Hormone-induced expression of tumor necrosis factor alpha-converting enzyme/A disintegrin and metalloprotease-17 impacts porcine cumulus cell oocyte complex expansion and meiotic maturation via ligand activation of the epidermal growth factor receptor

Endocrinology. 2007 Dec;148(12):6164-75. doi: 10.1210/en.2007-0195. Epub 2007 Sep 27.

Abstract

The epidermal growth factor (EGF)-like growth factors, amphiregulin (AREG) and epiregulin (EREG), are expressed in murine cumulus oocyte complexes (COCs) where they impact the function of cumulus cells and oocyte maturation during LH-mediated ovulation. Because TNFalpha-converting enzyme (TACE)/a disintegrin and metalloprotease-17 (ADAM17) is essential for ectodomain shedding of AREG and EREG from the surface of other cell types, the expression and function of TACE/ADAM17 was analyzed in a porcine COC culture system in which FSH- and LH-mediated expansion and oocyte meiotic maturation have been well characterized and shown to occur between 20 and 40 h. In this model, Areg, Ereg, and Tace/Adam17 mRNAs increased significantly with maximal levels observed between 5 and 20 h of culture with FSH plus LH. TACE/ADAM17 protein and protease activity were up-regulated markedly at 10 h and maintained to 40 h. Treatment of COCs with the TACE/ADAM17-selective inhibitor TNFalpha-processing inhibitor-2 (TAPI-2) significantly suppressed in a time-dependent manner downstream targets of EGF receptor activation such as ERK1/2 phosphorylation, Ptgs2, Has2, and Tnfaip6 mRNA expression, hormone-induced COC expansion, and meiotic maturation of the oocytes. Addition of EGF to COCs cultured in the presence of FSH/LH reversed the inhibitory effects of TAPI-2 on these ovulation-related processes. Gonadotropin-induced phosphorylation of ERK1/2 was also inhibited in rat granulosa cells treated with TAPI-2 or after transfection with Tace/Adam17 small interfering RNA. Induced expression of Tnfaip6 mRNA was also reduced by Tace/Adam17 small interfering RNA. Thus, TACE/ADAM17 is induced and the activity is involved in porcine COC expansion as well as oocyte meiotic maturation through the activation of EGF receptor in cumulus cells.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADAM Proteins / genetics
  • ADAM Proteins / metabolism*
  • ADAM17 Protein
  • Amphiregulin
  • Animals
  • Blotting, Western
  • Cells, Cultured
  • Cumulus Cells / cytology
  • Cumulus Cells / drug effects
  • Cumulus Cells / metabolism*
  • EGF Family of Proteins
  • Epidermal Growth Factor / genetics
  • Epidermal Growth Factor / metabolism
  • Epiregulin
  • ErbB Receptors / genetics
  • ErbB Receptors / metabolism*
  • Female
  • Flavonoids / pharmacology
  • Follicle Stimulating Hormone / pharmacology
  • Gene Expression / drug effects
  • Glycoproteins / genetics
  • Glycoproteins / metabolism
  • Humans
  • Intercellular Signaling Peptides and Proteins / genetics
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Luteinizing Hormone / pharmacology
  • Mitogen-Activated Protein Kinase 1 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Oocytes / cytology
  • Oocytes / drug effects
  • Oocytes / metabolism*
  • Phosphorylation / drug effects
  • Quinazolines
  • RNA, Small Interfering / genetics
  • Rats
  • Rats, Wistar
  • Reverse Transcriptase Polymerase Chain Reaction
  • Swine
  • Transfection
  • Tyrphostins / pharmacology

Substances

  • AREG protein, human
  • Amphiregulin
  • Areg protein, rat
  • EGF Family of Proteins
  • EREG protein, human
  • Epiregulin
  • Ereg protein, rat
  • Flavonoids
  • Glycoproteins
  • Intercellular Signaling Peptides and Proteins
  • Quinazolines
  • RNA, Small Interfering
  • Tyrphostins
  • RTKI cpd
  • Epidermal Growth Factor
  • Luteinizing Hormone
  • Follicle Stimulating Hormone
  • ErbB Receptors
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • ADAM Proteins
  • ADAM17 Protein
  • ADAM17 protein, human
  • Adam17 protein, rat
  • 2-(2-amino-3-methoxyphenyl)-4H-1-benzopyran-4-one