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Differential Distribution of Inositol Trisphosphate Receptor Isoforms in Mouse Oocytes¹

^a Departments of Obstetrics/Gynecology and Anatomy/Cell Biology, Tufts University School of Medicine and New England Medical Center Hospital, Boston, Massachusetts 02111 ^b Department of Veterinary and Animal Sciences, University of Massachusetts, Amherst, Massachusetts 01003 ^c Department of Anatomy and Cell Biology, University of Iowa, Iowa City, Iowa 52242 ^d Department of Cell Biology, Harvard Medical School, Boston, Massachusetts 02115-5701 ^e Laboratorium voor Fysiologie, Campus Gasthuisberg O/N, K. U. Leuven, B-3000 Leuven, Belgium

In mammalian fertilization, inositol 1,4,5-trisphosphate receptor (IP₃R)-dependent Ca²⁺ release is a crucial signaling event that originates from the vicinity of sperm-egg interaction and spreads as a wave throughout the egg cytoplasm. While it is known that Ca²⁺ is released by the type 1 IP₃R in the egg cortex, the potential involvement of other isoform types responsible for the Ca²⁺ rise in the mouse egg (interior) and their spatial distribution are not known. In addition, the biochemical basis has not been definitively established for the development of increased sensitivity to inositol 1,4,5-trisphosphate (IP₃) during meiotic maturation. Using specific antibodies to the type 1, 2, and 3 IP₃R, we tested the hypotheses that different IP₃R isoforms are responsible for the internal Ca²⁺ elevation and that they contribute to the maturation-associated acquisition of IP₃ sensitivity. In both preovulatory oocytes and ovulated eggs of CF-1 mice, immunofluorescence revealed that types 1 and 2 isoforms were present in the cell cortex and interior. Type 1 was observed throughout the cytoplasm, and Western analysis indicated a 1.9-fold maturation-associated increase. In contrast, the signals detected for the type 2 (high-affinity) isoform and type 3 were present to a lesser extent, with type 2 restricted to isolated islands (similar to aggregates of vesicles detected by electron microscopy), which, in the cortex, may amplify early sperm-egg signaling events. The cortical-to-perinuclear localization of the receptor and cortical vesicle aggregates imply an efficient mechanism for propagating Ca²⁺ release from the cortex into the interior of the egg to activate development, and the isoform localization analysis indicates a clear spatial and biochemical heterogeneity. Types 1 and 2 isoforms were also present in granulosa cells.

¹ This work was supported by grants to T.D. (NIH HD 24191), E.A. (NIH HD 14574), F.L. (NIH HD 22085), and R.A.F. (USDA 94–1428, USDA 97–2919). J.B.P. is Research Associate of the Fund for Scientific Research—Flanders (F.W.O.) and was supported in part by G.O.A. grant 94/4.

² Correspondence: Tom Ducibella, Dept. Ob/Gyn, Tufts University, School of Medicine, 136 Harrison Ave., Boston, MA 02111. FAX: 617 636 2917; tducibel{at}opal.tufts.edu

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