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

Jianhua Xu, Frederick W. Tse, Amy Tse

Research output: Contribution to journalArticle

52 Citations (Scopus)

Abstract

Using a Ca2+-imaging technique, we studied the action of ATP on the intracellular Ca2+ concentration ([Ca2+]i) of fura-2-loaded mixtures of type I and type II cells dissociated from rat carotid bodies. ATP (100 μM) triggered a transient rise in [Ca2+]i in the spindle-shaped type II (sustentacular) cells, but not the ovoid type I (glomus) cells. When challenged with ionomycin (1 μM), no amperometry signal could be detected from the ATP-responsive type II cells, suggesting that these cells lacked catecholamine-containing granules. In contrast, KCI 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 [Ca2+]i rise was not accompanied by any current change, suggesting that P2X receptors are not involved. The ATP-induced Ca2+ signal could be observed in the presence of Ni2+ (a blocker of voltage-gated Ca2+ channels) or in the absence of extracellular Ca2+, indicating that Ca2+ release from intracellular stores was the dominant mechanism. The order of purinoreceptor agonist potency in triggering the [Ca2+]i rise was UTP > ATP > 2-methylthioATP » α,β-methyleneATP, implicating the involvement of P2Y2 receptors. In carotid body sections, immunofluorescence revealed localization of P2Y2 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 Ca2+ signal in type II cells can mediate paracrine interactions within the carotid bodies.

Original languageEnglish (US)
Pages (from-to)739-747
Number of pages9
JournalJournal of Physiology
Volume549
Issue number3
DOIs
StatePublished - Jun 15 2003

Fingerprint

Carotid Body
Adenosine Triphosphate
Purinergic P2Y2 Receptors
Catecholamines
Cell Hypoxia
Uridine Triphosphate
Ionomycin
Fura-2
Fluorescent Antibody Technique

ASJC Scopus subject areas

  • Physiology

Cite this

ATP triggers intracellular Ca2+ release in type II cells of the rat carotid body. / Xu, Jianhua; Tse, Frederick W.; Tse, Amy.

In: Journal of Physiology, Vol. 549, No. 3, 15.06.2003, p. 739-747.

Research output: Contribution to journalArticle

Xu, Jianhua ; Tse, Frederick W. ; Tse, Amy. / ATP triggers intracellular Ca2+ release in type II cells of the rat carotid body. In: Journal of Physiology. 2003 ; Vol. 549, No. 3. pp. 739-747.
@article{da8a3551102c47fa8b60e7d5c40a14ee,
title = "ATP triggers intracellular Ca2+ release in type II cells of the rat carotid body",
abstract = "Using a Ca2+-imaging technique, we studied the action of ATP on the intracellular Ca2+ concentration ([Ca2+]i) of fura-2-loaded mixtures of type I and type II cells dissociated from rat carotid bodies. ATP (100 μM) triggered a transient rise in [Ca2+]i in the spindle-shaped type II (sustentacular) cells, but not the ovoid type I (glomus) cells. When challenged with ionomycin (1 μM), no amperometry signal could be detected from the ATP-responsive type II cells, suggesting that these cells lacked catecholamine-containing granules. In contrast, KCI 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 [Ca2+]i rise was not accompanied by any current change, suggesting that P2X receptors are not involved. The ATP-induced Ca2+ signal could be observed in the presence of Ni2+ (a blocker of voltage-gated Ca2+ channels) or in the absence of extracellular Ca2+, indicating that Ca2+ release from intracellular stores was the dominant mechanism. The order of purinoreceptor agonist potency in triggering the [Ca2+]i rise was UTP > ATP > 2-methylthioATP » α,β-methyleneATP, implicating the involvement of P2Y2 receptors. In carotid body sections, immunofluorescence revealed localization of P2Y2 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 Ca2+ signal in type II cells can mediate paracrine interactions within the carotid bodies.",
author = "Jianhua Xu and Tse, {Frederick W.} and Amy Tse",
year = "2003",
month = "6",
day = "15",
doi = "10.1113/jphysiol.2003.039735",
language = "English (US)",
volume = "549",
pages = "739--747",
journal = "Journal of Physiology",
issn = "0022-3751",
publisher = "Wiley-Blackwell",
number = "3",

}

TY - JOUR

T1 - ATP triggers intracellular Ca2+ release in type II cells of the rat carotid body

AU - Xu, Jianhua

AU - Tse, Frederick W.

AU - Tse, Amy

PY - 2003/6/15

Y1 - 2003/6/15

N2 - Using a Ca2+-imaging technique, we studied the action of ATP on the intracellular Ca2+ concentration ([Ca2+]i) of fura-2-loaded mixtures of type I and type II cells dissociated from rat carotid bodies. ATP (100 μM) triggered a transient rise in [Ca2+]i in the spindle-shaped type II (sustentacular) cells, but not the ovoid type I (glomus) cells. When challenged with ionomycin (1 μM), no amperometry signal could be detected from the ATP-responsive type II cells, suggesting that these cells lacked catecholamine-containing granules. In contrast, KCI 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 [Ca2+]i rise was not accompanied by any current change, suggesting that P2X receptors are not involved. The ATP-induced Ca2+ signal could be observed in the presence of Ni2+ (a blocker of voltage-gated Ca2+ channels) or in the absence of extracellular Ca2+, indicating that Ca2+ release from intracellular stores was the dominant mechanism. The order of purinoreceptor agonist potency in triggering the [Ca2+]i rise was UTP > ATP > 2-methylthioATP » α,β-methyleneATP, implicating the involvement of P2Y2 receptors. In carotid body sections, immunofluorescence revealed localization of P2Y2 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 Ca2+ signal in type II cells can mediate paracrine interactions within the carotid bodies.

AB - Using a Ca2+-imaging technique, we studied the action of ATP on the intracellular Ca2+ concentration ([Ca2+]i) of fura-2-loaded mixtures of type I and type II cells dissociated from rat carotid bodies. ATP (100 μM) triggered a transient rise in [Ca2+]i in the spindle-shaped type II (sustentacular) cells, but not the ovoid type I (glomus) cells. When challenged with ionomycin (1 μM), no amperometry signal could be detected from the ATP-responsive type II cells, suggesting that these cells lacked catecholamine-containing granules. In contrast, KCI 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 [Ca2+]i rise was not accompanied by any current change, suggesting that P2X receptors are not involved. The ATP-induced Ca2+ signal could be observed in the presence of Ni2+ (a blocker of voltage-gated Ca2+ channels) or in the absence of extracellular Ca2+, indicating that Ca2+ release from intracellular stores was the dominant mechanism. The order of purinoreceptor agonist potency in triggering the [Ca2+]i rise was UTP > ATP > 2-methylthioATP » α,β-methyleneATP, implicating the involvement of P2Y2 receptors. In carotid body sections, immunofluorescence revealed localization of P2Y2 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 Ca2+ signal in type II cells can mediate paracrine interactions within the carotid bodies.

UR - http://www.scopus.com/inward/record.url?scp=0038380659&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0038380659&partnerID=8YFLogxK

U2 - 10.1113/jphysiol.2003.039735

DO - 10.1113/jphysiol.2003.039735

M3 - Article

C2 - 12730345

AN - SCOPUS:0038380659

VL - 549

SP - 739

EP - 747

JO - Journal of Physiology

JF - Journal of Physiology

SN - 0022-3751

IS - 3

ER -