IP3 Receptor Activity Is Differentially Regulated in Endoplasmic Reticulum Subdomains during Oocyte Maturation

Abstract

SummaryFertilization competency results from hormone-induced remodeling of oocytes into eggs. The signaling pathways that effect this change exemplify bistability, where brief hormone exposure irrevocably switches cell fate. In Xenopus, changes in Ca2+ signaling epitomize such remodeling: The reversible Ca2+ signaling phenotype of oocytes rapidly adapts to support irreversible propagation of the fertilization Ca2+ wave. Here, we simultaneously resolved IP3 receptor (IP3R) activity with endoplasmic reticulum (ER) structure to optically dissect the functional architecture of the Ca2+ release apparatus underpinning this reorganization. We show that changes in Ca2+ signaling correlate with IP3R redistribution from specialized ER substructures called annulate lamellae (AL), where Ca2+ release activity is attenuated, into IP3R-replete patches in the cortical ER of eggs that support the fertilization Ca2+ wave. These data show: first, that IP3R sensitivity is regulated with high spatial acuity even between contiguous ER regions; and second, that drastic reorganization of Ca2+ signaling dynamics can be driven by subcellular redistribution in the absence of changes in channel number or molecular or familial Ca2+ channel diversity. Finally, these results define a novel role for AL in Ca2+ signaling. Because AL are prevalent in other scenarios of rapid cell division, further studies of their impact on Ca2+ signaling are warranted