Dephosphorylation and inactivation of NPR2 guanylyl cyclase in granulosa cells contributes to the LH-induced decrease in cGMP that causes resumption of meiosis in rat oocytes

Development. 2014 Sep;141(18):3594-604. doi: 10.1242/dev.112219.

Abstract

In mammals, the meiotic cell cycle of oocytes starts during embryogenesis and then pauses. Much later, in preparation for fertilization, oocytes within preovulatory follicles resume meiosis in response to luteinizing hormone (LH). Before LH stimulation, the arrest is maintained by diffusion of cyclic (c)GMP into the oocyte from the surrounding granulosa cells, where it is produced by the guanylyl cyclase natriuretic peptide receptor 2 (NPR2). LH rapidly reduces the production of cGMP, but how this occurs is unknown. Here, using rat follicles, we show that within 10 min, LH signaling causes dephosphorylation and inactivation of NPR2 through a process that requires the activity of phosphoprotein phosphatase (PPP)-family members. The rapid dephosphorylation of NPR2 is accompanied by a rapid phosphorylation of the cGMP phosphodiesterase PDE5, an enzyme whose activity is increased upon phosphorylation. Later, levels of the NPR2 agonist C-type natriuretic peptide decrease in the follicle, and these sequential events contribute to the decrease in cGMP that causes meiosis to resume in the oocyte.

Keywords: Guanylyl cyclase; Luteinizing hormone; Meiosis; Natriuretic peptide receptor; Ovarian follicle; Phosphorylation.

Publication types

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

MeSH terms

  • Analysis of Variance
  • Animals
  • Blotting, Western
  • Cyclic GMP / metabolism*
  • Cyclic Nucleotide Phosphodiesterases, Type 5 / metabolism
  • Enzyme Activation
  • Enzyme-Linked Immunosorbent Assay
  • Female
  • Granulosa Cells / metabolism*
  • Immunoprecipitation
  • Luteinizing Hormone / metabolism*
  • Meiosis / physiology*
  • Natriuretic Peptide, C-Type / metabolism
  • Oocytes / physiology*
  • Ovarian Follicle / metabolism
  • Phosphoprotein Phosphatases / metabolism
  • Phosphorylation
  • Rats
  • Receptors, Atrial Natriuretic Factor / agonists
  • Receptors, Atrial Natriuretic Factor / metabolism*

Substances

  • Natriuretic Peptide, C-Type
  • Luteinizing Hormone
  • Phosphoprotein Phosphatases
  • Cyclic Nucleotide Phosphodiesterases, Type 5
  • Receptors, Atrial Natriuretic Factor
  • atrial natriuretic factor receptor B
  • Cyclic GMP