Protein pattern formation induced by the joint effect of noise and delay in a multi-cellular system
Mathematical modelling of natural phenomena, Tome 17 (2022), article no. 16.

Voir la notice de l'article provenant de la source EDP Sciences

We explore the combined effect of the intrinsic noise and time delay on the spatial pattern formation within the framework of a multi-scale mobile lattice model mimicking two-dimensional epithelium tissues. Every cell is represented by an elastic polygon changing its form and size under pressure from the surrounding cells. The model includes the procedure of minimization of the potential energy of tissue. The protein fluctuations in the tissue are driven by transcription/translation processes in epithelial cells exchanging chemical and mechanical signals. Network architecture includes a simple autorepressor model with time-delayed negative feedback, in which the only gene defines the oscillatory activity. Simultaneously, the expressed protein of the autorepressor acts as a positive regulator of the signaling protein by activating its transcription. The signaling species is assumed to spread from one cell to the other by the diffusion mechanism. We provide both deterministic and stochastic descriptions. The numerical simulation of spatially-extended stochastic oscillations is performed using a generalized Gillespie algorithm. We developed this method earlier to account for the non-Markovian properties of random biochemical events with delay. Finally, we demonstrate that time delay, intrinsic noise, and spatial signaling can cause a system to develop the protein pattern even when its deterministic counterpart exhibits no pattern formation.
DOI : 10.1051/mmnp/2022011

Dmitry Bratsun 1

1 Department of Applied Physics, Perm National Research Polytechnic University, 614990 Perm, Russia
@article{MMNP_2022_17_a9,
     author = {Dmitry Bratsun},
     title = {Protein pattern formation induced by the joint effect of noise and delay in a multi-cellular system},
     journal = {Mathematical modelling of natural phenomena},
     eid = {16},
     publisher = {mathdoc},
     volume = {17},
     year = {2022},
     doi = {10.1051/mmnp/2022011},
     language = {en},
     url = {http://geodesic.mathdoc.fr/articles/10.1051/mmnp/2022011/}
}
TY  - JOUR
AU  - Dmitry Bratsun
TI  - Protein pattern formation induced by the joint effect of noise and delay in a multi-cellular system
JO  - Mathematical modelling of natural phenomena
PY  - 2022
VL  - 17
PB  - mathdoc
UR  - http://geodesic.mathdoc.fr/articles/10.1051/mmnp/2022011/
DO  - 10.1051/mmnp/2022011
LA  - en
ID  - MMNP_2022_17_a9
ER  - 
%0 Journal Article
%A Dmitry Bratsun
%T Protein pattern formation induced by the joint effect of noise and delay in a multi-cellular system
%J Mathematical modelling of natural phenomena
%D 2022
%V 17
%I mathdoc
%U http://geodesic.mathdoc.fr/articles/10.1051/mmnp/2022011/
%R 10.1051/mmnp/2022011
%G en
%F MMNP_2022_17_a9
Dmitry Bratsun. Protein pattern formation induced by the joint effect of noise and delay in a multi-cellular system. Mathematical modelling of natural phenomena, Tome 17 (2022), article  no. 16. doi : 10.1051/mmnp/2022011. http://geodesic.mathdoc.fr/articles/10.1051/mmnp/2022011/

[1] D. Austin, M. Allen, J. Mccollum Gene network shaping of inherent noise spectra Nature 2006 608 611

[2] M. Banerjee, V. Volpert Stochastic intracellular regulation can remove oscillations in a model of tissue growth Math. Med. Biol. 2020 551 568

[3] A. Becskei, L. Serrano Engineering stability in gene networks by autoregulation Nature 2000 590 593

[4] J. Bonnet, P. Yin, M.E. Ortiz, P. Subsoontorn, D. Endy Amplifying genetic logic gates Science 2013 599 603

[5] D. Bratsun, D. Volfson, J. Hasty, L. Tsimring Non-Markovian processes in Gene Regulation. In Noise in Complex Systems and Stochastic Dynamics III edited by Laszlo B. Kish, Katja Lindenberg Proc. SPIE 2005 210 219

[6] D. Bratsun, D. Volfson, J. Hasty, L.S. Tsimring Delay-induced stochastic oscillations in gene regulation Proc. Natl. Acad. Sci. U.S.A. 2005 14593 14598

[7] D. Bratsun and A. Zakharov, Adaptive numerical simulations of reaction-diffusion systems with history and time-delayed feedback. In Vol. 8 of Emergence, Complexity and Computation edited by A. Sanayei, I. Zelinka, and O.E. Rossler. Springer, Heidelberg (2014) 191–201.

[8] D. Bratsun and A. Zakharov, Deterministic modeling spatio-temporal dynamics of delay-induced circadian oscillations in Neurospora crassa. In Vol. 8 of Emergence, Complexity and Computation edited by A. Sanayei, I. Zelinka, and O.E. Rossler. Springer, Heidelberg (2014) 179–189.

[9] D.A. Bratsun, D.V. Merkuriev, A.P. Zakharov, L.P. Pismen Multiscale modeling of tumor growth induced by circadian rhythm disruption in epithelial tissue J. Biol. Phys. 2016 107 132

[10] D.A. Bratsun, I.V. Krasnyakov, L.M. Pismen Biomechanical modeling of invasive breast carcinoma under a dynamic change in cell phenotype: collective migration of large groups of cells Biomech. Model. Mechanobiol. 2020 723 743

[11] K. Burrage, P.M. Burrage, A. Leier, T. Marquez-Lago and D.V. Nicolau, Stochastic simulation for spatial modelling of dynamic processes in a living cell. In Design and Analysis of Biomolecular Circuits: Engineering Approaches to Systems and Synthetic Biology edited by H. Koeppl et al.. Springer, Heidelberg (2011) 43–62.

[12] X. Cai Exact stochastic simulation of coupled chemical reactions with delays J. Chem. Phys. 2007 124108

[13] R. Daniel, J.R. Rubens, R. Sarpeshkar, T.K. Lu Synthetic analog computation in living cells Nature 2013 619 623

[14] T. Danino, O. Mondragön-Palomino, L. Tsimring, J. Hasty A synchronized quorum of genetic clocks Nature 2010 326 330

[15] D. Denault, J. Loros, J. Dunlap WC-2 mediates WC-1—FRQ interaction within the PAS protein-linked circadian feedback loop of Neurospora EMBO J. 2001 109 117

[16] M.B. Elowitz, S. Leibler A synthetic oscillatory network of transcriptional regulators Nature 2000 335 338

[17] R. Farhadifar, J.C. Roper, B. Aigouy, S. Eaton, F. Jülicher The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing Curr. Biol. 2007 2095 2104

[18] A.E. Friedland, T.K. Lu, X. Wang, D. Shi, G. Church, J.J. Collins Synthetic gene networks that count Science 2009 1199 1202

[19] E. Fung, W.W. Wong, J.K. Suen, T. Bulter, S. Lee, J.C. Liao A synthetic gene-metabolic oscillator Nature 2005 118 122

[20] D.T. Gillespie Exact stochastic simulation of coupled chemical reactions J. Phys. Chem. 1977 2340 2361

[21] D. Gonze, S. Bernard, C. Waltermann, A. Kramer, H. Herzel Spontaneous synchronization of coupled circadian oscillators Biophys. J. 2005 120 129

[22] D. Gonze, P. Ruoff The Goodwin Oscillator and its Legacy Acta Biotheor. 2021 857 874

[23] B.C. Goodwin Oscillatory behavior in enzymatic control processes Adv. Enzyme Regul. 1965 425 438

[24] J.S. Griffith Mathematics of cellular control processes. I. Negative feedback to one gene J. Theor. Biol. 1968 202 208

[25] D.J. Higham Modeling and simulating chemical reactions SIAM Rev. 2008 347 368

[26] H. Honda, T. Nagai, M. Tanemura Two different mechanisms of planar cell intercalation leading to tissue elongation Dev. Dyn. 2008 1826 1836

[27] T. Jia, R.V. Kulkarni Intrinsic noise in stochastic models of gene expression with molecular memory and bursting Phys. Rev. Lett. 2011 058102

[28] M. Kaern, T.C. Elston, W.J. Blake, J.J. Collins Stochasticity in gene expression: from theories to phenotypes Nat. Rev. Genet. 2005 451 464

[29] C.L. Kelly A.W. K. Harris, H. Steel, E.J. Hancock, J.T. Heap and A. Papachristodoulou, Synthetic negative feedback circuits using engineered small RNAs Nucl. Acids Res. 2018 9875 9889

[30] T.B. Kepler, T.C. Elston Stochasticity in transcriptional regulation: origins, consequences, and mathematical representations Biophys. J. 2001 3116 3136

[31] I.V. Krasnyakov, D.A. Bratsun, L.M. Pismen Mathematical modelling of epithelial tissue growth Russ. J. Biomech. 2020 375 388

[32] A. Koseska, E. Ullner, E. Volkov, J. Kurths, J. Garcia-Ojalvo Cooperative differentiation through clustering in multicellular populations J. Theor. Biol. 2010 189 202

[33] K. Lee, J.J. Loros, J.C. Dunlap Interconnected feedback loops in the Neurospora circadian system Science 2000 107 110

[34] C. Lemerle, B. Di Ventura, L. Serrano Space as the final frontier in stochastic simulations of biological systems FEBS Lett. 2005 1789 1794

[35] C.-W. Li, B.-S. Chen Stochastic spatio-temporal dynamic model for gene/protein interac-tion network in early drosophila development Gene Regul. Syst. Biol. 2009 191 210

[36] T.T. Marquez-Lago, A. Leier, K. Burrage Probability distributed time delays: integrating spatial effects into temporal models BMC Syst. Biol. 2010 19

[37] N. Masuda, L.E.C. Rocha A gillespie algorithm for non-Markovian stochastic processes SIAM Rev. 2018 95 115

[38] D.V. Nicolau, K. Burrage Stochastic simulation of chemical reactions in spatially complex media Comput. Math. Appl. 2008 1007 1018

[39] L. Pagani, E.A. Semenova, E. Moriggi, V.L. Revell, L.M. Hack The physiological period length of the human circadian clock in vivo is directly proportional to period in human fibroblasts PLoS ONE 2010 e13376

[40] J. Pahle Biochemical simulations: stochastic, approximate stochastic and hybrid approaches Brief Bioinform. 2009 53 64

[41] J.M. Pedraza, J. Paulsson Effects of molecular memory and bursting on fluctuations in gene expression Science 2008 339 343

[42] L. Potvin-Trottier, N.D. Lord, G. Vinnicombe, J. Paulsson Synchronous long-term oscillations in a synthetic gene circuit Nature 2016 514 517

[43] D.C. Prasher, V.K. Eckenrode, W.W. Ward, F.G. Prendergast, M.J. Cormier Primary structure of the Aequorea victoria green-fluorescent protein Gene 1992 229 33

[44] N. Rosenfeld, J.W. Young, U. Alon, P.S. Swain, M.B. Elowitz Gene regulation at the single-cell level Science 2005 1962 1965

[45] M. Salm, L.M. Pismen Chemical and mechanical signaling in epithelial spreading Phys. Biol. 2012 026009

[46] K. Sriram, M.S. Gopinathan A two variable delay model for the circadian rhythm of Neurospora crassa J. Theor. Biol. 2004 23 38

[47] A. Stephanou, V. Volpert Hybrid Modelling in Cell Biology Math. Model. Nat. Phenom. 2015 1 3

[48] T. Szekely, K. Burrage Stochastic simulation in systems biology Comput. Struct. Biotechnol. J. 2014 14 25

[49] M. Tigges, T.T. Marquez-Lago, J. Stelling, M.A. Fussenegger A tunable synthetic mammalian oscillator Nature 2009 309 312

[50] T.M. Touaoula, M.N. Frioui, N. Bessonov, V. Volpert Dynamics of solutions of a reaction-diffusion equation with delayed inhibition Discr. Continu. Dyn. Syst. 2020 2425 2442

[51] L.S. Tsimring Noise in biology Rep. Prog. Phys. 2014 026601

[52] E. Ullner, A. Zaikin, E.I. Volkov, J. Garcia-Ojalvo Multistability and clustering in a popula-tion of synthetic genetic oscillators via phase-repulsive cell-to-cell communication Phys. Rev. Lett. 2007 148103

[53] C.L. Vestergaard, M. Genois Temporal Gillespie algorithm: Fast simulation of contagion processes on time-varying networks PLoS Comput. Biol. 2015 e1004579

[54] S.H. Yoo, S. Yamazaki, P.L. Lowrey, K. Shimomura, C.H. Ko, E.D. Buhr PERIOD2: LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues Proc. Natl. Acad. Sci. U.S.A. 2004 5339 5346

[55] J. Zhang, T. Zhou Markovian approaches to modeling intracellular reaction processes with molecular memory Proc. Natl. Acad. Sci. U.S.A. 2019 23542 23550

Cité par Sources :