BK channels and a cGMP-dependent protein kinase (PKG) function through independent mechanisms to regulate the tolerance of synaptic transmission to acute oxidative stress at the Drosophila larval neuromuscular junction

References

• Alioua, A., Tanaka, Y., Wallner, M., Hofmann, F., Ruth, P., Meera, P., & Toro, L. (1998). The large conductance, voltage-dependent, and calcium-sensitive K + channel, Hslo, is a target of cGMP-dependent protein kinase phosphorylation in vivo. Journal of Biological Chemistry, 273, 32950–32956. doi:10.1074/jbc.273.49.32950
   PubMed Web of Science ®Google Scholar
• Atkinson, N., Robertson, G., & Ganetzky, B. (1991). A component of calcium-activated potassium channels encoded by the Drosophila slo locus. Science, 253, 551–555. doi:10.1126/science.1857984
   PubMed Web of Science ®Google Scholar
• Behl, C., Davis, J.B., Lesley, R., & Schubert, D. (1994). Hydrogen peroxide mediates amyloid β protein toxicity. Cell, 77, 817–827. doi:10.1016/0092-8674(94)90131-7
   PubMed Web of Science ®Google Scholar
• Benoit, P., & Changeux, J. P. (1993). Voltage dependencies of the effects of chlorpromazine on the nicotinic receptor channel from mouse muscle cell line So18. Neuroscience Letters, 160, 81–84. doi:10.1016/0304-3940(93)90918-B
   PubMed Web of Science ®Google Scholar
• Bian, S., Favre, I., & Moczydlowski, E. (2001). Ca2+-binding activity of a COOH-terminal fragment of the Drosophila BK channel involved in Ca2+-dependent activation. Proceedings of the National Academy of Sciences, 98, 4776–4781. doi:10.1073/pnas.081072398
   PubMed Web of Science ®Google Scholar
• Bonnet, S., Archer, S. L., Allalunis-Turner, J., Haromy, A., Beaulieu, C., Thompson, R., … Michelakis, E. D. (2007). A mitochondria-K + channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell, 11, 37–51. doi:10.1016/j.ccr.2006.10.020
   PubMed Web of Science ®Google Scholar
• Bortner, C. D., Hughes, F. M., & Cidlowski, J. A. (1997). A primary role for K + and Na + efflux in the activation of apoptosis. Journal of Biological Chemistry, 272, 32436–32442. doi:10.1074/jbc.272.51.32436
   PubMed Web of Science ®Google Scholar
• Broderick, K. E., Kean, L., Dow, J. A. T., Pyne, N. J., & Davies, S. A. (2004). Ectopic expression of bovine type 5 phosphodiesterase confers a renal phenotype in Drosophila. Journal of Biological Chemistry, 279, 8159–8168. doi:10.1074/jbc.M304679200
   PubMed Web of Science ®Google Scholar
• Candia, S., Garcia, M. L., & Latorre, R. (1992). Mode of action of iberiotoxin, a potent blocker of the large conductance Ca(2+)-activated K + channel. Biophysical Journal, 63, 583–590. doi:10.1016/S0006-3495(92)81630-2
   PubMed Web of Science ®Google Scholar
• Caplan, S. L., Milton, S. L., & Dawson-Scully, K. (2013). A cGMP-dependent protein kinase (PKG) controls synaptic transmission tolerance to acute oxidative stress at the Drosophila larval neuromuscular junction. Journal of Neurophysiology, 109, 649–658. doi:10.1152/jn.00784.2011
   PubMed Web of Science ®Google Scholar
• Caplan, S. L., Zheng, B., Dawson-Scully, K., White, C. A., & West, L. M. (2016). Pseudopterosin a: Protection of synaptic function and potential as a neuromodulatory agent. Marine Drugs, 14, 55. doi:10.3390/md14030055
   Web of Science ®Google Scholar
• Carpenter, W. T., & Koenig, J. I. (2008). The evolution of drug development in schizophrenia: Past issues and future opportunities. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 33, 2061–2079. doi:10.1038/sj.npp.1301639
   PubMed Web of Science ®Google Scholar
• Castro, J., Bittner, C. X., Humeres, A., Montecinos, V. P., Vera, J. C., & Barros, L. F. (2004). A cytosolic source of calcium unveiled by hydrogen peroxide with relevance for epithelial cell death. Cell Death and Differentiation, 11, 468–478. doi:10.1038/sj.cdd.4401372
   PubMed Web of Science ®Google Scholar
• Chen, M., Sun, H. Y., Hu, P., Wang, C. F., Li, B. X., Li, S. J., … Gao, T. M. (2013). Activation of BKCa channels mediates hippocampal neuronal death after reoxygenation and reperfusion. Molecular Neurobiology, 48, 794–807. https://doi.org/10.1007/s12035-013-8467-x
   PubMed Web of Science ®Google Scholar
• Chi, S., Cai, W., Liu, P., Zhang, Z., Chen, X., Gao, L., … Qi, Z. (2010). Baifuzi reduces transient ischemic brain damage through an interaction with the STREX domain of BKCa channels. Cell Death Dis, 1, e13. doi:10.1038/cddis.2009.10
   PubMed Web of Science ®Google Scholar
• Croll, R. P., Baker, M. W., Khabarova, M., Voronezhskaya, E. E., & Sakharov, D. A. (1997). Serotonin depletion after prolonged chlorpromazine treatment in a simpler model system. General Pharmacology, 29, 91–96. doi:10.1016/S0306-3623(96)00530-7
   PubMedGoogle Scholar
• Cuzzocrea, S., Riley, D. P., Caputi, A. P., & Salvemini, D. (2001). Antioxidant therapy: A new pharmacological approach in shock, inflammation, and ischemia/reperfusion injury. Pharmacological Reviews, 426, 1–159. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/11171943
   Google Scholar
• Dawson-Scully, K., Armstrong, G. A. B., Kent, C., Robertson, R. M., & Sokolowski, M. B. (2007). Natural variation in the thermotolerance of neural function and behavior due to a cGMP-dependent protein kinase. PLoS Ond, 2, e773. doi:10.1371/journal.pone.0000773
   PubMed Web of Science ®Google Scholar
• Dawson-Scully, K., Bukvic, D., Chakaborty-Chatterjee, M., Ferreira, R., Milton, S. L., & Sokolowski, M. B. (2010). Controlling anoxic tolerance in adult Drosophila via the cGMP-PKG pathway. Journal of Experimental Biology, 213, 2410–2416. doi:10.1242/jeb.041319
   PubMed Web of Science ®Google Scholar
• Day, J. P., Dow, J. A. T., Houslay, M. D., & Davies, S. (2005). Cyclic nucleotide phosphodiesterases in Drosophila melanogaster. The Biochemical Journal, 388, 333–342. doi:10.1042/BJ20050057
   PubMed Web of Science ®Google Scholar
• DiChiara, T. J., & Reinhart, P. H. (1995). Distinct effects of Ca2+ and voltage on the activation and deactivation of cloned Ca(2+)-activated K + channels. The Journal of Physiology, 489, 403–418. doi:10.1113/jphysiol.1995.sp021061
   PubMed Web of Science ®Google Scholar
• Elkins, T., & Ganetzky, B. (1988). The roles of potassium currents in Drosophila flight muscles. Journal of Neuroscience, 8, 428–434. doi:10.1523/JNEUROSCI.08-02-00428.1988
   PubMed Web of Science ®Google Scholar
• Feder, M. E. (1997). Necrotic fruit: A novel model system for thermal ecologists. Journal of Thermal Biology, 22, 1–9. doi:10.1016/S0306-4565(96)00028-9
   Web of Science ®Google Scholar
• Faber, E. S. L., & Sah, P. (2003). Calcium-activated potassium channels: Multiple contributions to neuronal function. The Neuroscientist: A Review Journal Bringing Neurobiology, Neurology and Psychiatry, 9, 181–194. https://doi.org/10.1177/1073858403252673
   PubMed Web of Science ®Google Scholar
• Federico, A., Cardaioli, E., Da Pozzo, P., Formichi, P., Gallus, G. N., & Radi, E. (2012). Mitochondria, oxidative stress and neurodegeneration. Journal of the Neurological Sciences, 322, 254–262. doi:10.1016/j.jns.2012.05.030
   PubMed Web of Science ®Google Scholar
• Francis, S. H., Turko, I. V., & Corbin, J. D. (2001). Cyclic nucleotide phosphodiesterases: Relating structure and function. Progress in Nucleic Acid Research and Molecular Biology, 65, 1–52. https://doi.org/10.1016/S0079-6603(00)65001-8
   PubMed Web of Science ®Google Scholar
• Frolov, R. V., Bagati, A., Casino, B., & Singh, S. (2012). Potassium channels in drosophila: Historical breakthroughs, significance, and perspectives. Journal of Neurogenetics, 26, 275–290. https://doi.org/10.3109/01677063.2012.744990
   PubMed Web of Science ®Google Scholar
• Gerbino, A., Ranieri, M., Lupo, S., Caroppo, R., Debellis, L., Maiellaro, I., … Colella, M. (2009). Ca2+-dependent K + efflux regulates deoxycholate-induced apoptosis of BHK-21 and Caco-2 cells. Gastroenterology, 137, 955. doi:10.1053/j.gastro.2009.03.038
   PubMed Web of Science ®Google Scholar
• Giniatullin, A. R., & Giniatullin, R. A. (2003). Dual action of hydrogen peroxide on synaptic transmission at the frog neuromuscular junction. The Journal of Physiology, 552, 283–293. doi:10.1113/jphysiol.2003.050690
   PubMed Web of Science ®Google Scholar
• Gorczyca, M. G., & Wu, C. F. (1991). Single-channel K + currents in Drosophila muscle and their pharmacological block. The Journal of Membrane Biology, 121, 237–248. https://doi.org/10.1007/BF01951557
   PubMed Web of Science ®Google Scholar
• Gribkoff, V. K., Starrett, J. E., Dworetzky, S. I., Hewawasam, P., Boissard, C. G., Cook, D. A., … Yeola, S. W. (2001). Targeting acute ischemic stroke with a calcium-sensitive opener of maxi-K potassium channels. Nature Medicine, 7, 471–477. doi:10.1038/86546
   PubMed Web of Science ®Google Scholar
• Griguoli, M., Sgritta, M., & Cherubini, E. (2016). Presynaptic BK channels control transmitter release: Physiological relevance and potential therapeutic implications. The Journal of Physiology, 594, 3489–3500. doi:10.1113/JP271841
   PubMed Web of Science ®Google Scholar
• Haddad, G. G. (2006). Tolerance to low O2: Lessons from invertebrate genetic models. Experimental Physiology, 91, 277–282. doi:10.1113/expphysiol.2005.030767
   PubMed Web of Science ®Google Scholar
• Herson, P. S., Lee, K., Pinnock, R. D., Hughes, J., & Ashford, M. L. J. (1999). Hydrogen peroxide induces intracellular calcium overload by activation of a non-selective cation channel in an insulin-secreting cell line. Journal of Biological Chemistry, 274, 833–841. doi:10.1074/jbc.274.2.833
   PubMed Web of Science ®Google Scholar
• Hughes, F. M., Bortner, C. D., Purdy, G. D., & Cidlowski, J. A. (1997). Intracellular K + suppresses the activation of apoptosis in lymphocytes. Journal of Biological Chemistry, 272, 30567–30576. doi:10.1074/jbc.272.48.30567
   PubMed Web of Science ®Google Scholar
• Jenner, P. (2003). Oxidative stress in Parkinson’s disease. Annals of Neurology, 53, S26–S36. discussion S36–8. doi:10.1002/ana.10483
   PubMed Web of Science ®Google Scholar
• Josephson, R. A., Silverman, H. S., Lakatta, E. G., Stern, M. D., & Zweier, J. L. (1991). Study of the mechanisms of hydrogen peroxide and hydroxyl free radical-induced cellular injury and calcium overload in cardiac myocytes. Journal of Biological Chemistry, 266, 2354–2361. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/1846625
   PubMed Web of Science ®Google Scholar
• Juurlink, B. H., & Paterson, P. G. (1998). Review of oxidative stress in brain and spinal cord injury: Suggestions for pharmacological and nutritional management strategies. Journal of Spinal Cord Medicine, 21, 309–334. doi:10.1080/10790268.1998.11719540
   PubMedGoogle Scholar
• Kadas, D., Ryglewski, S., & Duch, C. (2015). Transient BK outward current enhances motoneurone firing rates during Drosophila larval locomotion. The Journal of Physiology, 593, 4871–4888. doi:10.1113/JP271323
   PubMed Web of Science ®Google Scholar
• Karunanithi, S., Barclay, J. W., Robertson, R. M., Brown, I. R., & Atwood, H. L. (1999). Neuroprotection at Drosophila synapses conferred by prior heat shock. The Journal of Neuroscience, 19, 4360–4369. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10341239 doi:10.1523/JNEUROSCI.19-11-04360.1999
   PubMed Web of Science ®Google Scholar
• Komatsu, A., Singh, S., Rathe, P., & Wu, C. F. (1990). Mutational and gene dosage analysis of calcium-activated potassium channels in Drosophila: Correlation of micro- and macroscopic currents. Neuron, 4, 313–321. doi:10.1016/0896-6273(90)90105-O
   PubMed Web of Science ®Google Scholar
• Krans, J. L., Parfitt, K. D., Gawera, K. D., Rivlin, P. K., & Hoy, R. R. (2010). The resting membrane potential of Drosophila melanogaster larval muscle depends strongly on external calcium concentration. Journal of Insect Physiology, 56, 304–313. doi:10.1016/j.jinsphys.2009.11.002
   PubMed Web of Science ®Google Scholar
• Krill, J. L., & Dawson-Scully, K. (2016). CGMP-dependent protein kinase inhibition extends the upper temperature limit of stimulus-evoked calcium responses in motoneuronal boutons of Drosophila melanogaster larvae. PLoS One, 11, e0164114. doi:10.1371/journal.pone.0164114
   PubMed Web of Science ®Google Scholar
• Lancaster, B., & Nicoll, R. A. (1987). Properties of two calcium-activated hyperpolarizations in rat hippocampal neurones. The Journal of Physiology, 389, 187–203. doi:10.1113/jphysiol.1987.sp016653
   PubMed Web of Science ®Google Scholar
• Lawson, K. (2000). Potassium channel openers as potential therapeutic weapons in ion channel disease. Kidney International, 57, 838–845. doi:10.1046/j.1523-1755.2000.00923.x
   PubMed Web of Science ®Google Scholar
• Lee, J., Ueda, A., & Wu, C. F. (2008). Pre- and post-synaptic mechanisms of synaptic strength homeostasis revealed by slowpoke and shaker K + channel mutations in Drosophila. Neuroscience, 154, 1283–1296. doi:10.1016/j.neuroscience.2008.04.043
   PubMed Web of Science ®Google Scholar
• Lee, J., Ueda, A., & Wu, C. F. (2014). Distinct roles of Drosophila cacophony and Dmca1D Ca2+ channels in synaptic homeostasis: Genetic interactions with slowpoke Ca2+-activated BK channels in presynaptic excitability and postsynaptic response. Developmental Neurobiology, 74, 1–15. doi:10.1002/dneu.22120
   PubMed Web of Science ®Google Scholar
• Lehmann, H. F., & Jurkat, R. K. (1999). Voltage-gated ion channels and hereditary disease. Physiological Reviews, 79, 1317–1372. doi:10.1152/physrev.1999.79.4.1317
   PubMed Web of Science ®Google Scholar
• Li, H. J., Zhang, Y. J., Zhou, L., Han, F., Wang, M. Y., Xue, M. Q., & Qi, Z. (2014). Chlorpromazine confers neuroprotection against brain ischemia by activating BKCa channel. European Journal of Pharmacology, 735, 38–43. doi:10.1016/j.ejphar.2014.04.017
   PubMed Web of Science ®Google Scholar
• Liu, Y., Fiskum, G., & Schubert, D. (2002). Generation of reactive oxygen species by the mitochondrial electron transport chain. Journal of Neurochemistry, 80, 780–787. doi:10.1046/j.0022-3042.2002.00744.x
   PubMed Web of Science ®Google Scholar
• Mantegazza, M., Curia, G., Biagini, G., Ragsdale, D. S., & Avoli, M. (2010). Voltage-gated sodium channels as therapeutic targets in epilepsy and other neurological disorders. The Lancet Neurology, 9, 413. doi:10.1016/S1474-4422(10)70059-4
   PubMed Web of Science ®Google Scholar
• McKay, M. C., Dworetzky, S. I., Meanwell, N. A., Olesen, S. P., Reinhart, P. H., Levitan, I. B., … Gribkoff, V. K. (1994). Opening of large-conductance calcium-activated potassium channels by the substituted benzimidazolone NS004. Journal of Neurophysiology, 71, 1873–1882. doi:10.1152/jn.1994.71.5.1873
   PubMed Web of Science ®Google Scholar
• McNaughton, N. C. L., Green, P. J., & Randall, A. D. (2001). Inhibition of human α1E subunit-mediated Ca2+ channels by the antipsychotic agent chlorpromazine. Acta Physiologica Scandinavica, 173, 401–408. doi:10.1046/j.1365-201X.2001.00914.x
   PubMedGoogle Scholar
• Meera, P., Wallner, M., Song, M., & Toro, L. (1997). Large conductance voltage- and calcium-dependent K + channel, a distinct member of voltage-dependent ion channels with seven N-terminal transmembrane segments (S0-S6), an extracellular N terminus, and an intracellular (S9-S10) C terminus. Proceedings of the National Academy of Sciences, 94, 14066–14071. doi:10.1073/pnas.94.25.14066
   PubMed Web of Science ®Google Scholar
• Michelakis, E. D., McMurtry, M. S., Wu, X. C., Dyck, J. R., Moudgil, R., Hopkins, T. A., … Archer, S. L. (2002). Dichloroacetate, a metabolic modulator, prevents and reverses chronic hypoxic pulmonary hypertension in rats: Role of increased expression and activity of voltage-gated potassium channels. Circulation, 105, 244–250. doi:10.1161/hc0202.101974
   PubMed Web of Science ®Google Scholar
• Misener, S. R., Chen, C.-P., & Walker, V. K. (2001). Cold tolerance and proline metabolic gene expression in Drosophila melanogaster. Journal of Insect Physiology, 47, 393–400. doi:10.1016/S0022-1910(00)00141-4
   PubMed Web of Science ®Google Scholar
• Miyata, M., & Smith, J. D. (1996). Apolipoprotein E allele–specific antioxidant activity and effects on cytotoxicity by oxidative insults and β-amyloid peptides. Nature Genetics, 14, 55–61. doi:10.1038/ng0996-55
   PubMed Web of Science ®Google Scholar
• Money, T. G. A., Rodgers, C. I., McGregor, S. M. K., & Robertson, R. M. (2009). Loss of potassium homeostasis underlies hyperthermic conduction failure in control and preconditioned locusts. Journal of Neurophysiology, 102, 285–293. doi:10.1152/jn.91174.2008
   PubMed Web of Science ®Google Scholar
• Nani, F., Cifra, A., & Nistri, A. (2010). Transient oxidative stress evokes early changes in the functional properties of neonatal rat hypoglossal motoneurons in vitro. European Journal of Neuroscience, 31, 951–966. doi:10.1111/j.1460-9568.2010.07108.x
   PubMed Web of Science ®Google Scholar
• Nimigean, C. M., & Magleby, K. L. (1999). The beta subunit increases the Ca2+ sensitivity of large conductance Ca2+-activated potassium channels by retaining the gating in the bursting states. The Journal of General Physiology, 113, 425–440. doi:10.1085/jgp.113.3.425
   PubMed Web of Science ®Google Scholar
• Pallotta, B. S., Magleby, K. L., & Barrett, J. N. (1981). Single channel recordings of Ca2+-activated K + currents in rat muscle cell culture. Nature, 293, 471–474. doi:10.1038/293471a0
   PubMed Web of Science ®Google Scholar
• Pandey, A., Vimal, D., Chandra, S., Saini, S., Narayan, G. K., & Chowdhuri, D. (2014). Long-term dietary exposure to low concentration of dichloroacetic acid promoted longevity and attenuated cellular and functional declines in aged Drosophila melanogaster. Age, 36, 1139–1154. https://doi.org/10.1007/s11357-014-9628-1
   Google Scholar
• Piskorowski, R., & Aldrich, R. W. (2002). Calcium activation of BKCa potassium channels lacking the calcium bowl and RCK domains. Nature, 420, 499–502. doi:10.1038/nature01199
   PubMed Web of Science ®Google Scholar
• Quamme, G. A. (1997). Chlorpromazine activates chloride currents in Xenopus oocytes. Biochimica et Biophysica Acta – Biomembranes, 1324, 18–26. doi:10.1016/S0005-2736(96)00205-2
   PubMed Web of Science ®Google Scholar
• Raffaelli, G., Saviane, C., Mohajerani, M. H., Pedarzani, P., & Cherubini, E. (2004). BK potassium channels control transmitter release at CA3–CA3 synapses in the rat hippocampus. The Journal of Physiology, 557, 147–157. doi:10.1113/jphysiol.2004.062661
   PubMed Web of Science ®Google Scholar
• Renger, J. J., Yao, W. D., Sokolowski, M. B., & Wu, C. F. (1999). Neuronal polymorphism among natural alleles of a cGMP-dependent kinase gene, foraging, in Drosophila. The Journal of Neuroscience, 19, RC28. doi:10.1523/JNEUROSCI.19-19-j0002.1999
   PubMed Web of Science ®Google Scholar
• Shen, K. Z., Lagrutta, A., Davies, N. W., Standen, N. B., Adelman, J. P., & North, R. A. (1994). Tetraethylammonium block of Slowpoke calcium-activated potassium channels expressed in Xenopus oocytes: Evidence for tetrameric channel formation. Pflügers Archive European Journal of Physiology, 426, 440–445 https://doi.org/10.1007/BF00388308
   PubMed Web of Science ®Google Scholar
• Singh, S., & Wu, C. F. (1990). Properties of potassium currents and their role in membrane excitability in Drosophila larval muscle fibers. The Journal of Experimental Biology, 152, 59–76. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/2121887
   PubMed Web of Science ®Google Scholar
• Smith, M. A., Herson, P. S., Lee, K., Pinnock, R. D., & Ashford, M. L. J. (2003). Hydrogen-peroxide-induced toxicity of rat striatal neurones involves activation of a non-selective cation channel. The Journal of Physiology, 547, 417–425. doi:10.1113/jphysiol.2002.034561
   PubMed Web of Science ®Google Scholar
• Stefani, E., Ottolia, M., Noceti, F., Olcese, R., Wallner, M., Latorre, R., & Toro, L. (1997). Voltage-controlled gating in a large conductance Ca2+-sensitive K + channel (hslo). Proceedings of the National Academy of Sciences of the United States of America, 94, 5427–5431. doi:10.1073/pnas.94.10.5427
   PubMed Web of Science ®Google Scholar
• Stewart, B. A., Schuster, C. M., Goodman, C. S., & Atwood, H. L. (1996). Homeostasis of synaptic transmission in Drosophila with genetically altered nerve terminal morphology. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 16, 3877–3886. Retrieved from https://doi.org/10.1523/JNEUROSCI.16-12-03877.1996
   PubMed Web of Science ®Google Scholar
• Vetri, F., Choudhury, M. S. R., Pelligrino, D. A., & Sundivakkam, P. (2014). BKca channels as physiological regulators: A focused review. Journal of Receptor, Ligand and Channel Research, 7, 3–13. https://doi.org/10.2147/JRLCR.S36065
   Google Scholar
• White, R. E., Lee, A. B., Shcherbatko, A. D., Lincoln, T. M., Schonbrunn, A., & Armstrong, D. L. (1993). Potassium channel stimulation by natriuretic peptides through cGMP-dependent dephosphorylation. Nature, 361, 263–266. https://doi.org/10.1038/361263a0
   PubMed Web of Science ®Google Scholar
• Yang, Y., Li, P.-Y., Cheng, J., Mao, L., Wen, J., Tan, X.-Q., … Zeng, X.-R. (2013). Function of BKCa channels is reduced in human vascular smooth muscle cells from Han Chinese patients with hypertension. Hypertension, 61, 519–525. https://doi.org/10.1161/HYPERTENSIONAHA.111.00211
   PubMed Web of Science ®Google Scholar
• Zhang, B., & Ma, J. (2008). SERPINA3K prevents oxidative stress induced necrotic cell death by inhibiting calcium overload. PloS One, 3, e4077. https://doi.org/10.1371/journal.pone.0004077
   PubMed Web of Science ®Google Scholar
• Zhang, J. (2016). Blockade of large conductance Ca(2+) activated K(+) channel may protect neuronal cells from hypoxia mimetic insult and oxidative stress. Acta Poloniae Pharmaceutica, 73, 895–902. Retrieved from https://europepmc.org/abstract/med/29648715
   PubMed Web of Science ®Google Scholar
• Zhou, Y., Schopperle, W. M., Murrey, H., Jaramillo, A., Dagan, D., Griffith, L. C., & Levitan, I. B. (1999). A dynamically regulated 14-3-3, Slob, and Slowpoke potassium channel complex in Drosophila presynaptic nerve terminals. Neuron, 22, 809–818. https://doi.org/10.1016/S0896-6273(00)80739-4
   PubMed Web of Science ®Google Scholar