Ionic Channel Blockage Effect on the Electromechanical Model of Human Gastric Wall Smooth Muscle Cells

Document Type : Research Paper

Authors

1 Ph.D., Department of Biomedical Engineering, Science and Research Branch, Islamic Azad University, Tehran, Iran, h.taghadosi@srbiau.ac.ir

2 Corresponding Author, Professor, Pediatric Neurorehabilitation Research Center, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran, fa.tabatabai@uswr.ac.ir

3 Associate Professor, Department of Biomedical Engineering, Science and Research Branch, Islamic Azad University, Tehran, Iran, jafarnia@srbiau.ac.ir

4 Associate Professor, Department of Electrical and Computer Engineering, New York Institute of Technology, Old Westbury, New York, USA, afarajid@nyit.edu

Abstract

In this paper, a three-dimensional electromechanical model is presented to investigate the effect of calcium and potassium ionic channels on the contractile behavior of human gastric wall smooth muscle cells with the finite element approach. In this model, simultaneous electrical and mechanical interactions of 240-cells and 548-links were considered. Electrophysiological interactions of cells through ion channels with the extrascellular environment and gap junctions with adjacent cells lead to the production and propagation of slow waves in smooth muscle. This wave causes contraction and peristaltic movements in the muscles of the gastric wall. By blocking calcium and potassium ionic channels by pharmacological agents can be improved disorders caused by these movements and contractions and brought them closer to the physiological state.

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Main Subjects


[1]  Huizinga, J.D., and Lammers, W.J., "Gut Peristalsis Is Governed by a Multitude of Cooperating Mechanisms", American Journal of Physiology-Gastrointestinal and Liver Physiology, Vol. 296, No. 1, pp. G1-G8, (2009).
 
[2]  Sanders, K.M., Kito, Y., Hwang, S.J., and Ward, S.M., "Regulation of Gastrointestinal Smooth Muscle Function by Interstitial Cells", Physiology, Vol. 31, No. 5, pp. 316-326, (2016).
 
[3]  Lodish, H., Berk, A., Zipursky, S.L., Matsudaira, P., Baltimore, D., and Darnell, J., "Molecular Cell Biology", 6th Edition, W.H., Freeman, New York, Vol. 4, (2004).
 
[4]  Hanani, M., Farrugia, G., and Komuro, T., "Intercellular Coupling of Interstitial Cells of Cajal in the Digestive Tract", International Review of Cytology, Vol. 242, pp. 249-282, (2005).
[5]  Heidlauf, T., and Röhrle, O., "A Multiscale Chemo-electro-mechanical Skeletal Muscle Model to Analyze Muscle Contraction and Force Generation for Different Muscle Fiber Arrangements", Frontiers in Physiology, Vol. 5, No. 498, pp. 1-14, (2014).
 
[6]  Röhrle, O., Sprenger, M., and Schmitt, S., "A Two-muscle, Continuum-mechanical Forward Simulation of the Upper Limb", Biomechanics and Modeling in Mechanobiology, Vol. 16, No. 3, pp. 743-762, (2017).
 
[7]  Cherubini, C., Filippi, S., Gizzi, A., and Ruiz-Baier, R., "A Note on Stress-driven Anisotropic Diffusion and Its Role in Active Deformable Media", Journal of Theoretical Biology, Vol. 430, pp. 221-228, (2017).
 
[8]  Costabal, F.S., Concha, F.A., Hurtado, D.E., and Kuhl, E., "The Importance of Mechano-electrical Feedback and Inertia in Cardiac Electromechanics", Computer Methods in Applied Mechanics and Engineering, Vol. 320, pp. 352-368, (2017).
 
[9] Tabatabai, F., Arshi, A., Mahmoudian, M., and Janahmadi, M., "Spatiotemporal Wavefront Propagation in 3D Geometric Excitable Heart Tissue", Iranian Journal of Mechanical Engineering, Vol. 6, No. 1, pp. 38-59, (2005).
 
[10] Tabatabai, G., Arshi, A., Mahmoudian, M., and Janahmadi, M., "New Combined Electrochemical Path Modeling of the Heart Based Membrane Ionic Channels", Iranian Journal of Biomedical Engineering, Vol. 1, pp. 77-92, (2004).
 
[11] Sanders, K.M., Koh, S.D., Ro, S., and Ward, S.M., "Regulation of Gastrointestinal Motility—insights from Smooth Muscle Biology", Nature Reviews Gastroenterology and Hepatology, Vol. 9, No. 11, pp. 633-645, (2012).
 
[12] Tse, G., Lai, E.T., Lee, A.P., Yan, B.P., and Wong, S.H., "Electrophysiological Mechanisms of Gastrointestinal Arrhythmogenesis: Lessons from the Heart", Frontiers in Physiology, Vol. 7, No. 230, pp. 1-10, (2016).
 
[13] He, X., "Modeling of the Interaction between Colon and Colonoscope During a Colonoscopy", Ph.D. Thesis, Department of Mechanical Engineering, University of Minnesota, Minneapolis, (2018).
 
[14] Patel, B., Guo, X., Noblet, J., Chambers, S., Gregersen, H., and Kassab, G.S., "Computational Analysis of Mechanical Stress in Colonic Diverticulosis", Scientific Reports, Vol. 10, No. 1, pp. 1-12, (2020).
 
[15] Brandstaeter, S., Gizzi, A., Fuchs, S.L., Gebauer, A.M., Aydin, R.C., and Cyron, C.J., "Computational Model of Gastric Motility with Active‐strain Electromechanics", ZAMM‐Journal of Applied Mathematics and Mechanics/Zeitschrift für Angewandte Mathematik und Mechanik, Vol. 98, No. 12, pp. 2177-2197, (2018).
 
[16] HajHosseini, P., and Takalloozadeh, M., "An Isotropic Hyperelastic Model of Esophagus Tissue Layers Along with Three-dimensional Simulation of Esophageal Peristaltic Behavior", Journal of Bioengineering Research, Vol. 1, No. 2, pp. 12-27, (2019).
 
[17] Liu, D., and Yan, G., "A Multi-layer Finite Element Model Based on Anisotropic Hyperelastic Fiber Reinforcements within Intestinal Walls", Nano Biomedicine and Engineering, Vol. 9, pp. 291-297, (2017).
 
[18] Arrieta, J., Cartwright, J.H., Gouillart, E., Piro, N., Piro, O., and Tuval, I., "Geometric Mixing, Peristalsis, and the Geometric Phase of the Stomach", PloS One, Vol. 10, No. 7, pp. e0130735, (2015).
 
[19] Ferrua, M., and Singh, R., "Modeling the Fluid Dynamics in a Human Stomach to Gain Insight of Food Digestion", Journal of Food Science, Vol. 75, No. 7, pp. R151-R162, (2010).
 
[20] Pal, A., Indireshkumar, K., Schwizer, W., Abrahamsson, B., Fried, M., and Brasseur, J.G., "Gastric Flow and Mixing Studied using Computer Simulation", Proceedings of the Royal Society of London, Series B: Biological Sciences, Vol. 271, No. 1557, pp. 2587-2594, (2004).
 
[21] Taghadosi, H., Tabatabai Ghomsheh, F., Farajidavar, A., Khazaee, F., Hoseinpour, F., and Beshkooh, Z., "Electromechanical Modeling and Simulation of the Physiological State of Human Gastric Wall Smooth Muscle Cells", Computational Sciences and Engineering, Vol. 2, No. 1, pp. 9-19, (2022).
 
[22] Javan-Khoshkholgh, A., and Farajidavar, A., "Simultaneous Wireless Power and Data Transfer: Methods to Design Robust Medical Implants for Gastrointestinal Tract", IEEE Journal of Electromagnetics, RF and Microwaves in Medicine and Biology, Vol. 6, No. 1, pp. 3-15, (2021).
 
[23] Hodgkin, A.L., and Huxley, A.F., "A Quantitative Description of Membrane Current and its Application to Conduction and Excitation in Nerve", The Journal of Physiology, Vol. 117, No. 4, pp. 500-544, (1952).
 
[24] Street, A.M., and Plonsey, R., "Propagation in Cardiac Tissue Adjacent to Connective Tissue: Two-dimensional Modeling Studies", IEEE Transactions on Biomedical Engineering, Vol. 46, No. 1, pp. 19-25, (1999).
 
[25] Harrild, D.M., and Henriquez, C.S., "A Computer Model of Normal Conduction in the Human Atria", Circulation Research, Vol. 87, No. 7, pp. e25-e36, (2000).
 
[26] Poh, Y.C., Corrias, A., Cheng, N., and Buist, M.L., "A Quantitative Model of Human Jejunal Smooth Muscle Cell Electrophysiology", Plos One, Vol. 7, No. 8, pp. e42385, (2012).
 
[27] Corrias, A., and Buist, M.L., "A Quantitative Model of Gastric Smooth Muscle Cellular Activation", Annals of Biomedical Engineering, Vol. 35, No. 9, pp. 1595-1607, (2007).
 
[28] Yeoh, J.W., Corrias, A., and Buist, M.L., "Modelling Human Colonic Smooth Muscle Cell Electrophysiology", Cellular and Molecular Bioengineering, Vol. 10, No. 2, pp. 186-197, (2017).
 
[29] O'Grady, G., Du, P., Cheng, L.K., Egbuji, J.U., Lammers, W.J., Windsor, J.A., and Pullan, A.J., "Origin and Propagation of Human Gastric Slow-wave Activity Defined by High-resolution Mapping", American Journal of Physiology-Gastrointestinal and Liver Physiology, Vol. 299, No. 3, pp. G585-G592, (2010).
[30] Taghadosi, H., Ghomsheh, F.T., Dabanloo, N.J., and Farajidavar, A., "Electrophysiological Modeling of the Effect of Potassium Channel Blockers on the Distribution of Stimulation Wave in the Human Gastric Wall Cells", Journal of Biomechanics, Vol. 127, pp. 110662, (2021).
 
[31] Sanders, K.M., and Ördög, T., "Properties of Electrical Rhythmicity in the Stomach: Handbook of Electrogastrography", New York, Oxford University Press, pp. 13-36, (2004).
 
[32] Lees-Green, R., Du, P., O'Grady, G., Beyder, A., Farrugia, G., and Pullan, A., "Biophysically Based Modeling of the Interstitial Cells of Cajal: Current Status and Future Perspectives", Frontiers in Physiology, Vol. 2, No. 29, pp. 1-19, (2011).
 
[33] Perez-Reyes, E., "Molecular Physiology of Low-voltage-activated T-type Calcium Channels", Physiological Reviews, Vol. 83, No. 1, pp. 117-161, (2003).
 
[34] Hotta, A., Okada, N., and Suzuki, H., "Mibefradil-sensitive Component Involved in the Plateau Potential in Submucosal Interstitial Cells of the Murine Proximal Colon", Biochemical and Biophysical Research Communications, Vol. 353, No. 1, pp. 170-176, (2007).
 
[35] Suzuki, H., and Hirst, G., "Regenerative Potentials Evoked in Circular Smooth Muscle of the Antral Region of Guinea‐pig Stomach", The Journal of physiology, Vol. 517, No. 2, pp. 563-573, (1999).
 
[36] Amberg, G.C., Baker, S.A., Koh, S.D., Hatton, W.J., Murray, K.J., Horowitz, B., and Sanders, K.M., "Characterization of the A‐type Potassium Current in Murine Gastric Antrum", The Journal of Physiology, Vol. 544, No. 2, pp. 417-428, (2002).
 
[37] Lee, J.Y., Ko, E.-j., Ahn, K.D., Kim, S., and Rhee, P.-L., "The Role of K+ Conductances in Regulating Membrane Excitability in Human Gastric Corpus Smooth Muscle", American Journal of Physiology-Gastrointestinal and Liver Physiology, Vol. 308, No. 7, pp. G625-G633, (2015).
 
[38] Sanders, K.M., Koh, S.D., and Ward, S.M., "Organization and Electrophysiology of Interstitial Cells of Cajal and Smooth Muscle Cells in the Gastrointestinal Tract:  Physiology of the Gastrointestinal Tract", 4rd  Edition, Academic Press, Massachusetts, pp. 533-576, (2006).
 
[39] Duridanova, D., Gagov, H., Dimitrov, S., and Boev, K., "Main Components of Voltage-sensitive K+ Currents of the Human Colonic Smooth Muscle Cells", Digestion, Vol. 58, No. 5, pp. 479-488, (1997).
 
[40] Tomalka, A., Borsdorf, M., Böl, M., and Siebert, T., "Porcine Stomach Smooth Muscle Force Depends on History-effects", Frontiers in Physiology, Vol. 8, No. 802, pp. 1-12, (2017).
 
[41] Doost, S.N., Ghista, D., Su, B., Zhong, L., and Morsi, Y.S., "Heart Blood Flow Simulation: A Perspective Review", Biomedical Engineering Online, Vol. 15, No. 1, pp. 1-28, (2016).
 
[42] Niederer, S.A., Lumens, J., and Trayanova, N.A., "Computational Models in Cardiology", Nature Reviews Cardiology, Vol. 16, No. 2, pp. 100-111, (2019).
 
[43] Piersanti, R., Africa, P.C., Fedele, M., Vergara, C., Dedè, L., Corno, A.F., and Quarteroni, A., "Modeling Cardiac Muscle Fibers in Ventricular and Atrial Electrophysiology Simulations", Computer Methods in Applied Mechanics and Engineering, Vol. 373, Article Number. 113468, (2021).
 
[44] Taghadosi, H., Tabatabai Ghomsheh, F., Jafarnia Dabanloo, N., and Farajidavar, A., "A Minimal Electrophysiological Model of Gastric Smooth Muscle Cell Based on Effective Ionic Currents", Journal of Modeling in Engineering, Vol. 19, No. 67, pp. 181-189, (2021).
 
[45] Whittaker, D.G., Clerx, M., Lei, C.L., Christini, D.J., and Mirams, G.R., "Calibration of Ionic and Cellular Cardiac Electrophysiology Models", Wiley Interdisciplinary Reviews: Systems Biology and Medicine, Vol. 12, No. 4, pp. e1482, (2020).
 
[46] Farajidavar, A., "Bioelectronics for Mapping Gut Activity", Brain Research, Vol. 1693, pp. 169-173, (2018).