Nicotinic Acid Adenine Dinucleotide Phosphate-induced Ca2+ Release

doi:10.1074/jbc.275.12.8301

Nicotinic Acid Adenine Dinucleotide Phosphate-induced Ca²⁺ Release

INTERACTIONS AMONG DISTINCT Ca²⁺ MOBILIZING MECHANISMS IN STARFISH OOCYTES*

From the ^‡Laboratory of Cell Biology Stazione Zoologica “A. Dohrn” Villa Comunale, I-80121, Napoli, Italy, the ^§Asamushi Marine Biological Station, Asamushi, Aomori 039-3501, Japan, the ^¶Department of Pharmacology, Tennis Court Road, Cambridge, CB2 1QJ United Kingdom, and the ^‖Department of Biochemistry, University of Padova, 35121 Padova, Italy

Abstract

An intracellular mechanism activated by nicotinic acid adenine dinucleotide phosphate (NAADP⁺) contributes to intracellular Ca²⁺ release alongside inositol 1,4,5-trisphosphate (Ins-P₃) and ryanodine receptors. The NAADP⁺-sensitive mechanism has been shown to be operative in sea urchin eggs, ascidian eggs, and pancreatic acinar cells. Furthermore, most mammalian cell types can synthesize NAADP⁺, with nicotinic acid and NADP⁺ as precursors. In this contribution, NAADP⁺-induced Ca²⁺ release has been investigated in starfish oocytes. Uncaging of injected NAADP⁺ induced Ca²⁺mobilization in both immature oocytes and in oocytes matured by the hormone 1-methyladenine (1-MA). The role of extracellular Ca²⁺ in NAADP⁺-induced Ca²⁺mobilization, which was minor in immature oocytes, was instead essential in mature oocytes. Thus, the NAADP⁺-sensitive Ca²⁺ pool, which is known to be distinct from those sensitive to inositol 1,4,5-trisphosphate or cyclic ADPribose, apparently migrated closer to (or became part of) the plasma membrane during the maturation process. Inhibition of both Ins-P₃and ryanodine receptors, but not of either alone, substantially inhibited NAADP⁺-induced Ca²⁺ mobilization in both immature and mature oocytes. The data also suggest that NAADP⁺-induced Ca²⁺ mobilization acted as a trigger for Ca²⁺ release via Ins-P₃ and ryanodine receptors.

Footnotes

↵* This work was made possible by the financial contributions of the Japan Society for the promotion of Science and the National Research Council of Italy (to L. S.), of the Italian Ministry of Scientific Research (M.U.R.S.T., P.R.I.N. 1998, to E. C.), of the National Research Council of Italy (Target Project of Biochemistry), and of the European Molecular Biology Organization (to A. A. G.). The support of Telethon (Grant 963) is also gratefully acknowledged.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
↵** To whom correspondence should be addressed: Dept. of Biochemistry, University of Padova, Viale G. Colombo 3, 35121, Padova, Italy. Tel.: 0039-049-8276137; Fax: 0039-049-8276125.
Abbreviations:

Ins-P₃

inositol 1,4,5-trisphosphate

1-MA

1-methyladenine

NAADP⁺

nicotinic acid adenine dinucleotide phosphate

cADPr

cyclic ADPribose

GVBD

germinal vesicle breakdown
- Received September 7, 1999.
- Revision received November 22, 1999.
The American Society for Biochemistry and Molecular Biology, Inc.