IP3 receptor activity is differentially regulated in endoplasmic reticulum subdomains during oocyte maturation

Fertilization 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 Ca(2+) signaling epitomize such remodeling: The reversible Ca(2+) signaling phenotype of oocytes rapidly adapts to support irreversible propagation of the fertilization Ca(2+) wave. Here, we simultaneously resolved IP(3) receptor (IP(3)R) activity with endoplasmic reticulum (ER) structure to optically dissect the functional architecture of the Ca(2+) release apparatus underpinning this reorganization. We show that changes in Ca(2+) signaling correlate with IP(3)R redistribution from specialized ER substructures called annulate lamellae (AL), where Ca(2+) release activity is attenuated, into IP(3)R-replete patches in the cortical ER of eggs that support the fertilization Ca(2+) wave. These data show: first, that IP(3)R sensitivity is regulated with high spatial acuity even between contiguous ER regions; and second, that drastic reorganization of Ca(2+) signaling dynamics can be driven by subcellular redistribution in the absence of changes in channel number or molecular or familial Ca(2+) channel diversity. Finally, these results define a novel role for AL in Ca(2+) signaling. Because AL are prevalent in other scenarios of rapid cell division, further studies of their impact on Ca(2+) signaling are warranted.