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The Journal of Neuroscience, July 13, 2005, 25(28):6631-6640; doi:10.1523/JNEUROSCI.1139-05.2005

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Cellular/Molecular
Rat Adrenal Chromaffin Cells Are Neonatal CO₂ Sensors

Ana M. Muñoz-Cabello, Juan J. Toledo-Aral, José López-Barneo, and Miriam Echevarría

Laboratorio de Investigaciones Biomédicas, Departamento de Fisiología, and Hospital Universitario Virgen del Rocío, Universidad de Sevilla, E-41013 Seville, Spain

We studied the participation of adrenal medulla (AM) chromaffin cells in hypercapnic chemotransduction. Using amperometric recordings, we measured catecholamine (CAT) secretion from cells in AM slices of neonatal and adult rats perfused with solutions bubbled with different concentrations of CO₂. The secretory activity augmented from 1.74 ± 0.19 pC/min at 5% CO₂ to 6.36 ± 0.77 pC/min at 10% CO₂. This response to CO₂ was dose dependent and appeared without changes in extracellular pH, although it was paralleled by a drop in intracellular pH. Responsiveness to hypercapnia was higher in neonatal than in adult slices. The secretory response to hypercapnia required extracellular Ca²⁺ influx. Both the CO₂-induced internal pH drop and increase in CAT secretion were markedly diminished by methazolamide (2 µM), a membrane-permeant carbonic anhydrase (CA) inhibitor. We detected the presence of two CA isoforms (CAI and CAII) in neonatal AM slices by in situ hybridization and real-time PCR. The expression of these enzymes decreased in adult AM together with the disappearance of responsiveness to CO₂. In patch-clamped chromaffin cells, hypercapnia elicited a depolarizing receptor potential, which led to action potential firing, extracellular Ca²⁺ influx, and CAT secretion. This receptor potential (inhibited by methazolamide) was primarily attributable to activation of a resting cationic conductance. In addition, voltage-gated K⁺ current amplitude was also decreased by high CO₂. The CO₂-sensing properties of chromaffin cells may be of physiologic relevance, particularly for the adaptation of neonates to extrauterine life, before complete maturation of peripheral and central chemoreceptors.

Key words: hypercapnia; chromaffin cells; catecholamine secretion; carbonic anhydrase; intracellular acidosis; cationic conductance

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Received Nov 19, 2004; revised June 2, 2005; accepted June 3, 2005.

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