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Sphingosine-1-phosphate induces Ca2+ mobilization via TRPC6 channels in SH-SY5Y cells and hippocampal neurons

  • 1.

    School of Basic Medical Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei 230026, China

  • 2.

    Institute on Aging and Brain Disorders, the First Affiliated Hospital of USTC, University of Science and Technology of China, Hefei 230036, China

Cite this:
https://doi.org/10.52396/JUSTC-2022-0014
More Information
  • Author Bio:

    Haotian Wu is currently a master’s student at the School of Basic Medical Sciences, University of Science and Technology of China, under the supervision of Prof. Chunlei Cang. His research mainly focuses on ion channels and ion homeostasis in cells and organelles

    Lili Qu received her Ph.D. degree in Neurobiology from Fudan University. She is currently an associate researcher at the University of Science and Technology of China. Her research interests include organelles and neurodegenerative diseases

    Chunlei Cang received his Ph.D. degree in Neurobiology from Fudan University. He is currently a Professor at the University of Science and Technology of China. His research interests include ion channels, organellar physiology and function, aging and neurodegenerative diseases

  • Corresponding author: E-mail: lilisqu@ustc.edu.cn; E-mail: ccang@ustc.edu.cn
  • Received Date: 20 January 2022
  • Accepted Date: 18 May 2022
    Abstract

  • Abstract

    Sphingosine-1-phosphate (S1P) is a widely expressed biologically active sphingolipid that plays an important role in cell differentiation, migration, proliferation, metabolism and apoptosis. S1P activates various signaling pathways, some of which evoke Ca2+ signals in the cytosol. Few studies have focused on the mechanism by which S1P evokes Ca2+ signals in neurons. Here, we show that S1P evokes global Ca2+ signals in SH-SY5Y cells and hippocampal neurons. Removal of extracellular calcium largely abolished the S1P-induced increase in intracellular Ca2+, suggesting that the influx of extracellular Ca2+ is the major contributor to this process. Moreover, we found that S1P-induced Ca2+ mobilization is independent of G protein-coupled S1P receptors. The TRPC6 inhibitor SAR7334 suppressed S1P-induced calcium signals, indicating that the TRPC6 channel acts as the downstream effector of S1P. Using patch-clamp recording, we showed that S1P activates TRPC6 currents. Two Src tyrosine kinase inhibitors, Src-I1 and PP2, dramatically inhibited the activation of TRPC6 by S1P. Taken together, our data suggest that S1P activates TRPC6 channels in a Src-dependent way to induce Ca2+ mobilization in SH-SY5Y cells and hippocampal neurons.

    Graphical abstract

    S1P activates TRPC6 in a Src-dependent way to induce Ca2+ mobilization in SH-SY5Y cells and hippocampal neurons.

    Abstract

    Sphingosine-1-phosphate (S1P) is a widely expressed biologically active sphingolipid that plays an important role in cell differentiation, migration, proliferation, metabolism and apoptosis. S1P activates various signaling pathways, some of which evoke Ca2+ signals in the cytosol. Few studies have focused on the mechanism by which S1P evokes Ca2+ signals in neurons. Here, we show that S1P evokes global Ca2+ signals in SH-SY5Y cells and hippocampal neurons. Removal of extracellular calcium largely abolished the S1P-induced increase in intracellular Ca2+, suggesting that the influx of extracellular Ca2+ is the major contributor to this process. Moreover, we found that S1P-induced Ca2+ mobilization is independent of G protein-coupled S1P receptors. The TRPC6 inhibitor SAR7334 suppressed S1P-induced calcium signals, indicating that the TRPC6 channel acts as the downstream effector of S1P. Using patch-clamp recording, we showed that S1P activates TRPC6 currents. Two Src tyrosine kinase inhibitors, Src-I1 and PP2, dramatically inhibited the activation of TRPC6 by S1P. Taken together, our data suggest that S1P activates TRPC6 channels in a Src-dependent way to induce Ca2+ mobilization in SH-SY5Y cells and hippocampal neurons.

    • Public Summary

    • Sphingosine-1-phosphate (S1P) evokes global Ca2+ signals in neurons.
    • TRPC6 channels mediate S1P-induced Ca2+ influx in SH-SY5Y cells and hippocampal neurons.
    • S1P activates TRPC6 channels in a Src-dependent manner.

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    • References(50)
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    Figure  1.  S1P evokes Ca2+ signals in SH-SY5Y cells. (a, b) Representative pseudocolor images of the Fura-2 AM fluorescence ratio (F340/F380) responding to vehicle (a) and 10 μmol/L S1P (b) in SH-SY5Y cells. (c) Changes in the F340/F380 ratio (ΔRatio) of cells induced by vehicle or S1P. (d, e) Representative F340/F380 ratios of SH-SY5Y cells in response to vehicle (d) or 10 µmol/L S1P (e). (f) Percentage of cells responding to the application of vehicle or S1P (ΔRatio > 0.2). Scale bar = 10 μm. The data are presented as the means ± SEMs. ***P < 0.001.

    Figure  2.  S1P induces the influx of extracellular Ca2+. (a) Representative pseudocolor images of F340/F380 in SH-SY5Y cells before and after the application of 10 μmol/L S1P in Ca2+-containing (left) and Ca2+-free (right) bath solution. (b) Representative traces of calcium signals responding to 10 μmol/L S1P treatment under Ca2+-containing (upper) and Ca2+-free (lower) conditions. (c) Statistics of the ΔRatio (F340/F380; upper) and percentage of responding cells (ΔRatio > 0.2) shown in (a) and (b). (d) Representative pseudocolor images of the F340/F380 ratio in SH-SY5Y cells treated with 100 μmol/L 2-APB (upper) or 100 μmol/L 2-APB + 10 μmol/L S1P (lower) in Ca2+-containing (left) and Ca2+-free (right) solution. (e) Representative F340/F380 ratios of SH-SY5Y cells in response to 100 μmol/L 2-APB + 10 μmol/L S1P in Ca2+ (upper) and Ca2+-free (lower) solution. (f) Statistics of the ΔRatio (F340/F380; upper) and percentage of responding cells (ΔRatio > 0.2) shown in (d) and (e). Scale bar = 10 μm. The data are presented as the means ± SEMs. *P < 0.05, **P < 0.01, ***P < 0.001.

    Figure  3.  The S1P-induced Ca2+ response is independent of G-protein coupled S1P receptors. (a) Representative pseudocolor images of F340/F380 in SH-SY5Y cells preincubated with the indicated antagonists and treated with 10 μmol/L S1P. (b) Representative traces of calcium signals responding to 10 μmol/L S1P treatment in SH-SY5Y cells incubated with the indicated antagonists. (c) Statistics of the ΔRatio (F340/F380). (d) Statistics of the percentage of responding cells. Scale bar = 10 μm. The data are presented as the means ± SEMs. *P < 0.05, ***P < 0.001. NS indicates no significant difference.

    Figure  4.  S1P-induced Ca2+ response is independent of the transactivation of EGFR. (a) Representative pseudocolor images of F340/F380 in SH-SY5Y cells preincubated with 1 μmol/L AG1478 and treated with 10 μmol/L S1P. (b) Representative traces of calcium signals responding to 10 μmol/L S1P treatment in SH-SY5Y cells incubated with 1 μmol/L AG1478. (c) Statistics of the ΔRatio (F340/F380) and statistics of the percentage of responding cells. Scale bar = 10 μm. The data are presented as the means ± SEMs. NS indicates no significant difference.

    Figure  5.  S1P induces calcium signals in high-K+ solution and Na+-free solution. (a) Representative pseudocolor images of F340/F380 showing the S1P-induced calcium signals in SH-SY5Y cells with low-K+ (5.4 mmol/L; upper), high-K+ (100 mmol/L; middle) or Na+-free (lower) solution treatment. (b) Representative traces of calcium signals responding to low-K+ (upper), high-K+ (middle) or Na+-free (lower) treatment in SH-SY5Y cells. (c) Statistics of the ΔRatio (F340/F380; upper) and percentage of responding cells (ΔRatio > 0.2; lower) shown in (a) and (b). Scale bar = 10 μm. The data are presented as the means ± SEMs. *P < 0.05. NS indicates no significant difference.

    Figure  6.  S1P-induced Ca2+ mobilization is mediated by the TRPC6 channel in both SH-SY5Y cells and hippocampal neurons. (a) Representative pseudocolor images of F340/F380 showing the S1P-induced calcium signals in SH-SY5Y cells preincubated with vehicle (left) or 1 μmol/L SAR7334 (right). (b) Representative traces of calcium signals responding to 10 μmol/L S1P treatment in SH-SY5Y cells preincubated with vehicle (upper) or 1 μmol/L SAR7334 (lower). (c) Statistics of the ΔRatio (F340/F380; upper) and percentage of responding cells (ΔRatio > 0.2) shown in (a) and (b). (d) Representative pseudocolor images of F340/F380 showing the S1P-induced calcium signals in hippocampal neurons preincubated with vehicle (left) or 0.1 μmol/L SAR7334 (right). (e) Representative traces of calcium signals responding to 10 μmol/L S1P treatment in hippocampal neurons preincubated with vehicle (upper) or 0.1 μmol/L SAR7334 (lower). (f) Statistics of the ΔRatio (F340/F380; upper) and percentage of responding cells (ΔRatio > 0.2) shown in (c) and (d). Scale bar = 10 μm. The data are presented as the means ± SEMs. **P < 0.01, ***P < 0.001.

    Figure  7.  Reconstitution of the TRPC6 current in HEK293T cells. (a, b) Representative whole-cell currents recorded in HEK293T cells transfected with empty vector (a) or TRPC6 (b). The currents were elicited with ramp protocols (−100 mV to +100 mV in 1 s). (c) Current amplitudes measured at +100 mV. (d) Representative currents recorded using whole-cell patch-clamp in TRPC6-transfected HEK293T cells at different time points after the start of recording. (e, f) Stability of the currents under whole-cell patch-clamp mode (e) or perforated patch-clamp mode (f). The current amplitudes (measured at +100 mV) at different time points were normalized to the values at the start of recordings. The data are presented as the means ± SEMs. ***P < 0.001.

    Figure  8.  S1P activates TRPC6 in a Src-dependent manner. (a–l) Perforated patch-clamp recordings were performed in HEK293T cells transfected with empty vector (a–c) or TRPC6 (d–i). Cells used in (g–l) were treated with 2 μmol/L Src-I1 (g–i) or 1 μmol/L PP2 (j–l) for 10 min before recording. (a, d, g, and j) Representative currents recorded with ramp protocols (−100 to +100 mV in 1 s). (b, e, h, and k) Representative currents recorded with step protocols (250 ms step pulses from −100 to +100 mV, 10 mV step; Vh = 0 mV). (c, f, i, and l) Amplitudes of the inward and outward currents shown in (a), (d), (g), and (j), respectively. The data are presented as the means ± SEMs. *P < 0.05. NS indicates no significant difference.

    [1]
    Dixit D, Okuniewska M, Schwab S R. Secrets and lyase: Control of sphingosine 1-phosphate distribution. Immunol. Rev., 2019, 289 (1): 173–185. doi: 10.1111/imr.12760
    [2]
    Książek M, Chacińska M, Chabowski A, et al. Sources, metabolism, and regulation of circulating sphingosine-1-phosphate. J. Lipid Res., 2015, 56 (7): 1271–1281. doi: 10.1194/jlr.R059543
    [3]
    Spiegel S, Milstien S. Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat. Rev. Mol. Cell Biol., 2003, 4 (5): 397–407. doi: 10.1038/nrm1103
    [4]
    Nagahashi M, Takabe K, Terracina K P, et al. Sphingosine-1-phosphate transporters as targets for cancer therapy. Biomed Res. Int., 2014, 2014: 651727. doi: 10.1155/2014/651727
    [5]
    Chun J, Hla T, Lynch K R, et al. International Union of Basic and Clinical Pharmacology. LXXVIII. Lysophospholipid receptor nomenclature. Pharmacol. Rev., 2010, 62 (4): 579–587. doi: 10.1124/pr.110.003111
    [6]
    Hait N C, Oskeritzian C A, Paugh S W, et al. Sphingosine kinases, sphingosine 1-phosphate, apoptosis and diseases. Biochim. Biophys. Acta, 2006, 1758 (12): 2016–2026. doi: 10.1016/j.bbamem.2006.08.007
    [7]
    Ng M L, Yarla N S, Menschikowski M, et al. Regulatory role of sphingosine kinase and sphingosine-1-phosphate receptor signaling in progenitor/stem cells. World J. Stem Cells, 2018, 10 (9): 119–133. doi: 10.4252/wjsc.v10.i9.119
    [8]
    Sukocheva O A. Expansion of sphingosine kinase and sphingosine-1-phosphate receptor function in normal and cancer cells: From membrane restructuring to mediation of estrogen signaling and stem cell programming. Int. J. Mol. Sci., 2018, 19 (2): 420. doi: 10.3390/ijms19020420
    [9]
    Birchwood C J, Saba J D, Dickson R C, et al. Calcium influx and signaling in yeast stimulated by intracellular sphingosine 1-phosphate accumulation. J. Biol. Chem., 2001, 276 (15): 11712–11718. doi: 10.1074/jbc.M010221200
    [10]
    Pulli I, Asghar M Y, Kemppainen K, et al. Sphingolipid-mediated calcium signaling and its pathological effects. Biochim. Biophys. Acta Mol. Cell Res., 2018, 1865 (11 Pt B): 1668–1677. doi: 10.1016/j.bbamcr.2018.04.012
    [11]
    Putney J W, Tomita T. Phospholipase C signaling and calcium influx. Adv. Biol. Regul., 2012, 52 (1): 152–164. doi: 10.1016/j.advenzreg.2011.09.005
    [12]
    Meyer zu Heringdorf D, Liliom K, Schaefer M, et al. Photolysis of intracellular caged sphingosine-1-phosphate causes Ca2+ mobilization independently of G-protein-coupled receptors. FEBS Lett., 2003, 554 (3): 443–449. doi: 10.1016/S0014-5793(03)01219-5
    [13]
    Ghosh T K, Bian J, Gill D L. Intracellular calcium release mediated by sphingosine derivatives generated in cells. Science, 1990, 248 (4963): 1653–1656. doi: 10.1126/science.2163543
    [14]
    Berridge M J. Neuronal calcium signaling. Neuron, 1998, 21 (1): 13–26. doi: 10.1016/S0896-6273(00)80510-3
    [15]
    Grassi S, Mauri L, Prioni S, et al. Sphingosine 1-phosphate receptors and metabolic enzymes as druggable targets for brain diseases. Front. Pharmacol., 2019, 10: 807. doi: 10.3389/fphar.2019.00807
    [16]
    Shirakawa H, Katsumoto R, Iida S, et al. Sphingosine-1-phosphate induces Ca2+ signaling and CXCL1 release via TRPC6 channel in astrocytes. Glia, 2017, 65 (6): 1005–1016. doi: 10.1002/glia.23141
    [17]
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