Abstract
Glomus cells isolated from rabbit and rat/mouse carotid bodies have been used for many years to study the role of ion channels in hypoxia sensing. Studies show that hypoxia inhibits the inactivating K+ channels (Kv4) in rabbits, but inhibits TASK in rats/mice to elicit the hypoxic response. Because the role of TASK in rabbit glomus cells is not known, we isolated glomus cells from rabbits and studied the expression of TASK mRNA in the whole carotid body (CB), changes in [Ca2+]i and TASK activity. RT-PCR showed that rabbit CB expressed mRNA for TASK-3 and several Kv (Kv2.1, Kv3.1 and Kv3.3). In rabbit glomus cells in which 20 mM KClo elevated [Ca2+], anoxia also elicited a strong rise in [Ca2+]. In cell-attached patches with 140 mM KCl in the pipette, basal openings of ion channels with single-channel conductance levels of 16-pS, 34-pS, and 42-pS were present. TREK-like channels were also observed. In inside-out patches with high [Ca2+]i, BK was activated. The 42-pS channel opened spontaneously and briefly. The 16-pS and 34-pS channels showed properties similar to those of TASK-1 and TASK-3, respectively. TASK activity in cell-attached patches was lower than that in rat glomus cells under identical recording conditions. Hypoxia (~0.5%O2) reduced TASK activity by ~52% and depolarized the cells by ~30 mV. Our results show that the O2-sensitive TASK contributes to the hypoxic response in rabbit glomus cells.
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Biscoe TJ, Duchen MR, Eisner DA et al (1989) Measurements of intracellular Ca2+ in dissociated type I cells of the rabbit carotid body. J Physiol 416:421–434
Buckler KJ (2015) TASK channels in arterial chemoreceptors and their role in oxygen and acid sensing. Pflugers Arch 467(5):1013–1025
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
Chen J, He L, Dinger B et al (2000) Cellular mechanisms involved in rabbit carotid body excitation elicited by endothelin peptides. Respir Physiol 121(1):13–23
Delpiano MA, Hescheler J (1989) Evidence for a PO2-sensitive K+ channel in the type-I cell of the rabbit carotid body. FEBS Lett 249(2):195–198
Fagerlund MJ, Kahlin J, Ebberyd A et al (2010) The human carotid body: expression of oxygen sensing and signaling genes of relevance for anesthesia. Anesthesiology 113(6):1270–1279
Ganfornina MD, Lopez-Barneo J (1991) Single K+ channels in membrane patches of arterial chemoreceptor cells are modulated by O2 tension. Proc Natl Acad Sci U S A 88(7):2927–2930
Ganfornina MD, Lopez-Barneo J (1992) Potassium channel types in arterial chemoreceptor cells and their selective modulation by oxygen. J Gen Physiol 100(3):401–426
Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260(6):3440–3450
Kang D, Han J, Talley EM et al (2004) Functional expression of TASK-1/TASK-3 heteromers in cerebellar granule cells. J Physiol 554(Pt 1):64–77
Kang D, Wang J, Hogan JO et al (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
Kim D (2013) K(+) channels in O(2) sensing and postnatal development of carotid body glomus cell response to hypoxia. Respir Physiol Neurobiol 185(1):44–56
Kim D, Cavanaugh EJ, Kim I et al (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
Kobayashi N, Yamamoto Y (2010) Hypoxic responses of arterial chemoreceptors in rabbits are primarily mediated by leak K channels. Adv Exp Med Biol 669:195–199
Lopez-Barneo J, Lopez-Lopez JR, Urena J et al (1988) Chemotransduction in the carotid body: K+ current modulated by PO2 in type I chemoreceptor cells. Science 241(4865):580–582
Lopez-Lopez J, Gonzalez C, Urena J et al (1989) Low pO2 selectively inhibits K+ channel activity in chemoreceptor cells of the mammalian carotid body. J Gen Physiol 93(5):1001–1015
Mkrtchian S, Kahlin J, Ebberyd A et al (2012) The human carotid body transcriptome with focus on oxygen sensing and inflammation--a comparative analysis. J Physiol 590(16):3807–3819
Montoro RJ, Urena J, Fernandez-Chacon R et al (1996) Oxygen sensing by ion channels and chemotransduction in single glomus cells. J Gen Physiol 107(1):133–143
Oliver D, Lien CC, Soom M et al (2004) Functional conversion between A-type and delayed rectifier K+ channels by membrane lipids. Science 304(5668):265–270
Perez-Garcia MT, Lopez-Lopez JR, Riesco AM et al (2000) Viral gene transfer of dominant-negative Kv4 construct suppresses an O2-sensitive K+ current in chemoreceptor cells. J Neurosci 20(15):5689–5695
Rocher A, Geijo-Barrientos E, Caceres AI et al (2005) Role of voltage-dependent calcium channels in stimulus-secretion coupling in rabbit carotid body chemoreceptor cells. J Physiol 562(Pt 2):407–420
Sanchez D, Lopez-Lopez JR, Perez-Garcia MT et al (2002) Molecular identification of Kvalpha subunits that contribute to the oxygen-sensitive K+ current of chemoreceptor cells of the rabbit carotid body. J Physiol 542(Pt 2):369–382
Schultz HD, Marcus NJ, Del Rio R (2013) Role of the carotid body in the pathophysiology of heart failure. Curr Hypertens Rep 15(4):356–362
Acknowledgements
This work was supported by funds from NIH, Rosalind Franklin University, and the Ministry of Science, ICT and Future Planning (NRF-2015R1A5A2008833, Korea).
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Kang, D., Wang, J., Hogan, J.O., Kim, D. (2018). TASK-1 (K2P3) and TASK-3 (K2P9) in Rabbit Carotid Body Glomus Cells. In: Gauda, E., Monteiro, M., Prabhakar, N., Wyatt, C., Schultz, H. (eds) Arterial Chemoreceptors. Advances in Experimental Medicine and Biology, vol 1071. Springer, Cham. https://doi.org/10.1007/978-3-319-91137-3_4
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DOI: https://doi.org/10.1007/978-3-319-91137-3_4
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