGFBP1, which was only found in liver, IGFBP2 to -6 and IGFPB-rP1 were expressed in the preovulatory ovary. IGFBP3 was also detected in liver, trunk, kidney, skin, and gills, whereas IGFBP2 to -6 and IGFBP-rP1 exhibited a wider tissue distribution. In the preovulatory ovary, IGFBP3 was strongly down-regulated during the postvitellogenesis period, whereas IGFBP5 exhibited a limited up-regulation. In addition, IGFBP6 and IGFBP-rP1 were up-regulated during oocyte maturation. Hormonal regulation data indicated that all ovarian IGFBPs and IGFBP-rP1 transcripts are regulated under gonadotropic stimulation at a concentration that induced 100% oocyte maturation. In addition, IGFBP2 to -5 transcripts are regulated by 17,20betaP and estradiol. Together, our observations strongly suggest that during final oocyte maturation, a down-regulation of IGFBP3, -4, and -5 occurs in the oocyte in response to gonadotropic and 17,20betaP (IGFBP3 and -5) stimulation, whereas an up-regulation of IGFBP2 and -6 occurs in follicular layers or extrafollicular tissue in response to gonadotropic stimulation.

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Cloning, Molecular
  • DNA, Complementary / metabolism
  • Estradiol / metabolism
  • Expressed Sequence Tags
  • Female
  • Gene Expression Regulation, Developmental*
  • Hormones / metabolism
  • Insulin-Like Growth Factor Binding Protein 1 / biosynthesis*
  • Insulin-Like Growth Factor Binding Protein 2 / biosynthesis*
  • Insulin-Like Growth Factor Binding Protein 3 / biosynthesis*
  • Insulin-Like Growth Factor Binding Protein 4 / biosynthesis*
  • Insulin-Like Growth Factor Binding Protein 5 / biosynthesis*
  • Insulin-Like Growth Factor Binding Protein 6 / biosynthesis*
  • Insulin-Like Growth Factor Binding Proteins / biosynthesis*
  • Liver / metabolism
  • Male
  • Molecular Sequence Data
  • Oncorhynchus mykiss
  • Oocytes / metabolism*
  • Ovary / metabolism
  • Phylogeny
  • RNA / metabolism
  • RNA, Messenger / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sequence Homology, Amino Acid
  • Tissue Distribution
  • Vitellogenesis*

Substances

  • DNA, Complementary
  • Hormones
  • Insulin-Like Growth Factor Binding Protein 1
  • Insulin-Like Growth Factor Binding Protein 2
  • Insulin-Like Growth Factor Binding Protein 3
  • Insulin-Like Growth Factor Binding Protein 4
  • Insulin-Like Growth Factor Binding Protein 5
  • Insulin-Like Growth Factor Binding Protein 6
  • Insulin-Like Growth Factor Binding Proteins
  • RNA, Messenger
  • insulin-like growth factor binding protein-related protein 1
  • Estradiol
  • RNA