Role of K2P channels in stimulus-secretion coupling

Pflugers Archiv European Journal of Physiology

Volumn 467, Issue 5, 2015, Pages 1001-1011

  Kim, Donghee ^a   Kang, Dawon ^b  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b Gyeongsang National University School of Medicine   (South Korea)

Author keywords

Adrenal gland; Carotid body glomus cells; Chemoreceptors; Hypoxia; Non selective cation channel

Indexed keywords

ANGIOTENSIN II; CALCIUM ION; CATION CHANNEL; TANDEM PORE DOMAIN POTASSIUM CHANNEL; TWO PORE DOMAIN POTASSIUM CHANNEL; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; CALCIUM;

ADRENAL CORTEX CELL; ADRENAL GLAND; ADRENAL MEDULLA; ALDOSTERONE RELEASE; ANIMAL CELL; AUTOREGULATION; CALCIUM TRANSPORT; CAROTID BODY; CAROTID BODY CHEMORECEPTOR; DEPOLARIZATION; HORMONE RELEASE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; REVIEW; STIMULUS SECRETION COUPLING; ANIMAL; CHEMORECEPTOR CELL; MEMBRANE POTENTIAL; METABOLISM; PHYSIOLOGY;

ADRENAL GLANDS; ANIMALS; CALCIUM; CAROTID BODY; CHEMORECEPTOR CELLS; HUMANS; MEMBRANE POTENTIALS; POTASSIUM CHANNELS, TANDEM PORE DOMAIN;

EID: 84939418326     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1663-3     Document Type: Review

References (67)

1. Abudara V, Eyzaguirre C (2008) Mechanical sensitivity of carotid body glomus cells. Respir Physiol Neurobiol 161(2):210–213
2. Abudara V, Jiang RG, Eyzaguirre C (2002) Behavior of junction channels between rat glomus cells during normoxia and hypoxia. J Neurophysiol 88(2):639–649
3. Bandulik S, Penton D, Barhanin J, Warth R (2010) TASK1 and TASK3 potassium channels: determinants of aldosterone secretion and adrenocortical zonation. Horm Metab Res 42(6):450–457
4. Bandulik S, Tauber P, Penton D, Schweda F, Tegtmeier I, Sterner C, Lalli E, Lesage F, Hartmann M, Barhanin J, Warth R (2013) Severe hyperaldosteronism in neonatal Task3 potassium channel knockout mice is associated with activation of the intraadrenal renin-angiotensin system. Endocrinology 154(8):2712–2722
5. Bayliss DA, Barrett PQ (2008) Emerging roles for two-pore-domain potassium channels and their potential therapeutic impact. Trends Pharmacol Sci 29(11):566–575
6. Bin-Jaliah I, Maskell PD, Kumar P (2004) Indirect sensing of insulin-induced hypoglycaemia by the carotid body in the rat. J Physiol 556(Pt 1):255–266
7. Bournaud R, Hidalgo J, Yu H, Girard E, Shimahara T (2007) Catecholamine secretion from rat foetal adrenal chromaffin cells and hypoxia sensitivity. Pflugers Arch 454(1):83–92
8. Brown ST, Buttigieg J, Nurse CA (2010) Divergent roles of reactive oxygen species in the responses of perinatal adrenal chromaffin cells to hypoxic challenges. Respir Physiol Neurobiol 174(3):252–258
9. Buckler KJ (1997) A novel oxygen-sensitive potassium current in rat carotid body type I cells. J Physiol 498(Pt 3):649–662
10. Buckler KJ (2007) TASK-like potassium channels and oxygen sensing in the carotid body. Respir Physiol Neurobiol 157(1):55–64
11. Buckler KJ, Turner PJ (2013) Oxygen sensitivity of mitochondrial function in rat arterial chemoreceptor cells. J Physiol 591(Pt 14):3549–3563
12. Buckler KJ, Williams BA, Honore E (2000) An oxygen-, acid- and anaesthetic-sensitive TASK-like background potassium channel in rat arterial chemoreceptor cells. J Physiol 525(Pt 1):135–142
13. Chen X, Talley EM, Patel N, Gomis A, McIntire WE, Dong B, Viana F, Garrison JC, Bayliss DA (2006) Inhibition of a background potassium channel by Gq protein alpha-subunits. Proc Natl Acad Sci U S A 103(9):3422–3427
14. Cotten JF, Keshavaprasad B, Laster MJ, Eger EI 2nd, Yost CS (2006) The ventilatory stimulant doxapram inhibits TASK tandem pore (K2P) potassium channel function but does not affect minimum alveolar anesthetic concentration. Anesth Analg 102(3):779–785
15. Czirjak G, Enyedi P (2002) Formation of functional heterodimers between the TASK-1 and TASK-3 two-pore domain potassium channel subunits. J Biol Chem 277(7):5426–5432
16. Czirjak G, Enyedi P (2002) TASK-3 dominates the background potassium conductance in rat adrenal glomerulosa cells. Mol Endocrinol 16(3):621–629
17. Czirjak G, Enyedi P (2010) TRESK background K (+) channel is inhibited by phosphorylation via two distinct pathways. J Biol Chem 285(19):14549–14557
18. Czirjak G, Fischer T, Spat A, Lesage F, Enyedi P (2000) TASK (TWIK-related acid-sensitive K+ channel) is expressed in glomerulosa cells of rat adrenal cortex and inhibited by angiotensin II. Mol Endocrinol 14(6):863–874
19. Dasso LL, Buckler KJ, Vaughan-Jones RD (1997) Muscarinic and nicotinic receptors raise intracellular Ca2+ levels in rat carotid body type I cells. J Physiol 498(Pt 2):327–338
20. Duprat F, Girard C, Jarretou G, Lazdunski M (2005) Pancreatic two P domain K+ channels TALK-1 and TALK-2 are activated by nitric oxide and reactive oxygen species. J Physiol 562(Pt 1):235–244
21. Enyeart JJ, Danthi SJ, Liu H, Enyeart JA (2005) Angiotensin II inhibits bTREK-1 K+ channels in adrenocortical cells by separate Ca2 + − and ATP hydrolysis-dependent mechanisms. J Biol Chem 280(35):30814–30828
22. Enyeart JJ, Liu H, Enyeart JA (2011) Calcium-dependent inhibition of adrenal TREK-1 channels by angiotensin II and ionomycin. Am J Physiol Cell Physiol 301(3):C619–C629
23. Enyeart JJ, Xu L, Danthi S, Enyeart JA (2002) An ACTH- and ATP-regulated background K+ channel in adrenocortical cells is TREK-1. J Biol Chem 277(51):49186–49199
24. Fagerlund MJ, Kahlin J, Ebberyd A, Schulte G, Mkrtchian S, Eriksson LI (2010) The human carotid body: expression of oxygen sensing and signaling genes of relevance for anesthesia. Anesthesiology 113(6):1270–1279
25. Fearon IM, Zhang M, Vollmer C, Nurse CA (2003) GABA mediates autoreceptor feedback inhibition in the rat carotid body via presynaptic GABAB receptors and TASK-1. J Physiol 553(Pt 1):83–94
26. Fitzgerald RS, Shirahata M, Chang I, Kostuk E (2009) The impact of hypoxia and low glucose on the release of acetylcholine and ATP from the incubated cat carotid body. Brain Res 1270:39–44
27. Fung ML, Lam SY, Chen Y, Dong X, Leung PS (2001) Functional expression of angiotensin II receptors in type-I cells of the rat carotid body. Pflugers Arch 441(4):474–480
28. Gallego-Martin T, Fernandez-Martinez S, Rigual R, Obeso A, Gonzalez C (2012) Effects of low glucose on carotid body chemoreceptor cell activity studied in cultures of intact organs and in dissociated cells. Am J Physiol Cell Physiol 302(8):C1128–C1140
29. Guagliardo NA, Yao J, Bayliss DA, Barrett PQ (2011) TASK channels are not required to mount an aldosterone secretory response to metabolic acidosis in mice. Mol Cell Endocrinol 336(1–2):47–52
30. Han J, Truell J, Gnatenco C, Kim D (2002) Characterization of four types of background potassium channels in rat cerebellar granule neurons. J Physiol 542(Pt 2):431–444
31. Hwang EM, Kim E, Yarishkin O, Woo DH, Han KS, Park N, Bae Y, Woo J, Kim D, Park M, Lee CJ, Park JY (2014) A disulphide-linked heterodimer of TWIK-1 and TREK-1 mediates passive conductance in astrocytes. Nat Commun 5:3227
32. Kang D, Hogan JO, Kim D (2014) THIK-1 (K2P13.1) is a small-conductance background K (+) channel in rat trigeminal ganglion neurons. Pflugers Arch 466(7):1289–1300
33. Kang D, Wang J, Hogan JO, Vennekens R, Freichel M, White C, Kim D (2014) Increase in cytosolic Ca2+ produced by hypoxia and other depolarizing stimuli activates a non-selective cation channel in chemoreceptor cells of rat carotid body. J Physiol 592(Pt 9):1975–1992
34. Kim D (2003) Fatty acid-sensitive two-pore domain K (+) channels. Trends Pharmacol Sci 24(12):648–654
35. Kim D, Cavanaugh EJ, Kim I, Carroll JL (2009) Heteromeric TASK-1/TASK-3 is the major oxygen-sensitive background K+ channel in rat carotid body glomus cells. J Physiol 587(Pt 12):2963–2975
36. Kim D, Gnatenco C (2001) TASK-5, a new member of the tandem-pore K (+) channel family. Biochem Biophys Res Commun 284(4):923–930
37. Kim D, Kim I, Papreck JR, Donnelly DF, Carroll JL (2011) Characterization of an ATP-sensitive K(+) channel in rat carotid body glomus cells. Respir Physiol Neurobiol 177(3):247–255
38. Kim D, Papreck JR, Kim I, Donnelly DF, Carroll JL (2011) Changes in oxygen sensitivity of TASK in carotid body glomus cells during early postnatal development. Respir Physiol Neurobiol 177(3):228–235
39. Koyama Y, Coker RH, Stone EE, Lacy DB, Jabbour K, Williams PE, Wasserman DH (2000) Evidence that carotid bodies play an important role in glucoregulation in vivo. Diabetes 49(9):1434–1442
40. Mathar I, Vennekens R, Meissner M, Kees F, Van der Mieren G, Camacho Londono JE, Uhl S, Voets T, Hummel B, van den Bergh A, Herijgers P, Nilius B, Flockerzi V, Schweda F, Freichel M (2010) Increased catecholamine secretion contributes to hypertension in TRPM4-deficient mice. J Clin Invest 120(9):3267–3279
41. Mathie A (2007) Neuronal two-pore-domain potassium channels and their regulation by G protein-coupled receptors. J Physiol 578(Pt 2):377–385
42. Mkrtchian S, Kahlin J, Ebberyd A, Gonzalez C, Sanchez D, Balbir A, Kostuk EW, Shirahata M, Fagerlund MJ, Eriksson LI (2012) The human carotid body transcriptome with focus on oxygen sensing and inflammation—a comparative analysis. J Physiol 590(Pt 16):3807–3819
43. Mulkey DK, Talley EM, Stornetta RL, Siegel AR, West GH, Chen X, Sen N, Mistry AM, Guyenet PG, Bayliss DA (2007) TASK channels determine pH sensitivity in select respiratory neurons but do not contribute to central respiratory chemosensitivity. J Neurosci 27(51):14049–14058
44. Murali S, Zhang M, Nurse CA (2014) Angiotensin II mobilizes intracellular calcium and activates pannexin-1 channels in rat carotid body type II cells via AT1 receptors. J Physiol 592(Pt 21):4747–4762
45. Musset B, Meuth SG, Liu GX, Derst C, Wegner S, Pape HC, Budde T, Preisig-Muller R, Daut J (2006) Effects of divalent cations and spermine on the K+ channel TASK-3 and on the outward current in thalamic neurons. J Physiol 572(Pt 3):639–657
46. Nurse CA (2014) Synaptic and paracrine mechanisms at carotid body arterial chemoreceptors. J Physiol 592(Pt 16):3419–3426
47. Ortega-Saenz P, Levitsky KL, Marcos-Almaraz MT, Bonilla-Henao V, Pascual A, Lopez-Barneo J (2010) Carotid body chemosensory responses in mice deficient of TASK channels. J Gen Physiol 135(4):379–392
48. Pardal R, Lopez-Barneo J (2002) Low glucose-sensing cells in the carotid body. Nat Neurosci 5(3):197–198
49. Pardal R, Ludewig U, Garcia-Hirschfeld J, Lopez-Barneo J (2000) Secretory responses of intact glomus cells in thin slices of rat carotid body to hypoxia and tetraethylammonium. Proc Natl Acad Sci U S A 97(5):2361–2366
50. Peers C, Wyatt CN (2007) The role of maxiK channels in carotid body chemotransduction. Respir Physiol Neurobiol 157(1):75–82
51. Renigunta V, Fischer T, Zuzarte M, Kling S, Zou X, Siebert K, Limberg MM, Rinne S, Decher N, Schlichthorl G, Daut J (2014) Cooperative endocytosis of the endosomal SNARE protein syntaxin-8 and the potassium channel TASK-1. Mol Biol Cell 25(12):1877–1891
52. Riesco-Fagundo AM, Perez-Garcia MT, Gonzalez C, Lopez-Lopez JR (2001) O(2) modulates large-conductance Ca(2+)-dependent K(+) channels of rat chemoreceptor cells by a membrane-restricted and CO-sensitive mechanism. Circ Res 89(5):430–436
53. Sandoz G, Douguet D, Chatelain F, Lazdunski M, Lesage F (2009) Extracellular acidification exerts opposite actions on TREK1 and TREK2 potassium channels via a single conserved histidine residue. Proc Natl Acad Sci U S A 106(34):14628–14633
54. Schiekel J, Lindner M, Hetzel A, Wemhoner K, Renigunta V, Schlichthorl G, Decher N, Oliver D, Daut J (2013) The inhibition of the potassium channel TASK-1 in rat cardiac muscle by endothelin-1 is mediated by phospholipase C. Cardiovasc Res 97(1):97–105
55. Schwingshackl A, Teng B, Ghosh M, West AN, Makena P, Gorantla V, Sinclair SE, Waters CM (2012) Regulation and function of the two-pore-domain (K2P) potassium channel Trek-1 in alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 302(1):L93–L102
56. Sterni LM, Bamford OS, Tomares SM, Montrose MH, Carroll JL (1995) Developmental changes in intracellular Ca2+ response of carotid chemoreceptor cells to hypoxia. Am J Physiol 268(5 Pt 1):L801–L808
57. Thompson RJ, Farragher SM, Cutz E, Nurse CA (2002) Developmental regulation of O(2) sensing in neonatal adrenal chromaffin cells from wild-type and NADPH-oxidase-deficient mice. Pflugers Arch 444(4):539–548
58. Trapp S, Aller MI, Wisden W, Gourine AV (2008) A role for TASK-1 (KCNK3) channels in the chemosensory control of breathing. J Neurosci 28(35):8844–8850
59. Tse A, Yan L, Lee AK, Tse FW (2012) Autocrine and paracrine actions of ATP in rat carotid body. Can J Physiol Pharmacol 90(6):705–711
60. Turner PJ, Buckler KJ (2013) Oxygen and mitochondrial inhibitors modulate both monomeric and heteromeric TASK-1 and TASK-3 channels in mouse carotid body type-1 cells. J Physiol 591(Pt 23):5977–5998
61. Veale EL, Kennard LE, Sutton GL, MacKenzie G, Sandu C, Mathie A (2007) G(alpha)q-mediated regulation of TASK3 two-pore domain potassium channels: the role of protein kinase C. Mol Pharmacol 71(6):1666–1675
62. Williams BA, Buckler KJ (2004) Biophysical properties and metabolic regulation of a TASK-like potassium channel in rat carotid body type 1 cells. Am J Physiol Lung Cell Mol Physiol 286(1):L221–L230
63. Woo DH, Han KS, Shim JW, Yoon BE, Kim E, Bae JY, Oh SJ, Hwang EM, Marmorstein AD, Bae YC, Park JY, Lee CJ (2012) TREK-1 and Best1 channels mediate fast and slow glutamate release in astrocytes upon GPCR activation. Cell 151(1):25–40
64. Xu F, Xu J, Tse FW, Tse A (2006) Adenosine stimulates depolarization and rise in cytoplasmic [Ca2+] in type I cells of rat carotid bodies. Am J Physiol Cell Physiol 290(6):C1592–C1598
65. Zhang M, Buttigieg J, Nurse CA (2007) Neurotransmitter mechanisms mediating low-glucose signalling in cocultures and fresh tissue slices of rat carotid body. J Physiol 578(Pt 3):735–750
66. Zhang M, Zhong H, Vollmer C, Nurse CA (2000) Co-release of ATP and ACh mediates hypoxic signalling at rat carotid body chemoreceptors. J Physiol 525(Pt 1):143–158
67. Zuzarte M, Heusser K, Renigunta V, Schlichthorl G, Rinne S, Wischmeyer E, Daut J, Schwappach B, Preisig-Muller R (2009) Intracellular traffic of the K+ channels TASK-1 and TASK-3: role of N- and C-terminal sorting signals and interaction with 14-3-3 proteins. J Physiol 587(Pt 5):929–952