Mapping the functional expression of auxiliary subunits of K


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
20 12 2022
Historique:
received: 15 02 2022
accepted: 12 12 2022
entrez: 20 12 2022
pubmed: 21 12 2022
medline: 23 12 2022
Statut: epublish

Résumé

Glioblastoma (GBM) is the most aggressive glial tumor, where ion channels, including K

Identifiants

pubmed: 36539587
doi: 10.1038/s41598-022-26196-w
pii: 10.1038/s41598-022-26196-w
pmc: PMC9768140
doi:

Substances chimiques

Carbachol 8Y164V895Y

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

22023

Informations de copyright

© 2022. The Author(s).

Références

Tan, A. C. et al. Management of glioblastoma: State of the art and future directions. CA Cancer J. Clin. 70, 299–312 (2020).
doi: 10.3322/caac.21613
Hofschröer, V. et al. Ion Channels Orchestrate Pancreatic Ductal Adenocarcinoma Progression and Therapy. Front. Pharmacol. 11, 586599 (2021).
Capatina, A. L., Lagos, D. & Brackenbury, W. J. Targeting Ion Channels for Cancer Treatment: Current Progress and Future Challenges. Rev. Physiol. Biochem. Pharmacol. 1–43 https://doi.org/10.1007/112_2020_46 (2020).
Liu, X., Chang, Y., Reinhart, P. H. & Sontheimer, H. Cloning and characterization of glioma BK, a novel BK channel isoform highly expressed in human glioma cells. J. Neurosci. 22, 1840–1849 (2002).
doi: 10.1523/JNEUROSCI.22-05-01840.2002
Ransom, C. B., Liu, X. & Sontheimer, H. BK channels in human glioma cells have enhanced calcium sensitivity. Glia 38, 281–291 (2002).
doi: 10.1002/glia.10064
Edalat, L. et al. BK K
doi: 10.18632/oncotarget.7423
Rosa, P. et al. BK channels blockage inhibits hypoxia-induced migration and chemoresistance to cisplatin in human glioblastoma cells. J. Cell Physiol. 233, 6866–6877 (2018).
doi: 10.1002/jcp.26448
Li, Q. & Yan, J. Modulation of BK channel function by auxiliary beta and gamma subunits. Int. Rev. Neurobiol. 128, 51–90 (2016).
doi: 10.1016/bs.irn.2016.03.015
Petho, Z. et al. Erratum to: Different expression of β subunits of the K
Ge, L. et al. Big potassium (BK) ion channels in biology, disease and possible targets for cancer immunotherapy. Int. Immunopharmacol. 22, 427–443 (2014).
doi: 10.1016/j.intimp.2014.06.040
Turner, K. L., Honasoge, A., Robert, S. M., Mcferrin, M. M. & Sontheimer, H. A proinvasive role for the Ca2+-activated K+ channel KCa3.1 in malignant glioma. Glia 62, 971–981 (2014).
doi: 10.1002/glia.22655
Cox, D. H. Modeling a Ca
doi: 10.1016/j.bpj.2014.10.069
Kuntze, A. et al. Protonation of Piezo1 Impairs Cell-Matrix Interactions of Pancreatic Stellate Cells. Front. Physiol. 11, 89 (2020).
doi: 10.3389/fphys.2020.00089
Waschk, D. E. J., Fabian, A., Budde, T. & Schwab, A. Dual-color quantum dot detection of a heterotetrameric potassium channel (hK
doi: 10.1152/ajpcell.00053.2010
Kraft, R. et al. BK channel openers inhibit migration of human glioma cells. Pflugers Arch. 446, 248–255 (2003).
doi: 10.1007/s00424-003-1012-4
Bordey, A., Sontheimer, H. & Trouslard, J. Muscarinic activation of BK channels induces membrane oscillations in glioma cells and leads to inhibition of cell migration. J. Membr. Biol. 176, 31–40 (2000).
doi: 10.1007/s002320001073
Dopico, A. M., Walsh, J. V. & Singer, J. J. Natural bile acids and synthetic analogues modulate large conductance Ca
doi: 10.1085/jgp.20028537
Bukiya, A. N., Vaithianathan, T., Toro, L. & Dopico, A. M. Channel beta2-4 subunits fail to substitute for beta1 in sensitizing BK channels to lithocholate. Biochem. Biophys. Res. Commun. 390, 995–1000 (2009).
doi: 10.1016/j.bbrc.2009.10.091
Martín, P. et al. Arachidonic acid activation of BKCa (Slo1) channels associated to the β1-subunit in human vascular smooth muscle cells. Pflugers Arch. 466, 1779–1792 (2014).
doi: 10.1007/s00424-013-1422-x
Sun, X., Zhou, D., Zhang, P., Moczydlowski, E. G. & Haddad, G. G. Beta-subunit-dependent modulation of hSlo BK current by arachidonic acid. J. Neurophysiol. 97, 62–69 (2007).
doi: 10.1152/jn.00700.2006
Xia, X. M., Ding, J. P. & Lingle, C. J. Inactivation of BK channels by the NH2 terminus of the beta2 auxiliary subunit: An essential role of a terminal peptide segment of three hydrophobic residues. J. Gen. Physiol. 121, 125–148 (2003).
doi: 10.1085/jgp.20028667
Ding, J. P. & Lingle, C. J. Steady-state and closed-state inactivation properties of inactivating BK channels. Biophys. J. 82, 2448–2465 (2002).
doi: 10.1016/S0006-3495(02)75588-4
Wallner, M., Meera, P. & Toro, L. Molecular basis of fast inactivation in voltage and Ca2+-activated K+ channels: A transmembrane beta-subunit homolog. Proc. Natl. Acad. Sci. U S A 96, 4137–4142 (1999).
doi: 10.1073/pnas.96.7.4137
Meera, P., Wallner, M. & Toro, L. A neuronal beta subunit (KCNMB4) makes the large conductance, voltage- and Ca
doi: 10.1073/pnas.100118597
Tanner, M. R. et al. Targeting KCa1.1 channels with a scorpion venom peptide for the therapy of rat models of rheumatoid arthritis. J. Pharmacol. Exp. Ther. 365, 227 (2018).
doi: 10.1124/jpet.117.245118
Petrik, D., Wang, B. & Brenner, R. Modulation by the BK accessory β4 subunit of phosphorylation-dependent changes in excitability of dentate gyrus granule neurons. Eur. J. Neurosci. 34, 695–704 (2011).
doi: 10.1111/j.1460-9568.2011.07799.x
Shruti, S. et al. The brain-specific Beta4 subunit downregulates BK channel cell surface expression. PLoS One 7(3), e33429 (2012).
doi: 10.1371/journal.pone.0033429
Kiriyama, Y. & Nochi, H. The biosynthesis, signaling, and neurological functions of bile acids. Biomolecules 9, 232 (2019).
doi: 10.3390/biom9060232
Antollini, S. S. & Barrantes, F. J. Fatty acid regulation of voltage- and ligand-gated ion channel function. Front. Physiol. 7, 573 (2016).
doi: 10.3389/fphys.2016.00573
Garza Lopez, E., Sánchez-Carranza, O., Nishigaki, T. & López-González, I. Pharmacological identification of endogenous Slo1 channel-B1 subunit complexes in CHO cells using three aKTX1 subfamily toxins. Int. J. Pharm. Therapeutics 6, 11–24 (2015).
Xia, X. M., Ding, J. P., Zeng, X. H., Duan, K. L. & Lingle, C. J. Rectification and rapid activation at low Ca
doi: 10.1523/JNEUROSCI.20-13-04890.2000
Zeng, X. H., Xia, X. M. & Lingle, C. J. Redox-sensitive extracellular gates formed by auxiliary beta subunits of calcium-activated potassium channels. Nat. Struct. Biol. 10, 448–454 (2003).
doi: 10.1038/nsb932
Thompson, E. G. & Sontheimer, H. Acetylcholine receptor activation as a modulator of glioblastoma invasion. Cells 8(10), 1203 (2019).
doi: 10.3390/cells8101203
Urrego, D., Tomczak, A. P., Zahed, F., Stühmer, W. & Pardo, L. A. Potassium channels in cell cycle and cell proliferation. Philosophical Transactions R. Soc. B Biol. Sci. 369(1638), 20130094 (2014).
doi: 10.1098/rstb.2013.0094
Ouadid-Ahidouch, H. & Ahidouch, A. K
doi: 10.3389/fphys.2013.00220
Hoffmann, E. K., Lambert, I. H. & Pedersen, S. F. Physiology of cell volume regulation in vertebrates. Physiol. Rev. 89, 193–277 (2009).
doi: 10.1152/physrev.00037.2007
Behrens, R. et al. hKCNMB3 and hKCNMB4, cloning and characterization of two members of the large-conductance calcium-activated potassium channel beta subunit family. FEBS Lett. 474, 99–106 (2000).
doi: 10.1016/S0014-5793(00)01584-2
Lippiat, J. D., Standen, N. B., Harrow, I. D., Phillips, S. C. & Davies, N. W. Properties of BKCa Channels Formed by Bicistronic Expression of hSloα and β1–4 Subunits in HEK293 Cells. J. Membr. Biol. 2003 192:2 192, 141–148 (2003).
Dopico, A. M., Bukiya, A. N. & Jaggar, J. H. Calcium- and voltage-gated BK channels in vascular smooth muscle. Pflugers Arch. 470, 1271 (2018).
doi: 10.1007/s00424-018-2151-y
Bukiya, A. N., Vaithianathan, T., Toro, L. & Dopico, A. M. The second transmembrane domain of the large conductance, voltage- and calcium-gated potassium channel β1 subunit is a lithocholate sensor. FEBS Lett. 582, 673 (2008).
doi: 10.1016/j.febslet.2008.01.036
Wiemuth, D., Assmann, M. & Gründer, S. The bile acid-sensitive ion channel (BASIC), the ignored cousin of ASICs and ENaC. Channels 8, 29 (2014).
doi: 10.4161/chan.27493
Gonzalez-Perez, V. & Lingle, C. J. Regulation of BK channels by beta and gamma subunits. Annu. Rev. Physiol. 81, 113 (2019).
doi: 10.1146/annurev-physiol-022516-034038
Wang, Y. W., Ding, J. P., Xia, X. M. & Lingle, C. J. Consequences of the stoichiometry of Slo1 alpha and auxiliary beta subunits on functional properties of large-conductance Ca
doi: 10.1523/JNEUROSCI.22-05-01550.2002
Kuntamallappanavar, G., Bisen, S., Bukiya, A. N. & Dopico, A. M. Differential distribution and functional impact of BK channel beta1 subunits across mesenteric, coronary, and different cerebral arteries of the rat. Pflugers Arch. 469, 263–277 (2017).
doi: 10.1007/s00424-016-1929-z
Martinez-Espinosa, P. L., Yang, C., Gonzalez-Perez, V., Xia, X. M. & Lingle, C. J. Knockout of the BK β2 subunit abolishes inactivation of BK currents in mouse adrenal chromaffin cells and results in slow-wave burst activity. J. Gen. Physiol. 144, 275–295 (2014).
doi: 10.1085/jgp.201411253
Brenner, R., Jegla, T. J., Wickenden, A., Liu, Y. & Aldrich, R. W. Cloning and functional characterization of novel large conductance calcium-activated potassium channel beta subunits, hKCNMB3 and hKCNMB4. J. Biol. Chem. 275, 6453–6461 (2000).
doi: 10.1074/jbc.275.9.6453
Candia, S., Garcia, M. L. & Latorre, R. Mode of action of iberiotoxin, a potent blocker of the large conductance Ca
doi: 10.1016/S0006-3495(92)81630-2
Steinle, M. et al. Ionizing radiation induces migration of glioblastoma cells by activating BK K(+) channels. Radiother. Oncol. 101, 122–126 (2011).
doi: 10.1016/j.radonc.2011.05.069
Contreras, G. F., Neely, A., Alvarez, O., Gonzalez, C. & Latorre, R. Modulation of BK channel voltage gating by different auxiliary β subunits. Proc. Natl. Acad. Sci. U S A 109, 18991–18996 (2012).
doi: 10.1073/pnas.1216953109
Haworth, A. S. & Brackenbury, W. J. Emerging roles for multifunctional ion channel auxiliary subunits in cancer. 80, 125–140 (2019).
Pethő, Z., Najder, K., Bulk, E. & Schwab, A. Mechanosensitive ion channels push cancer progression. Cell Calcium vol. 80 79–90 Preprint at https://doi.org/10.1016/j.ceca.2019.03.007 (2019).
Pedersen, S. F., Novak, I., Alves, F., Schwab, A. & Pardo, L. A. Alternating pH landscapes shape epithelial cancer initiation and progression: Focus on pancreatic cancer. BioEssays vol. 39 Preprint at https://doi.org/10.1002/bies.201600253 (2017).
Pethő, Z. et al. pH-channeling in cancer: How pH-dependence of cation channels shapes cancer pathophysiology. Cancers vol. 12 1–37 Preprint at https://doi.org/10.3390/cancers12092484 (2020).
Xin, X. F. et al. The extracellular loop of the auxiliary β1-subunit is involved in the regulation of BK Ca channel mechanosensitivity. Am. J. Physiol. Cell Physiol. 315, C485–C493 (2018).
doi: 10.1152/ajpcell.00037.2018
Louis, D. N. et al. The 2016 World Health Organization classification of tumors of the central nervous system: A summary. Acta Neuropathol. 131, 803–820 (2016).
doi: 10.1007/s00401-016-1545-1
Souza, D. G., Bellaver, B., Souza, D. O. & Quincozes-Santos, A. Characterization of adult rat astrocyte cultures. PLoS One 8(3), e60282 (2013).
doi: 10.1371/journal.pone.0060282
Oliva, M. A. et al. Characterization of primary glioma cell lines derived from the patients according to 2016 CNS tumour WHO classification and comparison with their parental tumours. J. Neuro Oncol. 2021 151:2 151, 123–133 (2021).
Darzynkiewicz, Z. Critical Aspects in Analysis of Cellular DNA Content. Curr Protoc Cytom 52, 7.2.1–7.2.8 (2010).
Kuhn, S. A. et al. Glioblastoma cells express functional cell membrane receptors activated by daily used medical drugs. J. Cancer Res. Clin. Oncol. 135, 1729 (2009).
doi: 10.1007/s00432-009-0620-6
R Core Team. R: A language and environment for statistical computing. Preprint at (2021).

Auteurs

Adam Feher (A)

Department of Biophysics and Cell Biology, Faculty of Medicine, University Debrecen, Debrecen, Hungary.

Zoltán Pethő (Z)

Department of Biophysics and Cell Biology, Faculty of Medicine, University Debrecen, Debrecen, Hungary.
Institute of Physiology II, University Münster, Münster, Germany.

Tibor G Szanto (TG)

Department of Biophysics and Cell Biology, Faculty of Medicine, University Debrecen, Debrecen, Hungary.

Álmos Klekner (Á)

Department of Neurosurgery, Faculty of Medicine, University Debrecen, Debrecen, Hungary.

Gabor Tajti (G)

Department of Biophysics and Cell Biology, Faculty of Medicine, University Debrecen, Debrecen, Hungary.

Gyula Batta (G)

Department of Genetics and Applied Microbiology, University Debrecen, Debrecen, Hungary.

Tibor Hortobágyi (T)

Faculty of Medicine, Institute of Pathology, University of Szeged, Szeged, Hungary.
ELKH-DE Cerebrovascular and Neurodegenerative Research Group, Department of Neurology, Faculty of Medicine, University Debrecen, Debrecen, Hungary.

Zoltan Varga (Z)

Department of Biophysics and Cell Biology, Faculty of Medicine, University Debrecen, Debrecen, Hungary.

Albrecht Schwab (A)

Institute of Physiology II, University Münster, Münster, Germany.

Gyorgy Panyi (G)

Department of Biophysics and Cell Biology, Faculty of Medicine, University Debrecen, Debrecen, Hungary. panyi@med.unideb.hu.

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