Spatially compartmentalized phase regulation of a Ca2+-cAMP-PKA oscillatory circuit

Abstract

Signaling networks are spatiotemporally organized to sense diverse inputs, process information, and carry out specific cellular tasks. In β cells, Ca2+, cyclic adenosine monophosphate (cAMP), and Protein Kinase A (PKA) exist in an oscillatory circuit characterized by a high degree of feedback. Here, we describe a mode of regulation within this circuit involving a spatial dependence of the relative phase between cAMP, PKA, and Ca2+. We show that in mouse MIN6 β cells, nanodomain clustering of Ca2+-sensitive adenylyl cyclases (ACs) drives oscillations of local cAMP levels to be precisely in-phase with Ca2+ oscillations, whereas Ca2+-sensitive phosphodiesterases maintain out-of-phase oscillations outside of the nanodomain. Disruption of this precise phase relationship perturbs Ca2+ oscillations, suggesting the relative phase within an oscillatory circuit can encode specific functional information. This work unveils a novel mechanism of cAMP compartmentation utilized for localized tuning of an oscillatory circuit and has broad implications for the spatiotemporal regulation of signaling networks.

Document Details

Document Type
Pub Defense Publication
Publication Date
Nov 17, 2020
Source ID
10.7554/elife.55013

Entities

People

  • Brian L Ross
  • Brian Tenner
  • Christopher H Bohrer
  • Donya Ohadi
  • Eric C Greenwald
  • Jie Xiao
  • Jin Zhang
  • Michael Getz
  • Padmini Rangamani
  • Sohum Mehta

Organizations

  • Johns Hopkins University
  • National Institutes of Health
  • National Science Foundation
  • Office of Naval Research
  • United States Department of Defense
  • University of California, San Diego

Tags

Fields of Study

  • Biology

Readers

  • Atmospheric Science / Meteorology, specifically Wind Wave Turbulence.
  • Cellular and Molecular Pathways of Apoptosis.
  • Systems Analysis and Design