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J Biol Chem, Vol. 274, Issue 50, 35693-35702, December 10, 1999

Characterization of a Plasma Membrane Calcium Oscillator in Rat Pituitary Somatotrophs*

Melanija Tomic', Taka-aki Koshimizu, Davy Yuan, Silvana A. Andric, Dragoslava Zivadinovic, and Stanko S. StojilkovicDagger

From the Endocrinology and Reproduction Research Branch, NICHD, National Institutes of Health, Bethesda, Maryland 20892-4510

In excitable cells, oscillations in intracellular free calcium concentrations ([Ca2+]i) can arise from action-potential-driven Ca2+ influx, and such signals can have either a localized or global form, depending on the coupling of voltage-gated Ca2+ influx to intracellular Ca2+ release pathway. Here we show that rat pituitary somatotrophs generate spontaneous [Ca2+]i oscillations, which rise from fluctuations in the influx of external Ca2+ and propagate within the cytoplasm and nucleus. The addition of caffeine and ryanodine, modulators of ryanodine-receptor channels, and the depletion of intracellular Ca2+ stores by thapsigargin and ionomycin did not affect the global nature of spontaneous [Ca2+]i signals. Bay K 8644, an L-type Ca2+ channel agonist, initiated [Ca2+]i signaling in quiescent cells, increased the amplitude of [Ca2+]i spikes in spontaneously active cells, and stimulated growth hormone secretion in perifused pituitary cells. Nifedipine, a blocker of L-type Ca2+ channels, decreased the amplitude of spikes and basal growth hormone secretion, whereas Ni2+, a blocker of T-type Ca2+ channels, abolished spontaneous [Ca2+]i oscillations. Spiking was also abolished by the removal of extracellular Na+ and by the addition of 10 mM Ca2+, Mg2+, or Sr2+, the blockers of cyclic nucleotide-gated channels. Reverse transcriptase-polymerase chain reaction and Southern blot analyses indicated the expression of mRNAs for these channels in mixed pituitary cells and purified somatotrophs. Growth hormone-releasing hormone, an agonist that stimulated cAMP and cGMP productions in a dose-dependent manner, initiated spiking in quiescent cells and increased the frequency of spiking in spontaneously active cells. These results indicate that in somatotrophs a cyclic nucleotide-controlled plasma membrane Ca2+ oscillator is capable of generating global Ca2+ signals spontaneously and in response to agonist stimulation. The Ca2+-signaling activity of this oscillator is dependent on voltage-gated Ca2+ influx but not on Ca2+ release from intracellular stores.

* 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.

Dagger To whom correspondence and reprint requests should be addressed: Section on Cellular Signaling/ERRB/NICHD, Bldg. 49, Room 6A-36, 49 Convent Dr., Bethesda, MD 20892-4510. Tel.: 301-496-1638; Fax: 301-594-7031; E-mail: stankos@helix.nih.gov.

Copyright © 1999 by The American Society for Biochemistry and Molecular Biology, Inc.
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