Transmitter-like action of ATP on patched membranes of cultured myoblasts and myotubes

Kolb, Hans‐Albert; Wakelam, Michael J.O.

doi:10.1038/303621a0

Cited by 138 publications

(70 citation statements)

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“…Localization of zP2X 5.1 The existence of an ion channel sensitive to ATP in skeletal muscle was first suggested many years ago [24]. Although subsequent studies confirmed the existence of ATP-sensitive ion channels in avian skeletal muscle, they suggested that the single-channel currents had a very low unitary conductance compared to the initial report [25,26].…”

Section: Cloning Of Zebrafish P2x Receptor Cdnas Uncovered Three New mentioning

confidence: 59%

“…Evidence from other species had suggested that ATP responses would be found in zebrafish muscle. For instance, contractions of frog skeletal muscle in response to extracellular ATP were first reported in the 1940s [39], and the electrophysiological characterization of P2X receptor properties on cultured chick myoblasts and myotubes was explored in detail in the 1980s [24,25,40]. In the 1990s, cloning studies demonstrated that P2X 5 was expressed in chick skeletal muscle, and when chick P2X 5 was expressed in oocytes, the currents exhibited properties expected for the endogenous chick receptors [41].…”

Section: Discussionmentioning

confidence: 99%

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Amino acid variations resulting in functional and nonfunctional zebrafish P2X1 and P2X5.1 receptors

Low

Kuwada

Hume

2008

Purinergic Signalling

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Section: Cloning Of Zebrafish P2x Receptor Cdnas Uncovered Three New mentioning

confidence: 59%

Section: Discussionmentioning

confidence: 99%

Amino acid variations resulting in functional and nonfunctional zebrafish P2X1 and P2X5.1 receptors

Low

Kuwada

Hume

2008

Purinergic Signalling

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“…The original evidence that ATP directly gates the opening of ion channels was based on whole-cell and single-channel recordings from embryonic chick skeletal muscle myotubes (Kolb and Wakelam, 1983). Subsequent studies in chick and frog showed striking developmental regulation of these channels; they disappear during late embryogenesis but reappear in the adult after denervation (Hume and Honig, 1986;Igusa, 1988;Thomas and Hume, 1990a;Thomas et al, 1991;Wells et al, 1995).…”

Section: Discussionmentioning

confidence: 99%

Pharmacological and Biophysical Properties of the Human P2X₅Receptor

et al. 2003

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We constructed a full-length human P2X 5 purinoceptor cDNA by incorporating a sequence corresponding to exon 10, which is missing in cDNAs cloned previously from human tissues. We studied the functional properties by patch-clamp recording and fluorescence imaging after expression in human embryonic kidney 293 cells. ATP (1-100 M; half-maximal current at 4 M) elicited inward currents at Ϫ60 mV; these persisted during brief (2 s) applications but declined during longer applications. The peak current was dependent on the holding potential and showed little rectification; however, both the desensitization during the application and the decline in the current when ATP was washed out were slower at ϩ30 mV than at Ϫ60 mV. 2Ј,3Ј-O-(4-Benzoyl)-benzoyl-ATP and ␣␤-methylene-ATP mimicked the action of ATP (half-maximal concentrations 6 and 161 M, respectively). The currents were inhibited by suramin, pyridoxal-5-phosphate-6-azo-2Ј,4Ј-disulfonic acid and Brilliant Blue G, with half-maximal inhibition at 3, 0.2, and 0.5 M, respectively; 2Ј,3Ј-O-(2Ј,4Ј,6Ј-trinitrophenol)-ATP (1 M) was ineffective. Removing divalent cations did not significantly alter ATP concentration-response curves. Reversal potential measurements showed that the human P2X 5 receptor was permeable to calcium (P Ca /P Na ϭ 1.5) and N-methyl-D-glucamine (NMDG) (P NMDG /P Na ϭ 0.4); it was also permeable to chloride (P Cl /P Na ϭ 0.5) but not gluconate (P gluc /P Na ϭ 0.01) ions. The permeability to NMDG developed as quickly as the channel opened, in contrast to the P2X 7 receptor where the NMDG permeability develops over several seconds. Cells expressing human P2X 5 receptors also rapidly accumulated the propidium dye YO-PRO-1 in response to ATP.A P2X 5 subunit cDNA was first isolated from libraries of rat sympathetic ganglia (Collo et al., 1996) and heart (Garcia-Guzman et al., 1996). The RNA is expressed predominantly in heart (Garcia-Guzman et al., 1996) but there is also expression in brain, spinal cord, and adrenal gland (GarciaGuzman et al., 1996). Immunoreactivity for P2X 5 subunits has also been described in developing skeletal muscle of the rat (Meyer et al., 1999;Ryten et al., 2001); recently, the receptor has been implicated in the differentiation of satellite cells into mature multinucleated muscle fibers (Ryten et al., 2002). Mammalian skin and endocrine (Glass and Burnstock, 2001) cells also show P2X 5 immunoreactivity.When expressed in HEK293 cells, the rat P2X 5 subunit cDNAs gave rise to currents activated by ATP, but these were very small and their properties not extensively studied. The current was elicited by ATP [half-maximal concentration (EC 50 ) about 10 M] but not by ␣␤meATP, and it was readily blocked by suramin and PPADS in the 1 to 10 M concentration range (Collo et al., 1996;Garcia-Guzman et al., 1996). A mouse cDNA has also been cloned and expressed; again, the currents recorded from HEK293 cells were only a few tens of picoamperes and they were not studied in detail . On the other hand, although these two mammalian recep...

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“…These characteristics, as well as the nucleotide specificity (ATP > ATP-gamma-s > ADP) are very similar to the results reported here, in which the TEA-sensitive effiux appears to be due to the activation of a Ca~+-sensitive BK channel, and the TEA-insensitive channel may include the activation of the nonspecific cation channel. Extracellular ATP also activated a nonselective cation conductance in a mouse macrophage cell line (Buisman et al, 1988), rat vas deferens (Freil, 1988), and cultured chick myoblasts (Kolb and Wakelam, 1983), and a Ca2+-sensitive K + channel in cultured bovine aortic endothelial cells (Sauve et al, 1988).…”

Section: Atp and Carbachol Activate K + Efflux Through Multiple Pathwaysmentioning

confidence: 99%

Effects of extracellular ATP on ion transport systems and [Ca2+]i in rat parotid acinar cells. Comparison with the muscarinic agonist carbachol.

Soltoff

McMillian

Cragoe

et al. 1990

The Journal of General Physiology

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The effects of extracellular ATP on ion fluxes and the intracellular free Ca 2 § concentration ([Ca~+]i) were examined using a suspension of rat parotid acinar cells and were contrasted with the effects of the muscarinic agonist carbachol. Although ATP and carbachol both rapidly increased [Ca2+] i about threefold above the resting level (200-250 nM), the effect of ATP was due primarily to an influx of Ca ~+ across the plasma membrane, while the initial response to carbachol was due to a release of Ca ~ § from intracellular stores. Within 10 s, ATP (1 mM) and carbachol (20 #M) reduced the cellular C1-content by 39-50% and cell volume by 15-25%. Both stimuli reduced the cytosolic K + content by 57-65%, but there were marked differences in the rate and pattern of net K § movement as well as the effects of K + channel inhibitors on the effluxes initiated by the two stimuli. The maximum rate of the ATP-stimulated K § efflux (~2,200 nmol K+/mg protein per min) was about two-thirds that of the carbachol-initiated efflux rate, and was reduced by ~30% (vs. 60% for the carbachol-stimulated K + efflux) by TEA (tetraethylammonium), an inhibitor of the large conductance (BK) K § channel. Charybdotoxin, another K § channel blocker, was markedly more effective than TEA on the effects of both agonists, and reduced the rate of K § effiux initiated by both ATP and carbachol by ~80%. The removal of extracellular Ca ~ § reduced the ATPand the carbachol-stimulated rates of K + efflux by 55 and 17%, respectively. The rate of K + effiux initiated by either agonist was reduced by 78-95% in cells that were loaded with BAPTA to slow the elevation of [Ca2+]i. These results indicated that ATP and carbachol stimulated the effiux of K + through multiple types of K § permeable channels, and demonstrated that the relative proportion of efflux 320THE JOURNAL OF GENERAL PHYSIOLOGY 9 VOLUME 95 9 1990 through the different pathways was different for the two stimuli. ATP and carbachol also stimulated the rapid entry of Na § into the parotid cell, and elevated the intracellular Na § content to 4.4 and 2.6 times the normal level, respectively. The rate of Na § entry through Na+-K+-2CI-cotransport and Na+-H § exchange was similar whether stimulated by ATP, carbachol, or ionomycin, and uptake through these two carrier-mediated transporters accounted for 50% of the ATP-promoted Na § influx. The remainder may be due to a nonselective cation channel and an ATP-gated cation channel that is also permeable to Ca ~ § The consumption of extracellular ATP by an ecto-ATPase (apparent K0.5 for ATP is 0.93 mM) on the plasma membrane limited the duration of the response to ATP when large concentrations of cells were used. The effects of ATP on [Ca~+]i and ion fluxes were blocked specifically by DIDS (4,4'-diisothiocyanostilbene-2,2'-disulfonic acid), and were more potent in the absence of Mg ~+, suggesting that the active nucleotide moiety was ATP 4-. These studies suggest that ATP may function as a neurotransmitter and modulate fluid secretion by stimula...

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Transmitter-like action of ATP on patched membranes of cultured myoblasts and myotubes

Cited by 138 publications

References 8 publications

Amino acid variations resulting in functional and nonfunctional zebrafish P2X1 and P2X5.1 receptors

Amino acid variations resulting in functional and nonfunctional zebrafish P2X1 and P2X5.1 receptors

Pharmacological and Biophysical Properties of the Human P2X₅Receptor

Effects of extracellular ATP on ion transport systems and [Ca2+]i in rat parotid acinar cells. Comparison with the muscarinic agonist carbachol.

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Transmitter-like action of ATP on patched membranes of cultured myoblasts and myotubes

Cited by 138 publications

References 8 publications

Amino acid variations resulting in functional and nonfunctional zebrafish P2X1 and P2X5.1 receptors

Amino acid variations resulting in functional and nonfunctional zebrafish P2X1 and P2X5.1 receptors

Pharmacological and Biophysical Properties of the Human P2X5Receptor

Effects of extracellular ATP on ion transport systems and [Ca2+]i in rat parotid acinar cells. Comparison with the muscarinic agonist carbachol.

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Pharmacological and Biophysical Properties of the Human P2X₅Receptor