Abstract
Two-dimensional Ca\(^{2+}\) oscillations are investigated in a cell network in the presence of bidirectional paracrine signaling interactions. The proposed model relies on Ca\(^{2+}\)-induced Ca\(^{2+}\) release, in which Ca\(^{2+}\)-stimulated degradation of inositol 1,4,5-triphosphate (IP\(_3\)) by a3-kinase plays a significant role. Via predictions from the synchronization factor R in the parameter domain, the propagation of intercellular Ca\(^{2+}\) wave is numerically studied. Large values of external stimulus are required for weak paracrine coupling to support synchronization, while the latter takes place for strong coupling when the hormonal stimulus is weak. Moreover, the rate of linear leak of Ca\(^{2+}\) from the endoplasmic reticulum to the cytosol favors synchronous states when the paracrine coupling is weak. Considering particularly weak values of the synchronization factor, importance is given to the effect of paracrine signaling. Different scenarios are recorded, especially the appearance of spiral Ca\(^{2+}\) waves and their disintegration to turbulent patterns under strong paracrine coupling. Additionally, weak paracrine coupling gives rise to target Ca\(^{2+}\) waves. It is also reported that a suitable balance between the IP\(_3\) degradation and the cell’s degree of stimulus is necessary for the robustness of spiral waves to be effective under appropriate paracrine coupling strength.
Similar content being viewed by others
Data availability
The simulation data related to the current study are not publicly available due to but can be obtained from the corresponding author, CBT, on reasonable request.
References
Berridge, M.J.: Inositol trisphosphate and calcium signaling mechanisms. Biochimi. Biophys. Acta 1793, 933 (2009)
Mikoshiba, K.: IP3 receptor/Ca\(^{2+}\) channel: from discovery to new signaling concepts. J. Neurochem. 102, 1426 (2007)
Berridge, M.J., Bootman, M.D., Roderick, H.L.: Calcium signaling: dynamics, homeostasis and remodelling. Nature Rev. Mol. Cell Biol. 4, 517 (2003)
Clapham, D.: Calcium signaling. Cell 131, 1047 (2007)
Cui, C., Merritt, R., Fu, L., Pan, Z.: Targeting calcium signaling in cancer therapy. Acta Pharm. Sin. B 7, 3 (2017)
Chang, Y., Funk, M., Roy, S., Stephenson, E., et al.: Developing a mathematical model of intracellular calcium dynamics for evaluating combined anticancer effects of Afatinib and RP4010 in esophageal cancer. Int. J. Mol. Sci. 23, 1763 (2022)
Falcke, M.: Reading the patterns in living cells - the physics of Ca\(^{2+}\) signaling. Adv. Phys. 53, 255 (2004)
Berridge, M.J.: Inositol trisphosphate and Ca\(^{2+}\) signalling. Nature 361, 315 (1993)
Rey, O., Young, S.H., Jacamo, R., Moyer, M.P., Rozengurt, E.: Extracellular calcium-sensing receptor stimulation in human colonic epithelial cells induces intracellular calcium oscillations and proliferation inhibition. J. Cell. Physiol. 225, 73 (2010)
Ridgway, E.B., Gilkey, J.C., Jaffe, L.F.: Free calcium increases explosively in activating medaka eggs. Adv. Physiol. 74, 623 (1977)
Lipp, P., Niggli, E.: Microscopic spiral waves reveal positive feedback in subcellular calcium signaling. Biophys. J . 65, 2272 (1993)
Sanderson, M.J., Charles, A.C., Boitano, S., Dirksen, E.R.: Mechanisms and function of intercellular calcium signaling. Mol. Cell. Endocrinol. 98, 173 (1994)
Robb-Gaspers, L.D., Thomas, A.P.: Coordination of Ca\({2+}\) signaling by intercellular propagation of Ca\(^{2+}\) waves in the intact liver. J. Biol. Chem. 270, 8102 (1995)
Thomas, A.P., Robb-Gaspers, L.D., Rooney, T.A., Hajnoczky, G., Renard- Rooney, D.C., Lin, C.: Spatial organization of oscillating calcium signals in liver. Biochem. Soc. Trans. 23, 642 (1995)
Harris-White, M.E., Zanotti, S.A., Frautschy, S.A., Charles, A.C.: Spiral intercellular calcium waves in hippocampal slice cultures. J. Neurophysiol. 79, 1045 (1998)
Putney, J., Bird, G.: The inositol phosphate-calcium signaling system in nonexcitable cells. Endocr. Rev. 14, 610 (1993)
Cornell-Bell, A.H., Finkbeiner, S.M., Cooper, M.S., Smith, S.J.: Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247, 470 (1990)
Charles, A.C., Merrill, J.E., Dirksen, E.R., Sanderson, M.J.: Intercellular signaling in glial cells: calcium waves and oscillations in response to mechanical stimulation and glutamate. Neuron 6, 983 (1991)
Charles, A.: Intercellular calcium waves in glia. Glia 24, 39 (1998)
Venance, L., Piomelli, D., Glowinski, J., Giaume, C.: Inhibition by anandamide of gap junctions and intercellular calcium signalling in striatal astrocytes. Nature 376, 590 (1995)
Giaume, C., Venance, L.: Intercellular calcium signaling and gap junctional communication in astrocytes. Glia 24, 50 (1998)
Fields, R.D., Stevens-Graham, B.: Neuroscience-new insights into neuron-glia communication. Science 298, 556 (2002)
Allen, N.J., Barres, B.A.: Glia-more than just brain glue. Nature 457, 675 (2009)
Hashimura, H., Morimoto, Y.V., Hirayama, Y., Ueda, M.: Calcium responses to external mechanical stimuli in the multicellular stage of Dictyostelium discoideum. Sci. Rep. 12, 12428 (2022)
Newman, E.A.: Propagation of intercellular calcium waves in retinal astrocytes and muller cells. J. Neurosci. 21, 2215 (2001)
Newman, E.A., Zahs, K.R.: Calcium waves in retinal glial cells. Science 275, 844 (1997)
Scemes, E., Suadicani, S.O., Spray, D.C.: Intercellular communication in spinal cord astrocytes: fine-tuning between gap junctions and P2 nucleotide receptors in calcium wave propagation. J. Neurosci. 20, 1435 (2000)
Kaouri, K., K., Maini, P. K., Skourides, P. A., Christodoulou, N., Chapman, S. J.: A simple mechanochemical model for calcium signalling in embryonic epithelial cells. J. Math. Biol. 78, 2059 (2019)
Katerina Kaouri, K., Méndez, P.E., Ruiz-Baier, R.: Mechanochemical models for calcium waves in embryonic epithelia. Viet. J. Math. (2022). https://doi.org/10.1007/s10013-022-00579-y
Dupont, G., Tordjmann, T., Clair, C., Swillens, S., Claret, M., Combettes, L.: Mechanism of receptor-oriented intercellular calcium wave propagation in hepatocytes. FASEB J. 14, 279 (2000)
Höfer, Th.: Model of intercellular calcium oscillations in hepatocytes: synchronization of heterogeneous cells. Biophys. J . 77, 1244 (1999)
Höfer, Th., Politi, A., Heinrich, R.: Intercellular Ca\(^{2+}\) wave propagation through gap-junctional Ca\(^{2+}\) diffusion: a theoretical study. Biophys. J . 80, 75 (2001)
Manhas, N., Anbazhagan, N.: A mathematical model of intricate calcium dynamics and modulation of calcium signalling by mitochondria in pancreatic acinar cells. Chaos Solit. Fract. 145, 110741 (2021)
Agarwal, R., Kritika, Purohit, S. D.: Mathematical model pertaining to the effect of buffer over cytosolic calcium concentration distribution. Chaos Solit. Fract. 143, 110610 (2021)
Gracheva, M.E., Toral, R., Gunton, J.D.: Stochastic effects in intercellular calcium spiking in hepatocytes. J. Theor. Biol. 212, 111 (2001)
Friedhoff, V.N., Ramlow, L., Lindner, B., Falcke, M.: Models of stochastic Ca\(^{2+}\) spiking-Established approaches and inspirations from models of neuronal spikes. Eur. Phys. J. Spec. Top. 230, 2911 (2021)
Bär, M., Falcke, M., Levine, H., Tsimring, L.S.X.: Discrete stochastic modeling of calcium channel dynamics. Phys. Rev. Lett. 84, 5664 (2000)
Falcke, M., Tsimring, L., Levine, H.: Stochastic spreading of intracellular Ca\(^{2+}\) release. Phys. Rev. E 62, 2636 (2000)
Hassinger, T.D., Guthrie, P.B., Atkinson, P.B., Bennett, M.V., Kater, S.B.: An extracellular signaling component in propagation of astrocytic calcium waves. Proc. Natl. Acad. Sci. U.S.A. 93, 13268 (1996)
Höfer, A.M., Curci, S., Doble, M.A., Brown, M.E., Soybel, D.I.: Intercellular communication mediated by the extracellular calcium-sensing receptor. Nat. Cell Biol. 2, 392 (2000)
Kepseu, W.D., Woafo, P.: Intercellular waves propagation in an array of cells coupled through paracrine signaling: a computer simulation study. Phys. Rev. E 76, 041912 (2006)
Goldbeter, A., Dupont, G., Berridge, M.J.: Minimal model for signal-induced Ca\(^{2+}\) oscillations and for their frequency encoding through protein phosphorylation. Proc. Natl. Acad. Sci. USA 87, 1461 (1990)
Kepseu, W.D., Woafo, P.: Long-range interaction effects on calcium-wave propagation. Phys. Rev. E 78, 011922 (2008)
Tabi, C.B., Maïna, I., Mohamadou, A., Ekobena Fouda, H.P., Kofané, T.C.: Wave instability of intercellular Ca\(^{2+}\) oscillations. Europhys. Lett. 106, 18005 (2014)
Tabi, C.B., Maïna, I., Mohamadou, A., Ekobena Fouda, H.P., Kofané, T.C.: Long- range intercellular Ca\(^{2+}\) wave patterns. Phys. A 435, 1 (2015)
Tabi, C.B., Etémé, A.S., Mohamadou, A., Kofané, T.C.: Oscillating two-dimensional Ca\(^{2+}\) waves in cell networks with bidirectional paracrine signaling. Waves Rand. Complex Med 31, 1028 (2021)
Houart, G., Dupont, G., Goldbeter, A.: Bursting, chaos and birhythmicity originating from self-modulation of the Inositol 1,4,5-trisphosphate signal in a model for intracellular Ca\(^{2+}\) oscillations. Bull. Math. Biol. 61, 507 (1999)
Sabir, Z.: Stochastic numerical investigations for nonlinear three-species food chain system. Int. J. Biomath. 15, 2250005 (2022)
Sabir, Z.: Neuron analysis through the swarming procedures for the singular two-point boundary value problems arising in the theory of thermal explosion. Eur. Phys. J. Plus 137, 638 (2022)
Sabir, Z., Baleanu, D., Ali, M.R., Sadat, R.: A novel computing stochastic algorithm to solve the nonlinear singular periodic boundary value problems. Int. J. Comput. Math. 99, 2091 (2022)
Sabir, Z., Ali, M. R., Sadat, R.: Gudermannian neural networks using the optimization procedures of genetic algorithm and active set approach for the three-species food chain nonlinear model. J. Amb. Intel. Human. Comput. Doi: doi.org/10.1007/s12652-021-03638-3
Sabir, Z., Raja, M.A.Z., Sánchez, Y.G.: Solving an infectious disease model considering its anatomical variables with stochastic numerical procedures. J. Health. Eng. 2022, 3774123 (2022)
Wang, Q., Duan, Z., Perc, M., Chen, G.: Synchronization transitions on small-world neuronal networks: effects of information transmission delay and rewiring probability. Europhys. Lett. 83, 50008 (2008)
Wang, Q., Perc, M., Duan, Z., Chen, G.: Synchronization transitions on scale-free neuronal networks due to finite information transmission delays. Phys. Rev. E 80, 026206 (2009)
Ma, J., Tang, J., Zhang, A., Jia, Y.: Robustness and breakup of the spiral wave in a two-dimensional lattice network of neurons. Sci. China Phys. Mech. Astron. 53, 672 (2010)
Shafiei, M., Parastesh, F., Jalili, M., Jafari, S., Perc, M., Slavinec, M.: Effects of partial time delays on synchronization patterns in Izhikevich neuronal networks. Eur. Phys. J. B 92, 36 (2019)
Majhi, S., Perc, M., Ghosh, D.: Chimera states in a multilayer network of coupled and uncoupled neurons. Chaos 27, 073109 (2017)
Majhi, S., Perc, M., Ghosh, D.: Chimera states in uncoupled neurons induced by a multilayer structure. Sci. Rep. 6, 39033 (2016)
Ma, J., Xu, Y., Wang, C., Jin, W.: Pattern selection and self-organization induced by random boundary initial values in a neuronal network. Phys. A 461, 586 (2016)
Tabi, C.B., Etémé, A.S., Kofané, T.C.: Unstable cardiac multi-spiral waves in a FitzHugh-Nagumo soliton model under magnetic flow effect. Nonl. Dyn. 100, 3799 (2020)
Etémé, A.S., Tabi, C.B., Mohamadou, A., Kofané, T.C.: Elimination of spiral waves in a two-dimensional Hindmarsh-Rose neural network under long-range interaction effect and frequency excitation. Phys. A 533, 122037 (2019)
Wang, C., Lv, M., Alsaedi, A., Ma, J.: Synchronization stability and pattern selection in a memristive neuronal network. Chaos 27, 113108 (2017)
Ma, J., Tang, J., Wang, C.-N., Jia, Y.: Propagation and synchronization of Ca\(_{2+}\) spiral waves in excitable media. Int. J. Bifurc. Chaos 21, 587 (2011)
Busa, W.B., Ferguson, J.E., Joseph, S.K., Williamson, J.R., Nuccitelli, R.: Activation of frog (Xenopus laevis) eggs by inositol trisphosphate I. Characterization of Ca\(^{2+}\) release from intracellular stores. J. Cell Biol. 101, 677 (1985)
Schoch, A., Pahle, J.: Requirements for band-pass activation of Ca\(^{2+}-\) sensitive proteins such as NFAT. Biophys. Chem. 245, 41 (2019)
Acknowledgements
CBT thanks the Kavli Institute for Theoretical Physics (KITP), University of California Santa Barbara (USA), where this work was supported in part by the National Science Foundation Grant no.NSF PHY-1748958, NIH Grant no.R25GM067110, and the Gordon and Betty Moore Foundation Grant no.2919.01.
Funding
The authors have not disclosed any funding.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Tiayo, T.K., Etémé, A.S., Tabi, C.B. et al. Nonlinear dynamics of inositol 1,4,5-trisphosphate-induced Ca\(^{2+}\) patterns in two-dimensional cell networks with paracrine signaling interaction. Nonlinear Dyn 111, 12593–12606 (2023). https://doi.org/10.1007/s11071-023-08491-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11071-023-08491-x