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.
Boulware
Michael J
MJ
Department of Pharmacology, University of Minnesota, Minneapolis, 55455, USA.
Marchant
Jonathan S
JS
D000818:Animals; D002118:Calcium / Q000378:metabolism*; D015220:Calcium Channels / Q000378:metabolism*; D004721:Endoplasmic Reticulum / Q000378:metabolism*; D005260:Female; D005306:Fertilization / Q000502:physiology*; D031541:Fluorescence Resonance Energy Transfer; D053496:Inositol 1,4,5-Trisphosphate Receptors; D018613:Microscopy, Confocal; D009865:Oocytes / Q000378:metabolism / Q000502:physiology*; D010063:Ovum / Q000378:metabolism; D018160:Receptors, Cytoplasmic and Nuclear / Q000378:metabolism*; D015398:Signal Transduction / Q000502:physiology*; D014982:Xenopus laevis
D015220:Calcium Channels; D053496:Inositol 1,4,5-Trisphosphate Receptors; D018160:Receptors, Cytoplasmic and Nuclear; D002118:Calcium