EXPRESSION PATTERN OF BK CHANNELS ON VARIOUS OXIDATIVE STRESS CONDITIONS IN SKELETAL MUSCLE

Yıl 2022, Cilt: 8 Sayı: 1, 46 - 55, 17.06.2022

Çağıl Coşkun Figen Amber Çiçek Onur Tokgün Işıl Öcal

https://doi.org/10.51477/mejs.1087669

Öz

BK (large conductance Ca2+-activated potassium) channels are expressed in myocytes though changes in their molecular levels in the presence of oxidative stress is not clear, yet. Excessive production of reactive oxygen species leads to many diseases including periodic paralysis. Therefore, determination the molecular effects of various oxidative stress conditions may reveal the possible mechanism and potential therapeutic effects. In the present study, isolated rat soleus muscle where KCNMA1 genes encoding BK channel protein expressed widely in skeletal muscle, were exposed to cyclopiazonic acid (CPA) and also hydrogen peroxide (H2O2) as oxidative stress inducers. Streptozotocin-induced diabetes mellitus model was also used to demonstrate the effects of the endogenous source of oxidative stress. Moreover, NS1619, a BK channel opener was used whether the activation of the channel re-regulate the channel expression back. After the incubation periods, KCNMA1 gene expression levels of each groups were determined by real-time PCR experiments. While CPA and H2O2 decreased the KCNMA1 expression significantly, its expression did not change in systemic diabetes mellitus condition. However, the transcriptional level significantly decreased in diabetes in the presence of H2O2. On the other hand, KCNMA1 expression was re-regulated back to the control’s level by addition of NS1619 in solely hydrogen peroxide groups. The results demonstrated for the first time that acute oxidative stress, rather than systemic conditions, effects the KCNMA1 gene expression level in skeletal muscle. The study was also showed the effects of NS1619 on the regulation of transcriptional levels of BK channel protein in hydrogen peroxide conditions.

Anahtar Kelimeler

Skeletal muscle, BK channels, Oxidative Stress, KCNMA1, NS1619

Kaynakça

• [1] Cui, J., Yang, H., Lee, U.S., "Molecular mechanisms of BK channel activation". Cell Mol Life Sci, 66(5): p. 852-75, 2009.
• [2] Carvalho-de-Souza, J.L., Varanda, W.A., Tostes, R.C., Chignalia, A.Z., "BK Channels in Cardiovascular Diseases and Aging". Aging Dis, 4(1): p. 38-49, 2013.
• [3] Imlach, W.L., Finch, S.C., Miller, J.H., Meredith, A.L., Dalziel, J.E., "A role for BK channels in heart rate regulation in rodents". PLoS One, 5(1): p. e8698, 2010.
• [4] Lai, M.H., Wu, Y., Gao, Z., Anderson, M.E., Dalziel, J.E., Meredith, A.L., "BK channels regulate sinoatrial node firing rate and cardiac pacing in vivo". Am J Physiol Heart Circ Physiol, 307(9): p. H1327-38, 2014.
• [5] Contet, C., Goulding, S.P., Kuljis, D.A., Barth, A.L., "BK Channels in the Central Nervous System". Int Rev Neurobiol, 128: p. 281-342, 2016.
• [6] Wang, Z.W., "Regulation of synaptic transmission by presynaptic CaMKII and BK channels". Mol Neurobiol, 38(2): p. 153-66, 2008.
• [7] Maqoud, F., Cetrone, M., Mele, A., Tricarico, D., "Molecular structure and function of big calcium-activated potassium channels in skeletal muscle: pharmacological perspectives". Physiol Genomics, 49(6): p. 306-317, 2017.
• [8] Layne, J.J., Nausch, B., Olesen, S.P., Nelson, M.T., "BK channel activation by NS11021 decreases excitability and contractility of urinary bladder smooth muscle". Am J Physiol Regul Integr Comp Physiol, 298(2): p. R378-84, 2010.
• [9] Dinardo, M.M., Camerino, G., Mele, A., Latorre, R., Conte Camerino, D., Tricarico, D., "Splicing of the rSlo gene affects the molecular composition and drug response of Ca2+-activated K+ channels in skeletal muscle". PLoS One, 7(7): p. e40235, 2012.
• [10] Pizzino, G., Irrera, N., Cucinotta, M., Pallio, G., Mannino, F., Arcoraci, V., Squadrito, F., Altavilla, D., Bitto, A., "Oxidative Stress: Harms and Benefits for Human Health". Oxid Med Cell Longev, 2017: p. 8416763, 2017.
• [11] Poprac, P., Jomova, K., Simunkova, M., Kollar, V., Rhodes, C.J., Valko, M., "Targeting Free Radicals in Oxidative Stress-Related Human Diseases". Trends Pharmacol Sci, 38(7): p. 592-607, 2017.
• [12] Jackson, M.J., Pollock, N., Staunton, C., Stretton, C., Vasilaki, A., McArdle, A., Oxidative stress in skeletal muscle: Unraveling the potential beneficial and deleterious roles of reactive oxygen species. 2020. p. 713-733.
• [13] Wan, J.-j., Qin, Z., Wang, P.-y., Sun, Y., Liu, X., "Muscle fatigue: general understanding and treatment". Experimental & Molecular Medicine, 49(10): p. e384-e384, 2017.
• [14] Hermann, A., Sitdikova, G.F., Weiger, T.M., "Oxidative Stress and Maxi Calcium-Activated Potassium (BK) Channels". Biomolecules, 5(3): p. 1870-911, 2015.
• [15] DiChiara, T.J., Reinhart, P.H., "Redox modulation of hslo Ca2+-activated K+ channels". J Neurosci, 17(13): p. 4942-55, 1997.
• [16] Barlow, R.S., El-Mowafy, A.M., White, R.E., "H(2)O(2) opens BK(Ca) channels via the PLA(2)-arachidonic acid signaling cascade in coronary artery smooth muscle". Am J Physiol Heart Circ Physiol, 279(2): p. H475-83, 2000.
• [17] Ighodaro, O.M., "Molecular pathways associated with oxidative stress in diabetes mellitus". Biomed Pharmacother, 108: p. 656-662, 2018.
• [18] Qian, L.L., Liu, X.Y., Yu, Z.M., Wang, R.X., "BK Channel Dysfunction in Diabetic Coronary Artery: Role of the E3 Ubiquitin Ligases". Front Physiol, 11: p. 453, 2020.
• [19] Mert, T., Gunay, I., Ocal, I., "Neurobiological effects of pulsed magnetic field on diabetes-induced neuropathy". Bioelectromagnetics, 31(1): p. 39-47, 2010.
• [20] Craner, M.J., Klein, J.P., Renganathan, M., Black, J.A., Waxman, S.G., "Changes of sodium channel expression in experimental painful diabetic neuropathy". Ann Neurol, 52(6): p. 786-92, 2002.
• [21] Malekinejad, H., Akbari, P., Allymehr, M., Hobbenaghi, R., Rezaie, A., "Cyclopiazonic acid augments the hepatic and renal oxidative stress in broiler chicks". Hum Exp Toxicol, 30(8): p. 910-9, 2011.
• [22] Livak, K.J., Schmittgen, T.D., "Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method". Methods, 25(4): p. 402-8, 2001.
• [23] Ransy, C., Vaz, C., Lombès, A., Bouillaud, F., "Use of H(2)O(2) to Cause Oxidative Stress, the Catalase Issue". International journal of molecular sciences, 21(23): p. 9149, 2020.
• [24] Vasilaki, A., Mansouri, A., Van Remmen, H., van der Meulen, J.H., Larkin, L., Richardson, A.G., McArdle, A., Faulkner, J.A., Jackson, M.J., "Free radical generation by skeletal muscle of adult and old mice: effect of contractile activity". Aging Cell, 5(2): p. 109-17, 2006.
• [25] Favero, T.G., Zable, A.C., Abramson, J.J., "Hydrogen peroxide stimulates the Ca2+ release channel from skeletal muscle sarcoplasmic reticulum". J Biol Chem, 270(43): p. 25557-63, 1995.
• [26] Bychkov, R., Pieper, K., Ried, C., Milosheva, M., Bychkov, E., Luft, F.C., Haller, H., "Hydrogen peroxide, potassium currents, and membrane potential in human endothelial cells". Circulation, 99(13): p. 1719-25, 1999.
• [27] Coskun, C., Buyuknacar, H.S., Cicek, F., Gunay, I., "BK channel openers NS1619 and NS11021 reverse hydrogen peroxide-induced membrane potential changes in skeletal muscle". Journal of Receptors and Signal Transduction, 40(5): p. 449-455, 2020.
• [28] Kang, J.H., Woo, J.S., "The Ca2+-activated K+ (BK) Channel-opener NS 1619 Prevents Hydrogen Peroxide-induced Cell Death and Mitochondrial Dysfunction in Retinal Pigment Epithelial Cells". Journal of Life Science, 27(11): p. 1349-1356, 2017.
• [29] Gáspár, T., Katakam, P., Snipes, J.A., Kis, B., Domoki, F., Bari, F., Busija, D.W., "Delayed neuronal preconditioning by NS1619 is independent of calcium activated potassium channels". J Neurochem, 105(4): p. 1115-28, 2008.
• [30] Coskun, C., Tokgun, O., "BK channel opener protects cell viability by regulating reactive oxygen levels in astrocyte cells". General physiology and biophysics, 40(5): p. 409-417, 2021.
• [31] Görlach, A., Bertram, K., Hudecova, S., Krizanova, O., "Calcium and ROS: A mutual interplay". Redox Biol, 6: p. 260-271, 2015.
• [32] Przygodzki, T., Sokal, A., Bryszewska, M., "Calcium ionophore A23187 action on cardiac myocytes is accompanied by enhanced production of reactive oxygen species". Biochim Biophys Acta, 1740(3): p. 481-8, 2005.
• [33] Même, W., Huchet-Cadiou, C., Léoty, C., "Cyclopiazonic acid-induced changes in the contraction and Ca2+ transient of frog fast-twitch skeletal muscle". Am J Physiol, 274(1): p. C253-61, 1998.
• [34] Bonyadi, F., Hasanzadeh, S., Malekinejad, H., "Cyclopiazonic acid induced p53-dependent apoptosis in the testis of mice: Another male related risk factor of infertility". Environ Toxicol, 36(5): p. 903-913, 2021.
• [35] Oeggerli, M., Tian, Y., Ruiz, C., Wijker, B., Sauter, G., Obermann, E., Güth, U., Zlobec, I., Sausbier, M., Kunzelmann, K., Bubendorf, L., "Role of KCNMA1 in Breast Cancer". PLOS ONE, 7(8): p. e41664, 2012.
• [36] O'Malley, D., Harvey, J., "Insulin activates native and recombinant large conductance Ca(2+)-activated potassium channels via a mitogen-activated protein kinase-dependent process". Mol Pharmacol, 65(6): p. 1352-63, 2004.
• [37] Olsen, M.L., Weaver, A.K., Ritch, P.S., Sontheimer, H., "Modulation of glioma BK channels via erbB2". J Neurosci Res, 81(2): p. 179-89, 2005.
• [38] Good, A.L., Stoffers, D.A., "Stress-Induced Translational Regulation Mediated by RNA Binding Proteins: Key Links to β-Cell Failure in Diabetes". Diabetes, 69(4): p. 499-507, 2020.
• [39] Cicek, F.A., Toy, A., Tuncay, E., Can, B., Turan, B., "Beta-blocker timolol alleviates hyperglycemia-induced cardiac damage via inhibition of endoplasmic reticulum stress". J Bioenerg Biomembr, 46(5): p. 377-87, 2014.
• [40] Wellen, K.E., Thompson, C.B., "Cellular Metabolic Stress: Considering How Cells Respond to Nutrient Excess". Molecular Cell, 40(2): p. 323-332, 2010.
• [41] Nieves-Cintrón, M., Syed, A.U., Buonarati, O.R., Rigor, R.R., Nystoriak, M.A., Ghosh, D., Sasse, K.C., Ward, S.M., Santana, L.F., Hell, J.W., Navedo, M.F., "Impaired BK(Ca) channel function in native vascular smooth muscle from humans with type 2 diabetes". Sci Rep, 7(1): p. 14058, 2017.
• [42] Gáspár, T., Domoki, F., Lenti, L., Katakam, P.V.G., Snipes, J.A., Bari, F., Busija, D.W., "Immediate neuronal preconditioning by NS1619". Brain research, 1285: p. 196-207, 2009