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Cell Membrane Transport Mechanisms: Ion Channels and Electrical Properties of Cell Membranes

  • Julita Kulbacka
  • Anna Choromańska
  • Joanna Rossowska
  • Joanna Weżgowiec
  • Jolanta Saczko
  • Marie-Pierre Rols
Chapter
Part of the Advances in Anatomy, Embryology and Cell Biology book series (ADVSANAT, volume 227)

Abstract

Cellular life strongly depends on the membrane ability to precisely control exchange of solutes between the internal and external (environmental) compartments. This barrier regulates which types of solutes can enter and leave the cell. Transmembrane transport involves complex mechanisms responsible for passive and active carriage of ions and small- and medium-size molecules. Transport mechanisms existing in the biological membranes highly determine proper cellular functions and contribute to drug transport. The present chapter deals with features and electrical properties of the cell membrane and addresses the questions how the cell membrane accomplishes transport functions and how transmembrane transport can be affected. Since dysfunctions of plasma membrane transporters very often are the cause of human diseases, we also report how specific transport mechanisms can be modulated or inhibited in order to enhance the therapeutic effect.

Notes

Acknowledgments

This work was supported by the Polish National Science Centre project SONATA BIS 6 - SONB.A040.17.001 (2016/22/E/NZ5/00671).

References

  1. Abdallah HM, Al-Abd AM, El-Dine RS, El-Halawany AM (2015) P-glycoprotein inhibitors of natural origin as potential tumor chemo-sensitizers: a review. J Adv Res 6(1):45–62CrossRefPubMedGoogle Scholar
  2. Adsit GS, Vaidyanathan R, Galler CM, Kyle JW, Makielski JC (2013) Channelopathies from mutations in the cardiac sodium channel protein complex. J Mol Cell Cardiol 61:34–43CrossRefPubMedPubMedCentralGoogle Scholar
  3. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Molecular biology of the cell, 4th edn. Garland Science, New York. Carrier proteins and active membrane transport. ISBN-10: 0-8153-3218-1Google Scholar
  4. Alberts B, Bray D, Hopkin K, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2010) Essential cell biology. Garland Science, New YorkGoogle Scholar
  5. Allen TW, Andersen OS, Roux B (2006) Molecular dynamics potential of mean force calculations as a tool for understanding ion permeation and selectivity in narrow channels. Biophys Chem 124:251–267CrossRefPubMedGoogle Scholar
  6. Alleva K, Chara O, Amodeo G (2012) Aquaporins: another piece in the osmotic puzzle. FEBS Lett 586(19):2991–2999. ISSN 0014-5793CrossRefPubMedGoogle Scholar
  7. Asher V, Warren A, Shaw R, Sowter H, Bali A, Khan R (2011) The role of Eag and HERG channels in cell proliferation and apoptotic cell death in SK-OV-3 ovarian cancer cell line. Cancer Cell Int 11:6CrossRefPubMedPubMedCentralGoogle Scholar
  8. Ashrafuzzaman M, Tuszynski JA (2013) Membrane biophysics. Springer-Verlag Berlin Heidelberg, New York, pp 9–30CrossRefGoogle Scholar
  9. Ashwell JD, Schwartz RH, Mitchell JB, Russo A (1986) Effect of gamma radiation on resting B lymphocytes. I. Oxygen-dependent damage to the plasma membrane results in increased permeability and cell enlargement. J Immunol 136(10):3649–3656PubMedGoogle Scholar
  10. Ateshian GA, Morrison B, Hung CT (2010) Modeling of active transmembrane transport in a mixture theory framework. Ann Biomed Eng 38(5):1801–1814CrossRefPubMedPubMedCentralGoogle Scholar
  11. Becchetti A, Munaron L, Arcangeli A (2013) The role of ion channels and transporters in cell proliferation and cancer. Frontiers in Physiology 4:312Google Scholar
  12. Bökel C, Brand M (2014) Endocytosis and signaling during development. Cold Spring Harb Perspect Biol 6(3):a017020CrossRefPubMedPubMedCentralGoogle Scholar
  13. Bowman A, Xiao S, Schoenbach KS, Pakhomov AG (2008) Inhibition of voltage-gated calcium channels of cell plasma membrane by nanosecond electric pulses. In: Bioelectromagnetics Society’s 30th annual meeting, San Diego, pp 75–76, June 8–12Google Scholar
  14. Boya P, Kroemer G (2008) Lysosomal membrane permeabilization in cell death. Oncogene 27:6434–6451CrossRefPubMedGoogle Scholar
  15. Brackenbury WJ, Isom LL (2011) Na+ channel beta subunits: overachievers of the ion channel family. Front Pharmacol 2:53CrossRefPubMedPubMedCentralGoogle Scholar
  16. Brackenbury WJ, Djamgoz MB, Isom LL (2008) An emerging role for voltage-gated Na+ channels in cellular migration: regulation of central nervous system development and potentiation of invasive cancers. Neuroscientist 14:571–583CrossRefPubMedPubMedCentralGoogle Scholar
  17. Brew HM, Hallows JL, Tempel BL (2003) Hyperexcitability and reduced low threshold potassium currents in auditory neurons of mice lacking the channel subunit Kv1. 1. J Physiol 548(1):1–20CrossRefPubMedPubMedCentralGoogle Scholar
  18. Brini M, Carafoli E (2011) The plasma membrane Ca2+ ATPase and the plasma membrane sodium calcium exchanger cooperate in the regulation of cell calcium. Cold Spring Harb Perspect Biol 3(2):1–15CrossRefGoogle Scholar
  19. Brini M, Calì T, Ottolini D, Carafoli E (2013) The plasma membrane calcium pump in health and disease. FEBS J. 280(21):5385–5397Google Scholar
  20. Brown DA, Passmore GM (2009) Neural KCNQ (Kv7) channels. Br J Pharmacol 156(8):1185–1195CrossRefPubMedPubMedCentralGoogle Scholar
  21. Burganos VN (2017) Modeling and simulation of membrane structure and transport properties, reference module in chemistry. Mol Sci Chem Eng. ISBN 9780124095472Google Scholar
  22. Cao G, Zhang M, Miao J, Li W, Wang J, Lu D, Xia J (2015) Effects of X-ray and carbon ion beam irradiation on membrane permeability and integrity in Saccharomyces cerevisiae cells. J Radiat Res 56(2):294–304CrossRefPubMedPubMedCentralGoogle Scholar
  23. Catterall WA, Perez-Reyes E, Snutch TP, Striessnig J (2005) International union of pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol Rev 57:411–425CrossRefPubMedGoogle Scholar
  24. Cleal K, He L, Watson PD, Jones AT (2013) Endocytosis, intracellular traffic and fate of cell penetrating peptide based conjugates and nanoparticles. Curr Pharm Des 19(16):2878–2894CrossRefPubMedGoogle Scholar
  25. Cooper GM (2000) The cell: a molecular approach, 2nd edn. Sinauer Associates, SunderlandGoogle Scholar
  26. Cui C, Merritt R, Fu L, Pan Z (2017) Targeting calcium signaling in cancer therapy. Acta Pharmaceutica Sinica B 7(1):3–17RGoogle Scholar
  27. Das A, Pushparaj C, Herreros J, Nager M, Vilella R, Portero M, Pamplona M-GX, Marti RM, Canti C (2013) T-type calcium channel blockers inhibit autophagy and promote apoptosis of malignant melanoma cells. Pigment Cell Melanoma Res 26:874–885CrossRefPubMedGoogle Scholar
  28. Dean M, Rzhetsky A, Allikmets R (2001) The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 11(7):1156–1166CrossRefPubMedGoogle Scholar
  29. Delemotte L, Treptow W, Klein ML, Tarek M (2010) Effect of sensor domain mutations on the properties of voltage-gated ion channels: molecular dynamics studies of the potassium channel Kv1.2. Biophys J 99(9):L72–L74CrossRefPubMedPubMedCentralGoogle Scholar
  30. Dziegielewska B, Brautigan DL, Larner JM, Dziegielewski J (2014) T-type Ca2+channel inhibition induces p53-dependent cell growth arrest and apoptosis through activation of p38-MAPK in colon cancer cells. Mol Cancer Res 12:348–358CrossRefPubMedGoogle Scholar
  31. Eisenberg RS (2013) Ionic interactions in biological and physical systems: a variational treatment. Faraday Discuss 160:279–296CrossRefPubMedGoogle Scholar
  32. Fan Z, Kumon RE, Park J, Deng CX (2010) Intracellular delivery and calcium transients generated in sonoporation facilitated by microbubbles. J Control Release 142(1):31CrossRefPubMedGoogle Scholar
  33. Gavrilova-Ruch O, Schonherr K, Gessner G, Schonherr R, Klapperstuck T, Wohlrab W, Heinemann SH (2002) Effects of imipramine on ion channels and proliferation of IGR1 melanoma cells. J Membr Biol 188:137–149CrossRefPubMedGoogle Scholar
  34. Gehl J (2003) Electroporation: theory and methods, perspectives for drug delivery, gene therapy and research. Acta Physiol Scand 177(4):437–447CrossRefPubMedGoogle Scholar
  35. Gerbeau P, Amodeo G, Henzler T, Santoni V, Ripoche P, Maurel C (2002) The water permeability of Arabidopsis plasma membrane is regulated by divalent cations and pH. Plant J 1:71–81CrossRefGoogle Scholar
  36. Gillespie D, Eisenberg RS (2002) Physical descriptions of experimental selectivity measurements in ion channels. Eur Biophys J 31:454–466CrossRefPubMedGoogle Scholar
  37. Golowasch J, Nadim F (2014) Capacitance, membrane. Encyclopedia of computational neuroscience. Springer, Berlin\HeidelbergGoogle Scholar
  38. Gomulkiewicz J, Bartoszkiewicz M, Miekisz S (2001) Some remarks on ion transport across excitable membranes. I. The stationary state. Curr Top Biophys 25:3–9Google Scholar
  39. Gouaux E, MacKinnon R (2004) Principles of selective ion transport in channels and pumps. Science 310:1461–1465CrossRefGoogle Scholar
  40. Gutman GA, Chandy KG, Grissmer S, Lazdunski M, Mckinnon D, Pardo LA, Robertson GA, Rudy B, Sanguinetti MC, Stühmer W, Wang X (2005) International union of pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels. Pharmacol Rev 57(4):473–508CrossRefPubMedGoogle Scholar
  41. Hedfalk K, Törnroth-Horsefield S, Nyblom M, Johanson U, Kjellbom P, Neutze R (2006) Aquaporin gating. Curr Opin Struct Biol 16:447–456CrossRefPubMedGoogle Scholar
  42. Johnston J, Forsythe ID, Kopp-Scheinpflug C (2010) SYMPOSIUM REVIEW: Going native: voltage-gated potassium channels controlling neuronal excitability. J Physiol 588(17):3187–3200CrossRefPubMedPubMedCentralGoogle Scholar
  43. Kaczorowski GJ, McManus OB, Priest BT, Garcia ML (2008) Ion channels as drug targets: the next GPCRs. J Gen Physiol 131(5):399–405CrossRefPubMedPubMedCentralGoogle Scholar
  44. Kale VP, Amin SG, Pandey MK (2015) Pandey targeting ion channels for cancer therapy by repurposing the approved drugs. Biochim Biophys Acta 1848:2747–2755CrossRefPubMedGoogle Scholar
  45. Kotnik T, Kramar P, Pucihar G, Miklavcic D, Tarek M (2012) IEEE Electrical Insulation Magazine 28(5):14–23Google Scholar
  46. Kruger LC, Isom LL (2016) Voltage-gated Na+ channels: not just for conduction. Cold Spring Harb Perspect Biol 8(6):a029264CrossRefPubMedPubMedCentralGoogle Scholar
  47. Kulbacka J, Pucek A, Kotulska M, Dubińska-Magiera M, Rossowska J, Rols MP, Wilk KA (2016a) Electroporation and lipid nanoparticles with cyanine IR-780 and flavonoids as efficient vectors to enhanced drug delivery in colon cancer. Bioelectrochemistry 110:19–31CrossRefPubMedGoogle Scholar
  48. Kulbacka J, Pucek A, Wilk KA, Dubińska-Magiera M, Rossowska J, Kulbacki M, Kotulska M (2016b) The effect of millisecond pulsed electric fields (msPEF) on intracellular drug transport with negatively charged large Nanocarriers made of solid lipid nanoparticles (SLN): in vitro study. J Membr Biol 249(5):645–661CrossRefPubMedPubMedCentralGoogle Scholar
  49. Leonard GD, Fojo T, Bates SE (2003) The role of ABC transporters in clinical practice. Oncologist 8(5):411–424CrossRefPubMedGoogle Scholar
  50. Li J, Lin H (2011) Numerical simulation of molecular uptake via electroporation. Bioelectrochemistry 82(1):10–21Google Scholar
  51. Li M, Xiong Z-G (2011) Ion channels as targets for cancer therapy. Int J Physiol Pathophysiol Pharmacol 3(2):156–166PubMedPubMedCentralGoogle Scholar
  52. Li Q, Shu Y (2014) Role of solute carriers in response to anticancer drugs. Molecular and Cellular Therapies 2(1):15Google Scholar
  53. Lin L, Yee SW, Kim RB, Giacomini KM (2015) SLC transporters as therapeutic targets: emerging opportunities. Nature Reviews Drug Discovery 14(8):543–560Google Scholar
  54. Linton KJ (2007) Structure and function of ABC transporters. Physiology (Bethesda) 22:122–130Google Scholar
  55. Lodish H, Berk A, Zipursky SL, Matsudaira P, Baltimore D, Darnell J (2000) Molecular cell biology, 4th edn. W. H. Freeman, New YorkGoogle Scholar
  56. McKeown L, Swanton L, Robinson P, Jones OT (2008) Surface expression and distribution of voltage gated potassium channels in neurons (review). Mol Membr Biol 25(4):332–343CrossRefPubMedGoogle Scholar
  57. Millward MJ, Cantwell BM, Munro NC, Robinson A, Corris PA, Harris AL (1993) Oral verapamil with chemotherapy for advanced non-small cell lung cancer: a randomized study. Br J Cancer 67:1031–1035CrossRefPubMedPubMedCentralGoogle Scholar
  58. Min KA, Shin MC, Yu F, Yang M, David AE, Yang VC, Rosania GR (2013) Pulsed magnetic field improves the transport of iron oxide nanoparticles through cell barriers. ACS Nano 7(3):2161–2171CrossRefPubMedPubMedCentralGoogle Scholar
  59. Mir LM, Orlowski S, Belehradek J, Paoletti C (1991) Electrochemotherapy potentiation of antitumour effect of bleomycin by local electric pulses. Eur J Cancer 27(1):68–72CrossRefPubMedGoogle Scholar
  60. Misonou H, Mohapatra DP, Menegola M, Trimmer JS (2005) Calcium-and metabolic state-dependent modulation of the voltage-dependent Kv2. 1 channel regulates neuronal excitability in response to ischemia. J Neurosci 25(48):11184–11193CrossRefPubMedGoogle Scholar
  61. Mohapatra DP, Misonou H, Sheng-Jun P, Held JE, Surmeier DJ, Trimmer JS (2009) Regulation of intrinsic excitability in hippocampal neurons by activity-dependent modulation of the KV2. 1 potassium channel. Channels 3(1):46–56CrossRefPubMedPubMedCentralGoogle Scholar
  62. Muscella A, Calabriso N, Vetrugno C, Fanizzi FP, De Pascali SA, Storelli C (2011) The platinum (II) complex [Pt(O,O′-acac)(γ-acac)(DMS)] alters the intracellular calcium homeostasis in MCF-7 breast cancer cells. Biochem Pharmacol 81:91–103CrossRefPubMedGoogle Scholar
  63. Nejad SM, Hosseini H, Akiyama H, Tachibana K (2016) Reparable cell Sonoporation in suspension: Theranostic potential of microbubble. Theranostics 6(4):446–455CrossRefPubMedPubMedCentralGoogle Scholar
  64. Nesin V, Bowman AM, Xiao S, Pakhomov AG (2012) Cell permeabilization and inhibition of voltage-gated Ca2+ and Na+ channel currents by nanosecond pulsed electric fields. Bioelectromagnetics 33(5):394–404CrossRefPubMedGoogle Scholar
  65. O’Grady SM, Lee SY (2005) Molecular diversity and function of voltage-gated (Kv) potassium channels in epithelial cells. Int J Biochem Cell Biol 37:1578–1594CrossRefPubMedGoogle Scholar
  66. O’Malley HA, Isom LL (2015) Sodium channel b subunits: emerging targets in channelopathies. Annu Rev Physiol 77:481–504CrossRefPubMedPubMedCentralGoogle Scholar
  67. Oh N, Park JH (2014) Endocytosis and exocytosis of nanoparticles in mammalian cells. Int J Nanomedicine 9(Suppl 1):51–63PubMedPubMedCentralGoogle Scholar
  68. Pakhomov AG, Kolb J, White J, Shevin R, Pakhomova ON, Schoenbach KS (2007a) Membrane effects of ultrashort (nanosecond) electric stimuli. Society for Neuroscience 37th Annual Meeting, San Diego, Nov 2–7 2007, Neuroscience meeting planner CD-ROM, Presentation No.: 317.14.Google Scholar
  69. Pakhomov AG, Shevin R, White JA, Kolb JF, Pakhomova ON, Joshi RP, Schoenbach KH (2007b) Membrane permeabilization and cell damage by ultrashort electric field shocks. Arch Biochem Biophys. 465(1):109–118Google Scholar
  70. Pardo LA, Stühmer W (2014) The roles of K(+) channels in cancer. Nat Rev Cancer 14(1):39–48CrossRefPubMedGoogle Scholar
  71. Patel F, Brackenbury WJ (2015) Dual roles of voltage-gated sodium channels in development and cancer. Int J Dev Biol 59(7–9):357–366CrossRefPubMedPubMedCentralGoogle Scholar
  72. Pavlin M, Kandušer M, Reberšek M, Pucihar G, Hart FX, Magjarevićcacute R, Miklavčič D (2005) Effect of cell electroporation on the conductivity of a cell suspension. Biophys J 88(6):4378–4390CrossRefPubMedPubMedCentralGoogle Scholar
  73. Perland E, Fredriksson R (2016) Classification Systems of Secondary Active Transporters. Trends Pharmacol Sci S0165-6147(16):30166–30163Google Scholar
  74. Pitt WG, Husseini GA, Staples BJ (2004) Ultrasonic drug delivery – a general review. Expert Opin Drug Deliv 1(1):37–56CrossRefPubMedPubMedCentralGoogle Scholar
  75. Qiao G, Duan W, Chatwin C, Sinclair A, Wang W (2010) Electrical properties of breast cancer cells from impedance measurement of cell suspensions. J Phys Conf Ser 224:012081CrossRefGoogle Scholar
  76. Rask-Andersen M, Masuram S, Fredriksson R, Schiöth HB (2013) Solute carriers as drug targets: Current use, clinical trials and prospective. Molecular Aspects of Medicine 34(2-3):702–710Google Scholar
  77. Ray S, Kassan A, Busija AR, Rangamani P, Patel HH (2016) The plasma membrane as a capacitor for energy and metabolism. Am J Physiol Cell Physiol 310(3):181–192Google Scholar
  78. Rim HK, Lee HW, Choi IS, Park JY, Choi HW, Choi JH, Cho YW, Lee JY, Lee KT (2012) T-type Ca2+ channel blocker, KYS05047 induces G1 phase cell cycle arrest by decreasing intracellular Ca2+ levels in human lung adenocarcinoma A549 cells. Bioorg Med Chem Lett 22:7123–7126CrossRefPubMedGoogle Scholar
  79. Rosazza C, Buntz A, Rieß T, Wöll D, Zumbusch A, Rols M-P (2013) Intracellular tracking of single-plasmid DNA particles after delivery by electroporation. Mol Ther 21(12):2217–2226CrossRefPubMedPubMedCentralGoogle Scholar
  80. Runas KA, Malmstadt N (2015) Low levels of lipid oxidation radically increase the passive permeability of lipid bilayers. Soft Matter 11(3):499–505CrossRefPubMedPubMedCentralGoogle Scholar
  81. Selwan EM, Finicle BT, Kim SM, Edinger AL (2016) Attacking the supply wagons to starve cancer cells to death. FEBS Lett 590(7):885–907CrossRefPubMedPubMedCentralGoogle Scholar
  82. Shattock MJ, Ottolia M, Bers DM, Blaustein MP, Boguslavskyi A, Bossuyt J, Bridge JH, Chen-Izu Y, Clancy CE, Edwards A, Goldhaber J, Kaplan J, Lingrel JB, Pavlovic D, Philipson K, Sipido KR, Xie ZJ (2015) Na+/Ca2+ exchange and Na+/K+-ATPase in the heart. J Physiol 593(6):1361–1382CrossRefPubMedPubMedCentralGoogle Scholar
  83. Shigekawa M, Iwamoto T (2001) Cardiac Na+-Ca2+ exchange. Circ Res 88:864–876CrossRefPubMedGoogle Scholar
  84. Shin JM, Munson K, Sachs G (2011) Gastric H+, K+-ATPase. Compr Physiol 1(4):2141–2153PubMedGoogle Scholar
  85. Shukla S, Ohnuma S, Ambudkar SV (2011 May) Improving cancer chemotherapy with modulators of ABC drug transporters. Curr Drug Targets 12(5):621–630CrossRefPubMedPubMedCentralGoogle Scholar
  86. Simms BA, Zamponi GW (2014) Neuronal voltage-gated calcium channels: structure, function, and dysfunction. Neuron 82:24–45CrossRefPubMedGoogle Scholar
  87. Steller L, Kreir M, Salzer R (2012) Natural and artificial ion channels for biosensing platforms. Anal Bioanal Chem 402(1):209–230CrossRefPubMedGoogle Scholar
  88. Strehler EE (2013) Plasma membrane calcium ATPases as novel candidates for therapeutic agent development. J Pharm Pharm Sci 16(2):190–206CrossRefPubMedPubMedCentralGoogle Scholar
  89. Sugano K, Kansy M, Artursson P, Avdeef A, Bendels S, Di L, Ecker GF, Faller B, Fischer H, Gerebtzoff G, Lennernaes H, Senner F (2010) Coexistence of passive and carrier-mediated processes in drug transport. Nat Rev Drug Discov 9(8):597–614CrossRefPubMedGoogle Scholar
  90. Tamošiūnas M, Mir LM, Chen WS, Lihachev A, Venslauskas M, Šatkauskas S (2016) Intracellular delivery of bleomycin by combined application of electroporation and sonoporation in vitro. J Membr Biol 249(5):677–689CrossRefPubMedGoogle Scholar
  91. Tan Q, Ferrier GA, Chen BK, Wang C, Sun Y (2012) Quantification of the specific membrane capacitance of single cells using a microfluidic device and impedance spectroscopy measurement. Biomicrofluidics 6:034112CrossRefPubMedCentralGoogle Scholar
  92. Taylor JM, Simpson RU (1992) Inhibition of cancer cell growth by calcium channel antagonists in the arrhythmic mouse. Cancer Res 52:2413–2418PubMedGoogle Scholar
  93. Tombola F, Pathak MM, Isacoff EY (2006) How does voltage open an ion channel? Ann Rev Cell Dev Biol 22:23–52CrossRefGoogle Scholar
  94. Vasiliou V, Vasiliou K, Nebert DW (2009) Human ATP-binding cassette (ABC) transporter family. Hum Genomics 3(3):281–290CrossRefPubMedPubMedCentralGoogle Scholar
  95. Wang L, Bhattacharjee A, Zuo Z, Hu F, Honkanen RE, Berggren PO, Li M (1999) A low voltage-activated Ca2+ current mediates cytokine-induced pancreatic beta-cell death. Endocrinology 140:1200–1204CrossRefPubMedGoogle Scholar
  96. Wang H, Zhang Y, Cao L, Han H, Wang J, Yang B, Nattel S, Wang Z (2002) HERG K+ channel, a regulator of tumor cell apoptosis and proliferation. Cancer Res 62:4843–4848PubMedGoogle Scholar
  97. Waterbeemd H, Lennernäs H, Artursson P (2006) Drug bioavailability: estimation of solubility, permeability, absorption and bioavailability. John Wiley & Sons, WeinheimGoogle Scholar
  98. Wezgowiec J, Derylo MB, Teissie J, Orio J, Rols M-P, Kulbacka J, Saczko J, Kotulska M (2013) Electric field-assisted delivery of photofrin to human breast carcinoma cells. J Membr Biol 246(10):725–735CrossRefPubMedPubMedCentralGoogle Scholar
  99. Xiong Q, Gao Z, Wang W, Li M (2008) Activation of Kv7 (KCNQ) voltage-gated potassium channels by synthetic compounds. Trends Pharmacol Sci 9(2):99–107CrossRefGoogle Scholar
  100. Yang NJ, Hinner MJ (2015) Getting across the cell membrane: an verviewo for small molecules, peptides, and proteins. Methods in molecular biology (Clifton, N.J.), 1266, 29–53Google Scholar
  101. Yellen G (2002) The voltage-gated potassium channels and their relatives. Nature 419(6902):35–42CrossRefPubMedGoogle Scholar
  102. Yukutake Y, Hirano Y, Suematsu M, Yasui M (2009) Rapid and reversible inhibition of aquaporin-4 by zinc. Biochemist 48:12059–12061CrossRefGoogle Scholar
  103. Zamponi GW (2016) Targeting voltage-gated calcium channels in neurological and psychiatric diseases. Nat Rev Drug Discov 15(1):19–34CrossRefPubMedGoogle Scholar
  104. Zamponi GW, Striessnig J, Koschak A, Dolphin AC (2015) The physiology, pathology, and pharmacology of voltage-gated calcium channels and their future therapeutic potential. Pharmacol Rev 67:821–870CrossRefPubMedPubMedCentralGoogle Scholar
  105. Zeghimi A, Escoffre JM, Bouakaz A (2015) Role of endocytosis in sonoporation-mediated membrane permeabilization and uptake of small molecules: a electron microscopy study. Phys Biol 12:066007CrossRefPubMedGoogle Scholar
  106. Zhang S, Morris ME (2003) Effects of the flavonoids biochanin A, morin, phloretin, and silymarin on P-glycoprotein-mediated transport. J Pharmacol Exp Ther 304(3):1258–1267CrossRefPubMedGoogle Scholar
  107. Zhang WM, Zhou J, Ye QJ (2008) Endothelin-1 enhances proliferation of lung cancer cells by increasing intracellular free Ca2+. Life Sci 82:764–771CrossRefPubMedGoogle Scholar
  108. Zhao Y, Zhao XT, Chen DY, Luo YN, Jiang M, Wei C, Long R, Yue WT, Wang JB, Chen J (2014) Tumor cell characterization and classification based on cellular specific membrane capacitance and cytoplasm conductivity. Biosens Bioelectron 57:245–253CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Julita Kulbacka
    • 1
  • Anna Choromańska
    • 1
  • Joanna Rossowska
    • 2
  • Joanna Weżgowiec
    • 3
  • Jolanta Saczko
    • 1
  • Marie-Pierre Rols
    • 4
  1. 1.Department of Medical BiochemistryWroclaw Medical UniversityWrocławPoland
  2. 2.Institute of Immunology and Experimental Therapy Polish Academy of SciencesWrocławPoland
  3. 3.Department of Dental Prosthetics, Division of Dental MaterialsWrocław Medical UniversityWrocławPoland
  4. 4.Institut de Pharmacologie et de Biologie StructuraleUniversité de Toulouse, CNRS, UPSToulouseFrance

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