ATP triggers intracellular Ca2+ release in type II cells of the rat carotid body

• Published in: The Journal of physiology 2003-06, Vol.549 (3), p.739-747
• Main Authors: Xu, Jianhua, Tse, Frederick W., Tse, Amy
• Format: Article
• Language: English
• Subjects: Adenosine Triphosphate - pharmacology; Animals; Calcium - metabolism; Calcium Channels - physiology; Calcium Signaling - drug effects; Carotid Body - cytology; Carotid Body - drug effects; Carotid Body - metabolism; Catecholamines - metabolism; Cell Separation; Cytoplasmic Granules - drug effects; Cytoplasmic Granules - metabolism; Electrophysiology; Immunohistochemistry; In Vitro Techniques; Ion Channel Gating - drug effects; Male; Membrane Potentials - physiology; Original; Patch-Clamp Techniques; Rats; Rats, Sprague-Dawley; Receptors, Purinergic P2 - drug effects; Receptors, Purinergic P2Y2; S100 Proteins - biosynthesis; Stimulation, Chemical
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/jphysiol.2003.039735

Using a Ca 2+ -imaging technique, we studied the action of ATP on the intracellular Ca 2+ concentration ([Ca 2+ ] i ) of fura-2-loaded mixtures of type I and type II cells dissociated from rat carotid bodies. ATP (100 μ m ) triggered a transient rise in [Ca 2+ ] i in the spindle-shaped type II (sustentacular) cells, but not the ovoid type I (glomus) cells. When challenged with ionomycin (1 μ m ), no amperometry signal could be detected from the ATP-responsive type II cells, suggesting that these cells lacked catecholamine-containing granules. In contrast, KCl depolarization triggered robust quantal catecholamine release from type I cells that were not responsive to ATP. In type II cells voltage clamped at −70 mV, the ATP-induced [Ca 2+ ] i rise was not accompanied by any current change, suggesting that P2X receptors are not involved. The ATP-induced Ca 2+ signal could be observed in the presence of Ni 2+ (a blocker of voltage-gated Ca 2+ channels) or in the absence of extracellular Ca 2+ , indicating that Ca 2+ release from intracellular stores was the dominant mechanism. The order of purinoreceptor agonist potency in triggering the [Ca 2+ ] i rise was UTP > ATP > 2-methylthioATP ≫α,β-methyleneATP, implicating the involvement of P2Y 2 receptors. In carotid body sections, immunofluorescence revealed localization of P2Y 2 receptors on spindle-shaped type II cells that partially enveloped ovoid type I cells. Since ATP is released from type I cells during hypoxia, we suggest that the ATP-induced Ca 2+ signal in type II cells can mediate paracrine interactions within the carotid bodies.