Menthol increases human glioblastoma intracellular Ca2+, BK channel activity and cell migration

Journal of Biomedical Science - Tập 16 - Trang 1-7 - 2009
Robert Wondergem1, Jeremy W Bartley1
1Department of Physiology, James H Quillen College of Medicine, East Tennessee State University, Johnson City, USA

Tóm tắt

This study examined the effect of menthol, an agonist for transient receptor potential melastatin 8 (TRPM8) ion channels, to increase intracellular Ca2+ concentration, [Ca2+]i, in human glioblastoma cells (DBTRG cells), which resulted in activation of the large-conductance Ca2+-activated K+ membrane ion channels (BK channels). Voltage ramps applied over 300 ms from -100 to 100 mV resulted in membrane currents with marked inwardly- and outwardly-rectifying components. Paxilline (2 μM) abolished the outwardly-rectifying current. Outwardly-rectifying on-cell patch currents were increased markedly by menthol (100 μM) added to the bath. The estimated on-cell conductance of these channels was 253 pS. Kinetic analysis showed that added menthol increased channel open probability and mean open frequency after 5 min. In a similar time course menthol increased [Ca2+]i, and this increase was abolished either by added paxilline, tetraethylammonium ion or by Ca2+-free external solution. Finally, menthol stimulated the rate of DBTRG cell migration into scratch wounds made in confluent cells, and this also was inhibited by paxilline or by tetraethylammonium ion. We conclude that menthol, a TRPM8 agonist, increases DBTRG cell [Ca2+]i that in turn activates membrane BK ion channels. Inhibition of BK channels by paxilline reverses menthol-stimulated increase of [Ca2+]i and of cell migration. Thus, BK channels function to maintain elevations in [Ca2+]i needed to sustain increases in DBTRG cell migration.

Tài liệu tham khảo

Demuth T, Berens ME: Molecular mechanisms of glioma cell migration and invasion. Journal of neuro-oncology. 2004, 70 (2): 217-228. 10.1007/s11060-004-2751-6. Wondergem R, Ecay TW, Mahieu F, Owsianik G, Nilius B: HGF/SF and menthol increase human glioblastoma cell calcium and migration. Biochem Biophys Res Commun. 2008, 372 (1): 210-215. 10.1016/j.bbrc.2008.05.032. Tsavaler L, Shapero MH, Morkowski S, Laus R: Trp-p8, a novel prostate-specific gene, is up-regulated in prostate cancer and other malignancies and shares high homology with transient receptor potential calcium channel proteins. Cancer Res. 2001, 61 (9): 3760-3769. Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, Jordt SE, Julius D: The menthol receptor TRPM8 is the principal detector of environmental cold. Nature. 2007, 448 (7150): 204-208. 10.1038/nature05910. Zhang L, Barritt GJ: Evidence that TRPM8 is an androgen-dependent Ca2+ channel required for the survival of prostate cancer cells. Cancer Res. 2004, 64 (22): 8365-8373. 10.1158/0008-5472.CAN-04-2146. Ransom CB, Sontheimer H: BK channels in human glioma cells. J Neurophysiol. 2001, 85 (2): 790-803. Liu X, Chang Y, Reinhart PH, Sontheimer H, Chang Y: Cloning and characterization of glioma BK, a novel BK channel isoform highly expressed in human glioma cells. J Neurosci. 2002, 22 (5): 1840-1849. Ransom CB, Liu X, Sontheimer H: BK channels in human glioma cells have enhanced calcium sensitivity. Glia. 2002, 38 (4): 281-291. 10.1002/glia.10064. McFerrin MB, Sontheimer H: A role for ion channels in glioma cell invasion. Neuron Glia Biol. 2006, 2 (1): 39-49. 10.1017/S1740925X06000044. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ: Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981, 391 (2): 85-100. 10.1007/BF00656997. Vriens J, Janssens A, Prenen J, Nilius B, Wondergem R: TRPV channels and modulation by hepatocyte growth factor/scatter factor in human hepatoblastoma (HepG2) cells. Cell Calcium. 2004, 36 (1): 19-28. 10.1016/j.ceca.2003.11.006. Knaus HG, McManus OB, Lee SH, Schmalhofer WA, Garcia-Calvo M, Helms LM, Sanchez M, Giangiacomo K, Reuben JP, Smith AB: Tremorgenic indole alkaloids potently inhibit smooth muscle high-conductance calcium-activated potassium channels. Biochemistry. 1994, 33 (19): 5819-5828. 10.1021/bi00185a021. Strobaek D, Christophersen P, Holm NR, Moldt P, Ahring PK, Johansen TE, Olesen SP: Modulation of the Ca(2+)-dependent K+ channel, hslo, by the substituted diphenylurea NS paxilline and internal Ca2+. Neuropharmacology. 1996, 35 (7): 903-914. 10.1016/0028-3908(96)00096-2. Hille B: Ionic channels of excitable membranes. 2001, Sunderland, M.A., U.S.A.: Sinauer Associates, Inc, Third Bilmen JG, Wootton LL, Michelangeli F: The mechanism of inhibition of the sarco/endoplasmic reticulum Ca2+ ATPase by paxilline. Archives of biochemistry and biophysics. 2002, 406 (1): 55-64. 10.1016/S0003-9861(02)00240-0. Longland CL, Dyer JL, Michelangeli F: The mycotoxin paxilline inhibits the cerebellar inositol 1,4, 5-trisphosphate receptor. European journal of pharmacology. 2000, 408 (3): 219-225. 10.1016/S0014-2999(00)00775-5. Clapham DE: Calcium signaling. Cell. 2007, 131 (6): 1047-1058. 10.1016/j.cell.2007.11.028. Monteith GR, McAndrew D, Faddy HM, Roberts-Thomson SJ: Calcium and cancer: targeting Ca2+ transport. Nature reviews. 2007, 7 (7): 519-530. 10.1038/nrc2171. Weaver AK, Bomben VC, Sontheimer H: Expression and function of calcium-activated potassium channels in human glioma cells. Glia. 2006, 54 (3): 223-233. 10.1002/glia.20364. Adelman JP, Shen KZ, Kavanaugh MP, Warren RA, Wu YN, Lagrutta A, Bond CT, North RA: Calcium-activated potassium channels expressed from cloned complementary DNAs. Neuron. 1992, 9 (2): 209-216. 10.1016/0896-6273(92)90160-F. Koochekpour S, Jeffers M, Rulong S, Taylor G, Klineberg E, Hudson EA, Resau JH, Woude Vande GF: Met and hepatocyte growth factor/scatter factor expression in human gliomas. Cancer Res. 1997, 57 (23): 5391-5398. Bezzerides VJ, Ramsey IS, Kotecha S, Greka A, Clapham DE: Rapid vesicular translocation and insertion of TRP channels. Nat Cell Biol. 2004, 6 (8): 709-720. 10.1038/ncb1150. Bidaux G, Flourakis M, Thebault S, Zholos A, Beck B, Gkika D, Roudbaraki M, Bonnal JL, Mauroy B, Shuba Y: Prostate cell differentiation status determines transient receptor potential melastatin member 8 channel subcellular localization and function. J Clin Invest. 2007, 117 (6): 1647-1657. 10.1172/JCI30168. Yang S, Zhang JJ, Huang XY: Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer cell. 2009, 15 (2): 124-134. 10.1016/j.ccr.2008.12.019. Fakler B, Adelman JP: Control of K(Ca) channels by calcium nano/microdomains. Neuron. 2008, 59 (6): 873-881. 10.1016/j.neuron.2008.09.001. Weaver AK, Olsen ML, McFerrin MB, Sontheimer H: BK channels are linked to inositol 1,4,5-triphosphate receptors via lipid rafts: a novel mechanism for coupling [Ca(2+)](i) to ion channel activation. J Biol Chem. 2007, 282 (43): 31558-31568. 10.1074/jbc.M702866200. Kraft R, Krause P, Jung S, Basrai D, Liebmann L, Bolz J, Patt S: BK channel openers inhibit migration of human glioma cells. Pflugers Arch. 2003, 446 (2): 248-255. Schwab A: Function and spatial distribution of ion channels and transporters in cell migration. Am J Physiol Renal Physiol. 2001, 280 (5): F739-747.