Skip to main content

Advertisement

Log in

Dexamethasone-induced up-regulation of two-pore domain K+ channel genes, TASK-1 and TWIK-2, in cultured human periodontal ligament fibroblasts

  • Report
  • Published:
In Vitro Cellular & Developmental Biology - Animal Aims and scope Submit manuscript

Abstract

Two-pore domain K+ channels are widely expressed in many types of cells, and have various important functions, especially maintaining the resting membrane potential. In the previous report, we have confirmed the presence of several kinds of two-pore domain K+ channels in the periodontal ligament (PDL) fibroblasts. It is well known that dexamethasone (Dex) regulates the functions of various kinds of ion channels. In this work, we investigate if Dex affects the gene expressions of the two-pore domain K+ channels in the PDL fibroblasts. We also examined the effects of other steroid hormones on the K+ channels gene expression. The mRNA levels of two-pore domain K+ channels in human PDL fibroblasts were examined in the presence or absence of Dex by RT-PCR. The effects of other steroid hormones (aldosterone, estrogen, 1α,25-dihydroxyvitamin D3 [1,25-(OH)2D3], and retinoic acid) were also examined. Dex significantly induced the expression of TASK-1 and TWIK-2 in mRNA levels in both a dose- and a time-dependent manner. The stimulatory effects of Dex were completely abolished by a glucocorticoid receptor antagonist. 1,25-(OH)2D3 also increased the TASK-1 mRNA levels but had no effect on TWIK-2 expression. Dex, one of the potent glucocorticoid, probably have a protective role against external stimuli by maintaining the membrane potential of PDL fibroblasts through the up-regulation of TASK-1 and TWIK-2 K+ channels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1.
Figure 2.
Figure 3.

Similar content being viewed by others

References

  • Arcari P.; Martinelli R.; Salvatore F. The complete sequence of a full length cDNA for human liver glyceraldehyde-3-phosphate dehydrogenase: evidence for multiple mRNA species. Nucleic Acids Res. 12(23): 9179–9189; 1984.

    Article  PubMed  CAS  Google Scholar 

  • BenMohamed F.; Ferron L.; Ruchon Y.; Gouadon E.; Renaud J. F.; Capuano V. Regulation of T-type Cav3.1 channels expression by synthetic glucocorticoid dexamethasone in neonatal cardiac myocytes. Mol Cell Biochem 320(1-2): 173–183; 2009.

    Article  PubMed  CAS  Google Scholar 

  • Buckingham S. D.; Kidd J. F.; Law R. J.; Franks C. J.; Sattelle D. B. Structure and function of two-pore-domain K+ channels: contributions from genetic model organisms. Trends Pharmacol Sci 26(7): 361–367; 2005.

    Article  PubMed  CAS  Google Scholar 

  • Byers M. R.; Rafie M. M.; Westenbroek R. E. Dexamethasone effects on Nav1.6 in tooth pulp, dental nerves, and alveolar osteoclasts of adult rats. Cell Tissue Res 338(2): 217–226; 2009.

    Article  PubMed  CAS  Google Scholar 

  • Carnes D. L.; Maeder C. L.; Graves D. T. Cells with osteoblastic phenotypes can be explanted from human gingiva and periodontal ligament. J Periodontol 68(7): 701–707; 1997.

    PubMed  CAS  Google Scholar 

  • Chavez R. A.; Gray A. T.; Zhao B. B.; Kindler C. H.; Mazurek M. J.; Mehta Y.; Forsayeth J. R.; Yost C. S. TWIK-2, a new weak inward rectifying member of the tandem pore domain potassium channel family. J Biol Chem 274(12): 7887–7892; 1999.

    Article  PubMed  CAS  Google Scholar 

  • Duprat F.; Lesage F.; Fink M.; Reyes R.; Heurteaux C.; Lazdunski M. TASK, a human background K+ channel to sense external pH variations near physiological pH. EMBO J. 16(17): 5464–5471; 1997.

    Article  PubMed  CAS  Google Scholar 

  • Goldstein S. A.; Bockenhauer D.; O’Kelly I.; Zilberberg N. Potassium leak channels and the KCNK family of two-P-domain subunits. Nat Rev Neurosci 2(3): 175–184; 2001.

    Article  PubMed  CAS  Google Scholar 

  • Hakki S. S.; Hakki E. E.; Nohutcu R. M. Regulation of matrix metalloproteinases and tissue inhibitors of matrix metalloproteinases by basic fibroblast growth factor and dexamethasone in periodontal ligament cells. J Periodontal Res 44(6): 794–802; 2009.

    Article  PubMed  CAS  Google Scholar 

  • Hayami T.; Zhang Q.; Kapila Y.; Kapila S. Dexamethasone’s enhancement of osteoblastic markers in human periodontal ligament cells is associated with inhibition of collagenase expression. Bone 40(1): 93–104; 2007.

    Article  PubMed  CAS  Google Scholar 

  • Holzer P. Taste receptors in the gastrointestinal tract. V. Acid sensing in the gastrointestinal tract. Am J Physiol Gastrointest Liver Physiol 292(3): 699–705; 2007.

    Article  Google Scholar 

  • Inglis S. K.; Brown S. G.; Constable M. J.; McTavish N.; Olver R. E.; Wilson S. M. A Ba2+-resistant, acid-sensitive K+ conductance in Na+-absorbing H441 human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 292(5): 1304–1312; 2007.

    Article  Google Scholar 

  • Kim D.; Fujita A.; Horio Y.; Kurachi Y. Cloning and functional expression of a novel cardiac two-pore background K+ channel (cTBAK-1). Circ. Res. 82(4): 513–518; 1998.

    PubMed  CAS  Google Scholar 

  • Kindler C. H.; Yost C. S. Two-pore domain potassium channels: new sites of local anesthetic action and toxicity. Reg Anesth Pain Med 30(3): 260–274; 2005.

    Article  PubMed  CAS  Google Scholar 

  • Kindler C. H.; Yost C. S.; Gray A. T. Local anesthetic inhibition of baseline potassium channels with two pore domains in tandem. Anesthesiology 90(4): 1092–1102; 1999.

    Article  PubMed  CAS  Google Scholar 

  • Leonoudakis D.; Gray A. T.; Winegar B. D.; Kindler C. H.; Harada M.; Taylor D. M.; Chavez R. A.; Forsayeth J. R.; Yost C. S. An open rectifier potassium channel with two pore domains in tandem cloned from rat cerebellum. J Neurosci 18(3): 868–877; 1998.

    PubMed  CAS  Google Scholar 

  • Lesage F. Pharmacology of neuronal background potassium channels. Neuropharmacology 44(1): 1–7; 2003.

    Article  PubMed  CAS  Google Scholar 

  • Lesage F.; Guillemare E.; Fink M.; Duprat F.; Lazdunski M.; Romey G.; Barhanin J. TWIK-1, a ubiquitous human weakly inward rectifying K+ channel with a novel structure. EMBO J. 15(5): 1004–1011; 1996.

    PubMed  CAS  Google Scholar 

  • Lesage F.; Lazdunski M. Molecular and functional properties of two-pore-domain potassium channels. Am. J. Physiol. Ren. Physiol. 279(5): F793–F801; 2000a.

    CAS  Google Scholar 

  • Lesage F.; Maingret F.; Lazdunski M. Cloning and expression of human TRAAK, a polyunsaturated fatty acids-activated and mechano-sensitive K+ channel. FEBS Lett. 471(2–3): 137–140; 2000b.

    Article  CAS  Google Scholar 

  • Lesage F.; Terrenoire C.; Romey G.; Lazdunski M. Human TREK2, a 2P domain mechano-sensitive K+ channel with multiple regulations by polyunsaturated fatty acids, lysophospholipids, and Gs, Gi, and Gq protein-coupled receptors. J. Biol. Chem. 275(37): 28398–28405; 2000c.

    Article  CAS  Google Scholar 

  • Maingret F.; Patel A. J.; Lazdunski M.; Honoré E. The endocannabinoid anandamide is a direct and selective blocker of the background K+ channel TASK-1. EMBO J 20(1-2): 47–54; 2001.

    Article  PubMed  CAS  Google Scholar 

  • McTavish N.; Getty J.; Burchell A.; Wilson S. M. Glucocorticoids can activate the α-ENaC gene promoter independently of SGK1. Biochem. J. 423(2): 189–197; 2009.

    Article  PubMed  CAS  Google Scholar 

  • Medhurst A. D.; Rennie G.; Chapman C. G.; Meadows H.; Duckworth M. D.; Kelsell R. E.; Gloger I. I.; Pangalos M. N. Distribution analysis of human two pore domain potassium channels in tissues of the central nervous system and periphery. Brain Res Mol Brain Res 86(1-2): 101–114; 2001.

    Article  PubMed  CAS  Google Scholar 

  • Meuth S. G.; Bittner S.; Meuth P.; Simon O. J.; Budde T.; Wiendl H. TWIK-related acid-sensitive K+ channel 1 (TASK1) and TASK3 critically influence T lymphocyte effector functions. J Biol Chem 283(21): 14559–14570; 2008.

    Article  PubMed  CAS  Google Scholar 

  • Nakajima T.; Jo T.; Meguro K.; Oonuma H.; Ma J.; Kubota N.; Imuta H.; Takano H.; Iida H.; Nagase T.; Nagata T. Effect of dexamethasone on voltage-gated Na+ channel in cultured human bronchial smooth muscle cells. Life Sci. 82(23–24): 1210–1215; 2008.

    Article  PubMed  CAS  Google Scholar 

  • Nishikawa M.; Yamaguchi Y.; Yoshitake K.; Saeki Y. Effects of TNFα and prostaglandin E2 on the expression of MMPs in human periodontal ligament fibroblasts. J. Periodontal Res. 37(3): 167–176; 2002.

    Article  PubMed  CAS  Google Scholar 

  • Ogata Y.; Yamauchi M.; Kim R. H.; Li J. J.; Freedman L. P.; Sodek J. Glucocorticoid regulation of bone sialoprotein (BSP) gene expression. Identification of a glucocorticoid response element in the bone sialoprotein gene promoter. Eur J Biochem 230(1): 183–92; 1995.

    Article  PubMed  CAS  Google Scholar 

  • Ohara A.; Saeki Y.; Nishikawa M.; Yamamoto Y.; Yamamoto G. Single-channel recordings of TREK-1 K+ channels in periodontal ligament fibroblasts. J. Dent. Res. 85(7): 664–669; 2006.

    Article  PubMed  CAS  Google Scholar 

  • Patel A. J.; Honoré E. Properties and modulation of mammalian 2P domain K+ channels. Trends Neurosci 24(6): 339–346; 2001.

    Article  PubMed  CAS  Google Scholar 

  • Patel A. J.; Honoré E.; Lesage F.; Fink M.; Romey G.; Lazdunski M. Inhalational anesthetics activate two-pore-domain background K+ channels. Nat Neurosci 2(5): 422–426; 1999.

    Article  PubMed  CAS  Google Scholar 

  • Patel A. J.; Maingret F.; Magnone V.; Fosset M.; Lazdunski M.; Honoré E. TWIK-2, an inactivating 2P domain K+ channel. J Biol Chem 275(37): 28722–28730; 2000.

    Article  PubMed  CAS  Google Scholar 

  • Reyes R.; Duprat F.; Lesage F.; Fink M.; Salinas M.; Farman N.; Lazdunski M. Cloning and expression of a novel pH-sensitive two pore domain K+ channel from human kidney. J. Biol. Chem. 273(47): 30863–30869; 1998.

    Article  PubMed  CAS  Google Scholar 

  • Roy J. W.; Cowley E. A.; Blay J.; Linsdell P. The intermediate conductance Ca2+-activated K+ channel inhibitor TRAM-34 stimulates proliferation of breast cancer cells via activation of oestrogen receptors. Br J Pharmacol 159(3): 650–658; 2010.

    Article  PubMed  CAS  Google Scholar 

  • Saeki Y.; Ohara A.; Nishikawa M.; Yamamoto T.; Yamamoto G. The presence of arachidonic acid-activated K+ channel, TREK-1, in human periodontal ligament fibroblasts. Drug Metab. Rev. 39(2–3): 457–465; 2007.

    Article  PubMed  CAS  Google Scholar 

  • Sanders K. M.; Koh S. D. Two-pore-domain potassium channels in smooth muscles: new components of myogenic regulation. J Physiol 570(Pt 1): 37–43; 2006.

    PubMed  CAS  Google Scholar 

  • Sano Y.; Inamura K.; Miyake A.; Mochizuki S.; Kitada C.; Yokoi H.; Nozawa K.; Okada H.; Matsushime H.; Furuichi K. A novel two-pore domain K+ channel, TRESK, is localized in the spinal cord. J. Biol. Chem. 278(30): 27406–27412; 2003.

    Article  PubMed  CAS  Google Scholar 

  • Sirois J. E.; Lei Q.; Talley E. M.; Lynch C.; Bayliss D. A. The TASK-1 two-pore domain K+ channel is a molecular substrate for neuronal effects of inhalation anesthetics. J Neurosci 20(17): 6347–6354; 2000.

    PubMed  CAS  Google Scholar 

  • Son E. J.; Kim S. H.; Park H. Y.; Kim S. J.; Yoon J. H.; Chung H. P.; Choi J. Y. Activation of epithelial sodium channel in human middle ear epithelial cells by dexamethasone. Eur J Pharmacol 602(2-3): 383–387; 2009.

    Article  PubMed  CAS  Google Scholar 

  • Talley E. M.; Solorzano G.; Lei Q.; Kim D.; Bayliss D. A. Cns distribution of members of the two-pore-domain (KCNK) potassium channel family. J Neurosci 21(19): 7491–7505; 2001.

    PubMed  CAS  Google Scholar 

  • Wei Y.; Zhang C.; Miao X.; Xing F.; Liu X.; Zhao H.; Zhan X.; Han D. Effects of glucocorticoid on cyclic nucleotide-gated channels of olfactory receptor neurons. J. Otolaryngol. Head Neck Surg. 38(1): 90–95; 2009.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Takahiro Yamamoto.

Additional information

Editor: J. Denry Sato

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yamamoto, T., Ohara, A., Nishikawa, M. et al. Dexamethasone-induced up-regulation of two-pore domain K+ channel genes, TASK-1 and TWIK-2, in cultured human periodontal ligament fibroblasts. In Vitro Cell.Dev.Biol.-Animal 47, 273–279 (2011). https://doi.org/10.1007/s11626-011-9388-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11626-011-9388-5

Keywords

Navigation