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J. Biol. Chem., Vol. 279, Issue 48, 50410-50419, November 26, 2004

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A New Regulation of Non-capacitative Calcium Entry in Insect Pacemaker Neurosecretory Neurons

INVOLVEMENT OF ARACHIDONIC ACID, NO-GUANYLYL CYCLASE/cGMP, AND cAMP^*

Dieter Wicher, Sandra Messutat, Céline Lavialle¶||, and Bruno Lapied¶

From the Saxon Academy of Sciences, Department Neurohormones, Erbertstrasse 1, 07743 Jena, Germany and the ^¶Laboratoire Récepteurs et Canaux Ioniques Membranaires RCIM UPRES EA 2647, Université d'Angers, 2 boulevard Lavoisier, 49045 Angers Cedex, France

Efferent dorsal unpaired median neurons are pacemaker neurosecretory cells. A Ca²⁺ background current contributing to the pacemaker activity of cockroach dorsal unpaired median neurons is up-regulated by neurohormone D (NHD), an octapeptide belonging to the adipokinetic hormone family. This modulation accelerates spiking and increases [Ca²⁺]_i. Using patch clamp, calcium imaging, and immunocytochemistry, we investigated the signaling pathway of NHD-induced current modulation. The membrane depolarization produced by NHD was related to the increase in membrane conductance for Ca²⁺, Ba²⁺, or Sr²⁺. This increase was abolished by LOE 908, an inhibitor of noncapacitive Ca²⁺ entry (NCCE), and it was strongly attenuated by the phospholipase C inhibitor U37122 and the diacylglycerol lipase inhibitor RHC80267 Arachidonic acid and ETYA mimicked the NHD effect on background current. This was abolished by L-NAME and ODQ, inhibitors of NO synthase and NO-sensitive guanylyl cyclase, respectively, but mimicked by the NO donor sodium nitroprusside and 8-bromo-cGMP. Immunocytochemistry using cGMP antibodies indicated that NHD and ETYA increase cGMP. Inhibition of protein kinase G with KT5823 and R_p-8-pCPT-cGMPS had no effect, whereas zaprinast, a cGMP-specific phosphodiesterase 5,6,9 inhibitor, mimicked the NHD effect. Furthermore, inhibition of the cGMP-activated phosphodiesterase 2 by EHNA and trequinsin abolished the effect of NHD. We conclude that the final step of the NHD signal transduction is the phosphodiesterase 2-induced down-regulation of the cAMP level. This removes a depression of NCCE directly attributed to cAMP because inhibition of protein kinase A with KT5720, R_p-cAMPS, and PKI14-22 amide did not mimic the NHD effect. We also demonstrate that any mechanism increasing the cGMP level can induce NCCE.

Received for publication, May 25, 2004 , and in revised form, August 17, 2004.

^* This work was supported in part by Deutsche Forschungsgemein-schaft Grant Wi 1422/2-3,4. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^|| Supported by a doctoral fellowship from Région Pays de la Loire.

To whom correspondence should be addressed. Tel.: 49-3641-949193; Fax: 49-3641-949192; E-mail: b6widi{at}pan.zoo.uni-jena.de.

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This article has been cited by other articles:

				D. Wicher, H.-J. Agricola, S. Sohler, M. Gundel, S. H. Heinemann, L. Wollweber, M. Stengl, and C. Derst Differential Receptor Activation by Cockroach Adipokinetic Hormones Produces Differential Effects on Ion Currents, Neuronal Activity, and Locomotion J Neurophysiol, April 1, 2006; 95(4): 2314 - 2325. [Abstract] [Full Text] [PDF]

				D. Wicher, H.-J. Agricola, R. Schonherr, S. H. Heinemann, and C. Derst TRP{gamma} Channels Are Inhibited by cAMP and Contribute to Pacemaking in Neurosecretory Insect Neurons J. Biol. Chem., February 10, 2006; 281(6): 3227 - 3236. [Abstract] [Full Text] [PDF]

				D. Wicher, J. Berlau, C. Walther, and A. Borst Peptidergic Counter-Regulation of Ca2+- and Na+-Dependent K+ Currents Modulates the Shape of Action Potentials in Neurosecretory Insect Neurons J Neurophysiol, January 1, 2006; 95(1): 311 - 322. [Abstract] [Full Text] [PDF]