Induction of sperm hypermotility through membrane progestin receptor alpha (mPRα): A teleost model of rapid, multifaceted, nongenomic progestin signaling

Wenxian Tan; Yefei Pang; Christopher Tubbs; Peter Thomas

doi:10.1016/j.ygcen.2018.12.002

Induction of sperm hypermotility through membrane progestin receptor alpha (mPRα): A teleost model of rapid, multifaceted, nongenomic progestin signaling

Gen Comp Endocrinol. 2019 Aug 1:279:60-66. doi: 10.1016/j.ygcen.2018.12.002. Epub 2018 Dec 7.

Authors

Wenxian Tan¹, Yefei Pang², Christopher Tubbs³, Peter Thomas⁴

Affiliations

¹ The University of Texas at Austin Marine Science Institute, 750 Channel View Drive, Port Aransas, TX 78373, United States; Huston-Tillotson University, 900 Chicon Street, Austin, TX 78702, United States.
² The University of Texas at Austin Marine Science Institute, 750 Channel View Drive, Port Aransas, TX 78373, United States.
³ The University of Texas at Austin Marine Science Institute, 750 Channel View Drive, Port Aransas, TX 78373, United States; San Diego Zoo Global, Institute for Conservation Research, 15600 San Pasqual Valley Road, Escondido, CA 92027, United States.
⁴ The University of Texas at Austin Marine Science Institute, 750 Channel View Drive, Port Aransas, TX 78373, United States. Electronic address: peter.thomas@utexas.edu.

PMID: 30529310
DOI: 10.1016/j.ygcen.2018.12.002

Abstract

Rapid progestin effects on sperm physiology have been described in a variety of vertebrate species. Here, we briefly review the signaling pathways mediating rapid progestin induction of sperm hypermotility and increased fertility in two teleost species, Atlantic croaker and southern flounder. Acute in vitro treatment of teleost sperm with the progestin hormone, 20β-S, causes activation of progestin membrane receptor alpha (mPRα, or Paqr7) coupled to a stimulatory olfactory G protein (G_olf), resulting in increased cAMP and calcium concentrations and hypermotility upon activation in a hyperosmotic medium. Pharmacological tools were used to investigate the involvement of mPRα and several intracellular signaling pathways in the hypermotility response. Evidence was obtained using the specific mPRα agonist, Org OD 02-0, that this progestin action is mediated through mPRα and not through the nuclear PR. The results indicate that progestins induce hypermotility through activation of a membrane adenylyl cyclase (Acy)/cAMP pathway, an epidermal growth factor receptor (Egfr)/Mapkinase pathway, and a Pi3kinase/Akt/phosphodiesterase (Pde) pathway which result in increased sperm calcium concentrations within 10 s. The finding that inhibition of any one of these pathways is sufficient to prevent hypermotility along with the calcium increase suggests that activation of all of them and the associated calcium increase are required for the progestin hypermotility response. On the basis of these findings a model of progestin induction of sperm hypermotility in teleosts is proposed. As teleosts lack CatSper, the model described here is a non-CatSper mediated one and may therefore be applicable to a wide variety of nonmammalian vertebrates.

Keywords: Adenylyl cyclase; Atlantic croaker; Egfr; Epidermal growth factor receptor; Mapkinase; Membrane progestin receptor alpha; Nongenomic steroid signaling; Olfactory G protein; Pde; Pi3k; Rapid progestin action; Southern flounder; Sperm hypermotility; cAMP; mPRα.

Publication types

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

MeSH terms

Animals
Fishes / metabolism*
Male
Models, Animal
Progestins / metabolism*
Receptors, Progesterone / metabolism*
Signal Transduction* / drug effects
Sperm Motility* / drug effects

Substances

Progestins
Receptors, Progesterone