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 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 IP 3R 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 Ca2+ signaling. Because AL are prevalent in other scenarios of rapid cell division, further studies of their impact on Ca2+ signaling are warranted.
Bibliographical noteFunding Information:
The authors were supported by National Institutes of Health grant NS046783 and a National Science Foundation CAREER Award to J.S.M. (0237946). We would like to thank Roger Tsien (University of California at San Diego) and Jan Ellenberg (European Molecular Biology Laboratory) for their generous gifts of reagents.