Quantification of Ca2+-activated K+ channels under hormonal control in pig pancreas acinar cells

Maruyama, Yoshio; Petersen, O. H.; Flanagan, Paul; Pearson, Gemma

doi:10.1038/305228a0

Cited by 190 publications

(118 citation statements)

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“…The mechanisms underlying the Ca2+ influx are the subject of further investigation. MARUYAMA and PETERSEN (1984) suggested that the number of K+ channels per cell (N) increases 2-3 fold with CCK application in the pig pancreatic acinar cells, which has large K+ channels similar to those in the parotid gland acinar cells (MARUYAMA et al, 1983b). The value of N, estimated by ensemble fluctuation analysis, is about 30-110 (9 experimens), in the unstimulating parotid acinar cells (Maruyama et al, unpublished observations).…”

Section: Discussionmentioning

confidence: 99%

Activation of Ca2+-dependent Cl- and K+ conductances in rat and mouse parotid acinar cells.

et al. 1985

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Isolated acinar cells from rat and mouse parotid glands were studied with patch-clamp whole-cell current recordings. Acetylcholine (ACh) stimulation caused a transient inward current at a membrane potential of -70 mV, and a sustained outward current at a membrane potential of 0 mV, in quasi physiological Nat, K+ ion gradients, except the zero-C1-ion gradient condition across the membrane. The reversal potential obtained from the ACh-evoked steady current was about -75 mV, in this ionic condition. When major Cl-ions of both the pipette and the bath solution were replaced, either by glutamate or by sulphate, only a large outward current was observed, at a membrane potential of -60 mV , in the presence of ACh. The addition of Cat+-ionophore A23187 caused responses similar to those evoked by ACh. The reversal potential of A23187-induced current was close to the K+ equilibrium potential of -90 mV, in a C1 -free condition. When K+-free NaCI solution was used in the pipette and the bath, A23187 caused only a large inward current, at a membrane potential of -60 mV. The reversal potential of A23187-evoked current was about -15 mV, in a symmetrical K+-free, NaCI condition. These results suggest that the ACh and A23187 activate Clr as well as K+ conducting pathways via an increase in [Ca2+]i in the parotid acinar cells. The A23187-evoked large K+ current could not be explained solely by a rise in open probability of the channels.

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Section: Discussionmentioning

confidence: 99%

Activation of Ca2+-dependent Cl- and K+ conductances in rat and mouse parotid acinar cells.

et al. 1985

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“…In regards to pancreas, although we detected low levels of Lrrc26 message in pancreatic samples, we were unable to detect LRRC26 protein. Based on early recordings from pancreatic acinar cells (39,40) in which half activation of BK channels occurred at very negative voltages, we think it likely that LRRC26-containing BK channels are present in such cells, albeit at low current density. In fact, probably the best criterion for the presence of LRRC26-containing BK channels in a given cell type will rest on demonstration of appreciable fractional activation of BK channels at membrane potentials negative to 0 mV with 0 cytosolic Ca 2+ .…”

Section: Discussionmentioning

confidence: 99%

Knockout of the LRRC26 subunit reveals a primary role of LRRC26-containing BK channels in secretory epithelial cells

Yang

González-Pérez

Mukaibo

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Leucine-rich-repeat-containing protein 26 (LRRC26) is the regulatory γ1 subunit of Ca 2+ -and voltage-dependent BK-type K + channels. BK channels that contain LRRC26 subunits are active near normal resting potentials even without Ca 2+ , suggesting they play unique physiological roles, likely limited to very specific cell types and cellular functions. By using Lrrc26 KO mice with a β-gal reporter, Lrrc26 promoter activity is found in secretory epithelial cells, especially acinar epithelial cells in lacrimal and salivary glands, and also goblet and Paneth cells in intestine and colon, although absent from neurons. We establish the presence of LRRC26 protein in eight secretory tissues or tissues with significant secretory epithelium and show that LRRC26 protein coassembles with the pore-forming BK α-subunit in at least three tissues: lacrimal gland, parotid gland, and colon. In lacrimal, parotid, and submandibular gland acinar cells, LRRC26 KO shifts BK gating to be like α-subunit-only BK channels. Finally, LRRC26 KO mimics the effect of SLO1/BK KO in reducing [K + ] in saliva. LRRC26-containing BK channels are competent to contribute to resting K + efflux at normal cell membrane potentials with resting cytosolic Ca 2+ concentrations and likely play a critical physiological role in supporting normal secretory function in all secretory epithelial cells.L arge-conductance, voltage-and Ca 2+ -regulated BK-type channels are widely expressed proteins, found not only in excitable cells, such as neurons, muscle, and endocrine cells, but also nonexcitable cells, including salivary (1) and lacrimal gland (2) acinar cells, and colonic crypt cells (3). Given the almost ubiquitous expression of BK channels among cells that play quite distinct physiological roles, it is particularly important to define the specific properties of BK channels in a given cell type and determine what the specific physiological role played by BK channels in a given cell may be. A hallmark of BK channels is their dual regulation by both membrane voltage and cytosolic Ca 2+ (4), both properties embedded within the tetramer of pore-forming α-subunits of each BK channel (5). However, the specific range of voltages over which a BK channel is active at a given Ca 2+ concentration is markedly dependent on the identity of regulatory subunits that can coassemble with the α-subunit in the mature channel complex. Of the two families of known BK regulatory subunits, β (6-11) and γ (12-14), an important feature of many of these subunits is the ability to shift the range of activation voltages at a given Ca 2+ . Although there is growing information about the loci of expression and functional roles of BK channels containing specific β-subunits (15), much less is known about those BK channels containing the γ1 (LRRC26, leucine-rich-repeat-containing subunit 26) subunit. However, LRRC26 is particularly fascinating because it causes the largest shift in BK gating (approximately −120 mV) of any known non-pore-forming regulatory subunit, resulting in BK channels that...

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“…In vivo, somatostatin inhibits both Ca 2ϩ -induced and cyclic AMP-induced amylase secretion [11][12][13][14], but in vitro, a few consistent effects on secretion have been described [13,15]. As for ionic fluid secretion from pancreatic acini, only one report concerns the effect of insulin on cation channel [16].Ca 2ϩ -activated K ϩ channels, which have been suggested to regulate the K ϩ permeability changes in plasma membrane during fluid secretion, have been identified on the basolateral membrane of Cl Ϫ -secreting pancreatic acinar cells in a variety of animal species [17][18][19][20]. It has been suggested that these K ϩ channels are important for Cl Ϫ uptake into cells [21].…”

mentioning

confidence: 99%

“…Ca 2ϩ -activated K ϩ channels, which have been suggested to regulate the K ϩ permeability changes in plasma membrane during fluid secretion, have been identified on the basolateral membrane of Cl Ϫ -secreting pancreatic acinar cells in a variety of animal species [17][18][19][20]. It has been suggested that these K ϩ channels are important for Cl Ϫ uptake into cells [21].…”

mentioning

confidence: 99%

A Reciprocal Regulation of Ca2+-Activated K+ Channel by Insulin and Somatostatin in Guinea-Pig Pancreatic Acinar Cells.

Yanagisawa¹,

Suzuki²

2001

JJP

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The pancreatic acini are in close contact with the surrounding islets, having no significant fibrous capsules, and receptors of insulin [1][2][3][4] and somatostatin [5,6] on the pancreatic acinar cell have been reported. Therefore, this might eventually enter into very close interrelation between the exocrine pancreas and the endocrine islet of Langerhans.The secretion of the pancreatic acinar cells has for a long time been thought to be regulated by the islet hormones [7], but few detailed studies indicate hormonal regulation of the acinar cells. In digestive enzyme secretion, for example, insulin potentiates acetylcholine-induced [8,9] and, cholecytokinin-induced amylase secretion [10]. In vivo, somatostatin inhibits both Ca 2ϩ -induced and cyclic AMP-induced amylase secretion [11][12][13][14], but in vitro, a few consistent effects on secretion have been described [13,15]. As for ionic fluid secretion from pancreatic acini, only one report concerns the effect of insulin on cation channel [16].Ca 2ϩ -activated K ϩ channels, which have been suggested to regulate the K ϩ permeability changes in plasma membrane during fluid secretion, have been identified on the basolateral membrane of Cl Ϫ -secreting pancreatic acinar cells in a variety of animal species [17][18][19][20]. It has been suggested that these K ϩ channels are important for Cl Ϫ uptake into cells [21]. Secretagogues evoking an increase in cytoplasmic Ca 2ϩ level activate K ϩ channels causing an increase in the local external K ϩ concentration. Na ϩ , K ϩ , and Cl Key words: insulin, somatostatin, potassium channels, pancreatic juice, cyclic AMP. Abstract:The effects of islet hormones, insulin and somatostatin, on the regulation of the opening of Ca 2ϩ -activated K ϩ channels in the basolateral plasma membrane of primary cultured pancreatic acinar cells of guinea-pig were studied by cell-attached single-channel recording technique. A single application of insulin or somatostatin did not influence the opening of K ϩ channel. The open-state probability (p) of K ϩ channel induced by the application of acetylcholine (ACh) to the bath solution was increased by insulin in the presence of ACh. The enhancement effect of insulin on the increased frequency of the channel opening was not seen when concomitantly applied with protein kinase A inhibitor, Rp-cAMPS triethylamine. Insulin increased the p value of K ϩ channel, which was reversed by an application of somatostatin (Tyr-somatostatin 28). The addition of ACh followed by forskolin or dibutyryl adenosine 3Ј,5Ј-cyclic monophosphate (dbcAMP) to the bath solution evoked an increase in the p value of K ϩ channel. After increasing the channel opening, the addition of somatostatin reduced the p value, but not with dbcAMP. Taken together, the results suggest that insulin and somatostatin reciprocally modify the ACh-induced opening of the Ca 2ϩ -activated K ϩ channel through a cyclic AMP-dependent signaling pathway.

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Quantification of Ca2+-activated K+ channels under hormonal control in pig pancreas acinar cells

Cited by 190 publications

References 9 publications

Activation of Ca2+-dependent Cl- and K+ conductances in rat and mouse parotid acinar cells.

Activation of Ca2+-dependent Cl- and K+ conductances in rat and mouse parotid acinar cells.

Knockout of the LRRC26 subunit reveals a primary role of LRRC26-containing BK channels in secretory epithelial cells

A Reciprocal Regulation of Ca2+-Activated K+ Channel by Insulin and Somatostatin in Guinea-Pig Pancreatic Acinar Cells.

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