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Interactions Between Pattern Formation and Domain Growth

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Abstract

In this paper we develop a theoretical framework for investigating pattern formation in biological systems for which the tissue on which the spatial pattern resides is growing at a rate which is itself regulated by the diffusible chemicals that establish the spatial pattern. We present numerical simulations for two cases of interest, namely exponential domain growth and chemically controlled growth. Our analysis reveals that for domains undergoing rapid exponential growth dilution effects associated with domain growth influence both the spatial patterns that emerge and the concentration of chemicals present in the domain. In the latter case, there is complex interplay between the effects of the chemicals on the domain size and the influence of the domain size on the formation of patterns. The nature of these interactions is revealed by a weakly nonlinear analysis of the full system. This yields a pair of nonlinear equations for the amplitude of the spatial pattern and the domain size. The domain is found to grow (or shrink) at a rate that depends quadratically on the pattern amplitude, the particular functional forms used to model the local tissue growth rate and the kinetics of the two diffusible species dictating the resulting behaviour.

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References

  • Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K., Watson, J.D., 1994. Molecular Biology of the Cell. Garland Publishing, New York.

    Google Scholar 

  • Alison, M.R., Sarraf, C.E., 1997. Understanding Cancer. Cambridge University Press, Cambridge, New York and Melbourne.

    Google Scholar 

  • Benson, D.L., Maini, P.K., Sherratt, J.A., 1998. Unravelling the Turing bifurcation using spatially varying diffusion coefficients. J. Math. Biol. 37, 381–417.

    Article  MATH  MathSciNet  Google Scholar 

  • Benson, D.L., Sherratt, J.A., Maini, P.K., 1993. Diffusion driven instability in an inhomogeneous domain. Bull. Math. Biol. 55, 365–384.

    Article  MATH  Google Scholar 

  • Breward, C.J.W., Byrne, H.M., Lewis, C.E., 2002. The role of cell—cell interactions in a two-phase model for avascular tumour growth. J. Math. Biol. 45, 125–152.

    Article  PubMed  MATH  MathSciNet  Google Scholar 

  • Byrne, H.M., Chaplain, M.A.J., 1995. Growth of nonnecrotic tumors in the presence and absence of inhibitors. Math. Biosci. 130, 151–181.

    Article  PubMed  MATH  Google Scholar 

  • Byrne, H.M., Chaplain, M.A.J., 1997. Free boundary value problems associated with the growth and development of multicellular spheroids. Eur. J. Appl. Math. 8, 639–658.

    Article  MATH  MathSciNet  Google Scholar 

  • Byrne, H.M., Chaplain, M.A.J., 1998. Necrosis and apoptosis: Distinct cell loss mechanisms in a mathematical model of avascular tumour growth. J. Theor. Med. 1, 223–235.

    Article  MATH  Google Scholar 

  • Byrne, H.M., Matthews, P.C., 2002. Asymmetric growth of models of avascular solid tumours: exploiting symmetries. IMA J. Math. Appl. Med. Biol. 19, 1–29.

    Article  PubMed  MATH  Google Scholar 

  • Campbell, J.W., Pollack, I.F., 1997. Growth factors in gliomas: Antisense and dominant negative mutant strategies. J. Neuro-Oncol. 35, 275–285.

    Article  Google Scholar 

  • Casciari, J.J., Sotirchos, S.V., Sutherland, R.M., 1992. Mathematical modelling of microenvironment and growth in EMT6/Ro multicellular tumour spheroids. Cell Prolif. 25, 1–22.

    PubMed  Google Scholar 

  • Chaplain, M.A.J., 1996. Avascular growth, angiogenesis and vascular growth in solid tumours: The mathematical modelling of the stages of tumour development. Math. Comp. Mod. 23, 47–87.

    Article  MATH  Google Scholar 

  • Chaplain, M.A.J., Ganesh, M., Graham, I.G., 2001. Spatio-temporal pattern formation on spherical surfaces: Numerical simulation and application to solid tumour growth. J. Math. Biol. 42, 387–423.

    Article  PubMed  MATH  MathSciNet  Google Scholar 

  • Crampin, E.J., Gaffney, E.A., Maini, P.K., 1999. Reaction and diffusion on growing domains: Scenarios for robust pattern formation. Bull. Math. Biol. 61, 1093–1120.

    Article  Google Scholar 

  • Crampin, E.J., Hackborn, W.W., Maini, P.K., 2002. Pattern formation in reaction-diffusion models with nonuniform domain growth. Bull. Math. Biol. 64, 747–769.

    Article  PubMed  Google Scholar 

  • Crank, J., 1984. Free and Moving Boundary Problems. Clarendon Press (Oxford University Press), Oxford.

    MATH  Google Scholar 

  • Fiedler, B., Liebscher, S., Alexander, J.C., 2000. Generic Hopf bifurcation from lines of equilibria without parameters: I. Theory. J. Diff. Equat. 167, 16–35.

    Article  MATH  MathSciNet  Google Scholar 

  • Fodde, R., 2001. Apc, signal transduction and genetic instability in colorectal cancer. Nat. Rev. Cancer 1, 55–67.

    Article  PubMed  Google Scholar 

  • Franks, S.J., King, J.R., 2003. Interactions between a uniformly proliferating tumour and its surroundings: uniform material properties. Math. Med. Biol. 20, 47–89.

    Article  PubMed  MATH  Google Scholar 

  • Gierer, A., Meinhardt, H., 1972. A theory of biological pattern formation. Kybernetik 12, 30–39.

    Article  PubMed  Google Scholar 

  • Gray, P., Scott, S.K., 1983. Autocatalytic reactions in the isothermal, continuous stirred tank reactor. Chem. Eng. Sci. 38, 29–43.

    Article  Google Scholar 

  • Greenspan, H.P., 1976. On the growth and stability of cell cultures and solid tumours. J. Theor. Biol. 56, 229–242.

    Article  PubMed  MathSciNet  Google Scholar 

  • Grindrod, P., 1996. The Theory and Applications of Reaction-Diffusion Equations—Patterns and Waves of Oxford Applied Mathematics and Computing Science Series. Clarendon Press (Oxford University Press), Oxford.

    Google Scholar 

  • Harrison, L.G., Kolá, M., 1988. Coupling between reaction-diffusion prepattern and expressed morphogenesis, applied to desmids and dasyclads. J. Theor. Biol. 130, 493–515.

    Article  Google Scholar 

  • Jackson, T.L., 2002. Vascular tumor growth and treatment: Consequences of polyclonality, competition and dynamic vascular support. J. Math. Biol. 44, 201–226.

    Article  PubMed  MATH  MathSciNet  Google Scholar 

  • Jones, A.F., Byrne, H.M., Gibson, J.S., Dold, J.W., 2000. A mathematical model of the stress induced during avascular tumour growth. J. Math. Biol. 40, 473–499.

    Article  PubMed  MATH  MathSciNet  Google Scholar 

  • Kondo, S., Asai, R., 1995. A reaction-diffusion wave on the skin of the marine angelfish Pomacanthus. Nature 376, 765–768.

    Article  Google Scholar 

  • Kuhnert, F., Davis, C.R., Wang, H.T., Chu, P., Lee, M., Yuan, J., Nusse, R., Kuo, C.J., 2004. Essential requirements for Wnt signalling in proliferation of adult small intestine and colon revealed by adenoviral expression of Dickkopf-1. Proc. Natl. Acad. Sci. USA 101, 266–271.

    Article  PubMed  Google Scholar 

  • Lengyel, I., Epstein, I.R., 1991. Modelling of Turing structures in the chlorite iodide malonic acid starch reaction system. Science 251, 650–652.

    Article  Google Scholar 

  • Maini, P.K., Painter, K.J., Nguyen Phong Chau, H., 1997. Spatial pattern formation in chemical and biological systems. J. Chem. Soc. Faraday Trans. 93, 3601–3610.

    Article  Google Scholar 

  • Majack, R.A., 1987. Beta-type transforming growth factor specifies organizational behaviour in vascular smooth muscle cell cultures. J. Cell Biol. 105, 465–471.

    Article  PubMed  Google Scholar 

  • Matthews, P.C., 1998. Hexagonal patterns in finite domains. Physica D 116, 81–94.

    Article  MathSciNet  MATH  Google Scholar 

  • Murray, A., Hunt, T., 1993. The Cell Cycle. Oxford University Press, Oxford, New York, Toronto and Delhi.

    Google Scholar 

  • Murray, J.D., 1981. A pre-pattern formation mechanism for animal coat markings. J. Theor. Biol. 88, 161–199.

    Article  Google Scholar 

  • Murray, J.D., 1993. Mathematical Biology, of Biomathematics Texts, vol. 19, 2nd edition. Springer-Verlag, Berlin and London.

    Google Scholar 

  • Neubert, M.G., Caswell, H., Murray, J.D., 2002. Transient dynamics and pattern formation: reactivity is necessary for Turing instabilities. Math. Biosci. 175, 1–11.

    Article  PubMed  MATH  MathSciNet  Google Scholar 

  • Neville, A.A., 2003. Biomedical Modelling Incorporating Growth, PhD thesis, University of Nottingham, Nottingham, England.

  • Ouyang, Q., Swinney, H.L., 1991. Transition from a uniform state to hexagonal and striped Turing patterns. Nat. (Lond.) 352, 610–612.

    Article  Google Scholar 

  • Owen, M.R., Sherratt, J.A., 1999. Mathematical modelling of macrophage dynamics in tumours. Math. Mod. Meth. Appl. Sci. 9, 513–539.

    Article  MATH  Google Scholar 

  • Painter, K.J., Maini, P.K., Othmer, H.G., 1999. Stripe formation in juvenile Pomacanthus explained by a generalised Turing mechanism with chemotaxis. Proc. Natl. Acad. Sci. USA 96, 5549–5554.

    Article  PubMed  Google Scholar 

  • Painter, K.J., Maini, P.K., Othmer, H.G., 2000. Development and applications of a model for cellular response to multiple chemotactic cues. J. Math. Biol. 41, 285–314.

    Article  PubMed  MATH  MathSciNet  Google Scholar 

  • Pettet, G.J., Please, C.P., Tindall, M.J., McElwain, D.L.S., 2001. The migration of cells in multicell tumor spheroids. Bull. Math. Biol. 63, 231–257.

    Article  PubMed  Google Scholar 

  • Pinto, D., Gregorioff, A., Beghtel, H., Clevers, H., 2003. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes Dev. 17, 1709–1713.

    Article  PubMed  Google Scholar 

  • Santini, M.T., Rainaldi, G., Indovina, P.L., 2000. Apoptosis, cell adhesion and the extracellular matrix in the three-dimensional growth of multicellular tumor spheroids. Crit. Rev. Oncol. Hemat. 36, 75–87.

    Article  Google Scholar 

  • Schnakenberg, J., 1979. Simple chemical reaction systems with limit cycle behaviour. J. Theor. Biol. 81, 389–400.

    Article  PubMed  MathSciNet  Google Scholar 

  • Sherratt, J.A., Chaplain, M.A.J., 2001. A new mathematical model for avascular tumour growth. J. Math. Biol. 43, 291–312.

    Article  PubMed  MATH  MathSciNet  Google Scholar 

  • Turing, A.M., 1952. The chemical basis of morphogenesis. Phil. Trans. Roy. Soc. Lond. B237, 37–72.

    Article  Google Scholar 

  • Varea, C., Aragon, J.L., Barrio, R.A., 1997. Confined Turing patterns in growing systems. Phys. Rev. E 56, 1250–1253.

    Article  Google Scholar 

  • Ward, J.P., King, J.R., 1997. Mathematical modelling of avascular-tumour growth. IMA J. Math. Appl. Med. Biol. 14, 39–69.

    Article  PubMed  MATH  Google Scholar 

  • Ward, J.P., King, J.R., 1999. Mathematical modelling of avascular-tumour growth II: Modelling growth saturation. IMA J. Math. Appl. Med. Biol. 16, 171–211.

    Article  PubMed  MATH  Google Scholar 

  • Wein, L.M., Wu, J.T., Kirn, D.H., 2003. Validation and analysis of a mathematical model of a replication and competent oncolytic virus for cancer treatment: implications for virus design and delivery. Cancer Res. 63, 1317–1324.

    PubMed  Google Scholar 

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Correspondence to H. M. Byrne.

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Neville, A.A., Matthews, P.C. & Byrne, H.M. Interactions Between Pattern Formation and Domain Growth. Bull. Math. Biol. 68, 1975–2003 (2006). https://doi.org/10.1007/s11538-006-9060-5

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  • DOI: https://doi.org/10.1007/s11538-006-9060-5

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