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Coupled Activation of Mechanosensitive and Calcium-Dependent Potassium Channels in 3T3 and 3T3-SV40 Cells

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Abstract

Using the patch–clamp method, mechanosensitive regulation of ion channels was studied in cultivated 3T3 and 3T3-SV40 fibroblasts. The activity of mechanosensitive cation channels with a conductivity 25 pS in response to plasma-membrane stretching was observed in both cell lines. Despite obvious differences in the actin network in normal and transformed cells, the threshold values of the stimulus required for the channel activation were close and were approximately 55 mm Hg. The frequency of channels was significantly higher in transformed 3T3-SV40 fibroblasts than in their untransformed 3T3 analogs. Coupled activation of mechanosensitive calcium-permeable channels and potassium calcium-controlled channels was found in both cell lines. The analysis of flows through single channels allows to detect functional interaction of different channels: stretch-induced local calcium entry activates potassium channels that do not have their own mechanosensitivity. The results of a comparative study show that there is a fundamental similarity between the ion mechanisms of cellular mechanotransduction in normal and transformed fibroblasts. The quantitative differences, first of all, concern the level of functional activity of mechanosensitive channels that provide the development of the local calcium signal in the near-membrane cell region.

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References

  • Arnadottir, J. and Chalfie, M., Eukaryotic mechanosensitive channels, Annu. Rev. Biophys., 2010, vol. 39, pp. 111–137.

    Article  PubMed  CAS  Google Scholar 

  • Chubinskiy-Nadezhdin, V.I., Functional coupling of ion channels as universal mechanism of cellular mechanotransduction, Acta Naturae, special issue, 2016, vol. 1, pp. 71–72.

    Google Scholar 

  • Chubinskiy-Nadezhdin, V.I., Negulyaev, Y.A., and Morachevskaya, E.A., Cholesterol depletion-induced inhibition of stretch-activated channels is mediated via actin rearrangement, Biochem. Biophys. Res. Commun., 2011, vol. 412, pp. 80–85.

    Article  PubMed  CAS  Google Scholar 

  • Chubinskiy-Nadezhdin, V.I., Nyapshaev, I.A., Morachevskaya, E.A., and Ankudinov, A.V., Evaluation of the changes of plasma membrane stiffness after partial extraction of membrane cholesterol, Tsitologiia, 2012, vol. 54, no. 9, pp. 714–715.

    Google Scholar 

  • Chubinskiy-Nadezhdin, V.I., Negulyaev, Y.A., and Morachevskaya, E.A., Functional coupling of ion channels in cellular mechanotransduction, Biochem. Biophys. Res. Commun., 2014, vol. 451, pp. 421–424.

    Article  PubMed  CAS  Google Scholar 

  • Chubinskiy-Nadezhdin V.I., Vasileva, V.Y., Pugovkina, N.A., Vassilieva, I.O., Morachevskaya, E.A., Nikolsky, N.N., and Negulyaev, Y.A., Local calcium signalling is mediated by mechanosensitive ion channels in mesenchymal stem cells, Biochem. Biophys. Res. Commun., 2017, vol. 482, pp. 563–568.

    Article  PubMed  CAS  Google Scholar 

  • Coste, B., Mathur, J., Schmidt, M., Earley, T.J., Ranade, S., Petrus, M.J., Dubin, A.E., and Patapoutian, A., Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels, Science, 2010, vol. 330, pp. 55–60.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Franco, S.J. and Huttenlocher, A., Regulating cell migration: calpains make the cut, J. Cell Sci., 2005, vol. 118, pp. 3829–3838.

    Article  PubMed  CAS  Google Scholar 

  • Gilbert G., Ducret, T., Marthan, R., Savineau, J.P., and Quignard, J.F., Stretch-induced Ca2+ signalling in vascular smooth muscle cells depends on Ca2+ store segregation, Cardiovasc. Res., 2014, vol. 103, pp. 313–323.

    Article  PubMed  CAS  Google Scholar 

  • Gueguinou, M., Chantome, A., Fromont, G., Bougnoux, P., Vandier, C., and Potier-Cartereau, M., KCa and Ca2+ channels: the complex thought, Biochim. Biophys. Acta, 2014, vol. 1843, pp. 2322–2333.

    Article  PubMed  CAS  Google Scholar 

  • Lee, J., Ishihara, A., Oxford, G., Johnson, B., and Jacobson, K., Regulation of cell movement is mediated by stretch-activated calcium channels, Nature, 1999, vol. 400, pp. 382–386.

    Article  PubMed  CAS  Google Scholar 

  • Li, C., Rezania, S., Kammerer, S., Sokolowski, A., Devaney, T., Gorischek, A., Jahn, S., Hackl, H., Groschner, K., Windpassinger, C., Malle, E., Bauernhofer, T., and Schreibmayer, W., Piezo1 forms mechanosensitive ion channels in the humanMCF-7 breast cancer cell line, Sci. Rep., 2015, vol. 5, p. 8364. doi doi 10.1038/srep08364

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mamoune, A., Luo, J.H., Lauffenberger, D.A., and Wells, A., Calpain-2 as a target for limiting prostate cancer invasion, Cancer Res., 2003, vol. 63, pp. 4632–4640.

    PubMed  CAS  Google Scholar 

  • Maroto, R. and Hamill, O.P., MscCa regulation of tumor cell migration and metastasis, in Mechanosensitive Channels. B: Current Topics in Membranes, New York: Academic Press, 2007, pp. 485–509.

    Book  Google Scholar 

  • McHugh, B.J., Murdoch, A., Haslett, C., and Sethi, T., Loss of integrin-activating transmembrane protein FAM38A (Piezo1) promotes a switch to integrin-independent mode of cell migration, PloS One, 2012, vol. 7, p. e40346.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Morachevskaya, E.A., Sudarikova, A.V., and Negulyaev, Y.A., Mechanosensitive channel activity and Factin organization in cholesterol-depleted human leukaemia cells, Cell Biol. Int., 2007, vol. 31, pp. 374–381.

    Article  PubMed  CAS  Google Scholar 

  • Rovenskii, Yu.A. and Vasil’ev, Yu.M., Morphogenetic reactions of cells and their disturbances in malignant transformation, in Kantserogenez (Carcinogenesis), Moscow: Meditsina, 2004, pp. 376–414.

    Google Scholar 

  • Staruschenko A.V. and Vedernikova E.A., Mechanosensitive cation channels in human leukaemia cells: calcium permeation and blocking effect, J. Physiol., 2002, vol. 541, pp. 81–90.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Staruschenko A.V., Negulyaev, Y.A., and Morachevskaya, E.A., Actin cytoskeleton disassembly affects conductive properties of stretch-activated cation channels in leukaemia cells, Biochim. Biophys. Acta, 2005, vol. 1669, pp. 53–60.

    Article  PubMed  CAS  Google Scholar 

  • Staruschenko, A.V., Sudarikova, A.V., Negulyaev, Y.A., and Morachevskaya, E.A., Magnesium permeation through mechanosensitive channels: single-current measurements, Cell Res., 2006, vol. 16, pp. 723–730.

    Article  PubMed  CAS  Google Scholar 

  • Suresh, S., Biomechanics and biophysics of cancer cells, Acta Biomater., 2007, vol. 3, pp. 413–438.

    Article  PubMed  PubMed Central  Google Scholar 

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Correspondence to V. I. Chubinskiy-Nadezhdin.

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Original Russian Text © V.I. Chubinskiy-Nadezhdin, T.N. Efremova, Yu.A. Negulyaev, E.A. Morachevskaya, 2018, published in Tsitologiya, 2018, Vol. 60, No. 1, pp. 14–20.

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Chubinskiy-Nadezhdin, V.I., Efremova, T.N., Negulyaev, Y.A. et al. Coupled Activation of Mechanosensitive and Calcium-Dependent Potassium Channels in 3T3 and 3T3-SV40 Cells. Cell Tiss. Biol. 12, 231–237 (2018). https://doi.org/10.1134/S1990519X18030021

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  • DOI: https://doi.org/10.1134/S1990519X18030021

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