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J. Biol. Chem., Vol. 280, Issue 34, 30611-30618, August 26, 2005

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Ca²+/Calmodulin-dependent Protein Kinase II Is an Essential Mediator in the Coordinated Regulation of Electrocyte Ca²+-ATPase by Calmodulin and Protein Kinase A^*

Rafael H. F. Valverde, Giovane G. Tortelote, Thiago Lemos¶, Elisabeth Mintz||, and Adalberto Vieyra**

From the Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941-590, Brazil and the ^||Laboratoire de Biophysique Moléculaire et Cellulaire, UMR 5090 Commissariat à l'Energie Atomique-CNRS-Université Joseph Fourier, 17 rue des Martyrs, 38054 Grenoble Cedex 9, France

The aim of this study was to investigate (a) whether Ca²⁺/calmodulin-dependent protein kinase II (CaM kinase II) participates in the regulation of plasma membrane Ca²⁺-ATPase and (b) its possible cross-talk with other kinase-mediated modulatory pathways of the pump. Using isolated innervated membranes of the electrocytes from Electrophorus electricus L., we found that stimulation of endogenous protein kinase A (PKA) strongly phosphorylated membrane-bound CaM kinase II with simultaneous substantial activation of the Ca²⁺ pump (2-fold). The addition of cAMP (5-50 pM), forskolin (10 nM), or cholera toxin (10 or 100 nM) stimulated both CaM kinase II phosphorylation and Ca²⁺-ATPase activity, whereas these activation processes were cancelled by an inhibitor of the PKA -catalytic subunit. When CaM kinase II was blocked by its specific inhibitor KN-93, the Ca²⁺-ATPase activity decreased to the levels measured in the absence of calmodulin; the unusually high Ca²⁺ affinity dropped 2-fold; and the PKA-mediated stimulation of Ca²⁺-ATPase was no longer seen. Hydroxylamine-resistant phosphorylation of the Ca²⁺-ATPase strongly increased when the PKA pathway was activated, and this phosphorylation was suppressed by inhibition of CaM kinase II. We conclude that CaM kinase II is an intermediate in a complex regulatory network of the electrocyte Ca²⁺ pump, which also involves calmodulin and PKA.

Received for publication, February 18, 2005 , and in revised form, June 10, 2005.

This work is dedicated to Dr. Darcy Fontoura de Almeida on his 75th birthday.

^* This work was supported in part by grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico, the Programa de Apoio aos Núcleos de Excelência (Conselho Nacional de Desenvolvimento Científico e Tecnológico/Ministério da Ciência e Tecnologia), the Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (Brazil), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior/Comité Français d'Evaluation de la Coopération Universitaire avec le Brésil Grant 378 (Brazil/France). 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.

Recipients of a fellowship from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior.

^¶ Recipient of a fellowship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico.

^** To whom correspondence should be addressed. Tel.: 55-21-2562-6520; Fax: 55-21-2280-8193; E-mail: avieyra{at}biof.ufrj.br.

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