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Increase of cGMP, cADP-ribose and inositol 1,4,5-trisphosphate preceding Ca²⁺ transients in fertilization of sea urchin eggs

Ritsu Kuroda¹, Kenji Kontani², Yasunari Kanda^2,*, Toshiaki Katada², Takashi Nakano¹, Yu-ichi Satoh³, Norio Suzuki³ and Hideyo Kuroda^1,

¹ Department of Environmental Biology and Chemistry, Faculty of Science, Toyama University, 3190 Gofuku, Toyama 930-8555, Japan
² Department of Physiological Chemistry, Graduate School of Pharmaceutical Sciences, University of Tokyo, 3-7-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
³ Division of Biological Sciences, Graduate School of Science, Hokkaido University, Kita-ku, Kita 10-jyo, Nishi 8-chome, Sapporo 060-0810, Japan
^* Present address: Department of Pharmacology, National Defense Medical College, Namiki, Tokorozawa 359-8513, Japan

Author for correspondence (e-mail: kuroda{at}sci.toyama-u.ac.jp)

Accepted July 27, 2001

Transient increases, or oscillations, of cytoplasmic free Ca²⁺ concentration, [Ca²⁺]_i, occur during fertilization of animal egg cells. In sea urchin eggs, the increased Ca²⁺ is derived from intracellular stores, but the principal signaling and release system involved has not yet been agreed upon. Possible candidates are the inositol 1,4,5-trisphosphate receptor/channel (IP₃R) and the ryanodine receptor/channel (RyR) which is activated by cGMP or cyclic ADP-ribose (cADPR). Thus, it seemed that direct measurements of the likely second messenger candidates during sea urchin fertilization would be essential to an understanding of the Ca²⁺ signaling pathway. We therefore measured the cGMP, cADPR and inositol 1,4,5-trisphosphate (IP₃) contents of sea urchin eggs during the early stages of fertilization and compared these with the [Ca²⁺]_i rise in the presence or absence of an inhibitor against soluble guanylate cyclase. We obtained three major experimental results: (1) cytosolic cGMP levels began to rise first, followed by cADPR and IP₃ levels, all almost doubling before the explosive increase of [Ca²⁺]_i; (2) most of the rise in IP₃ occurred after the Ca²⁺ peak; IP₃ production could also be induced by the artificial elevation of [Ca²⁺]_i, suggesting the large increase in IP₃ is a consequence, rather than a cause, of the Ca²⁺ transient; (3) the measured increase in cGMP was produced by the soluble guanylate cyclase of eggs, and inhibition of soluble guanylate cyclase of eggs diminished the production of both cADPR and IP₃ and the [Ca²⁺]_i increase without the delay of Ca²⁺ transients. Taken together, these results suggest that the RyR pathway involving cGMP and cADPR is not solely responsible for the initiating event, but contributes to the Ca²⁺ transients by stimulating IP₃ production during fertilization of sea urchin eggs.

Key words: cGMP, cADP-ribose, IP₃, Ca²⁺ transient, Fertilization, Sea urchin eggs

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