Advertisement

PCA Modelling of Multi-species Cell Clusters: Ganglion Development in the Gastrointestinal Nervous System

  • Kerry A. LandmanEmail author
  • Donald F. Newgreen
Chapter
Part of the Emergence, Complexity and Computation book series (ECC, volume 27)

Abstract

A defining characteristic of the enteric nervous system (ENS) is mesoscale patterned entities called ganglia. Ganglia are clusters of neurons with associated enteric neural crest (ENC) cells, which form in the simultaneously growing gut wall. At first, the precursor ENC cells proliferate and gradually differentiate to produce the enteric neurons; these neurons form clusters with ENC scattered around and later lying on the periphery of neuronal clusters. By immunolabelling neural cell–cell adhesion molecules, the adhesive capacity of neurons is determined to be greater than that of ENC cells. Using a probabilistic cellular automata (PCA) model, we test the hypothesis that local rules governing differential adhesion of neuronal agents and ENC agents will produce clusters that emulate ganglia. The clusters are relatively stable, relatively uniform and small in size, of fairly uniform spacing, with a balance between the number of neuronal and ENC agents. These features are attained in both fixed and growing domains, reproducing, respectively, organotypic in vitro and in vivo observations. Various threshold criteria governing ENC agent proliferation and differentiation and neuronal agent inhibition of differentiation are important for sustaining these characteristics. This investigation suggests possible explanations for observations in normal and abnormal ENS development.

Keywords

Aggregation and clusters Differential adhesion 

Notes

Acknowledgements

This work was supported by Australian Research Council and National Health and Medical Research Council grants. Thanks are given to Emily Hackett-Jones and Dongcheng Zhang. MCRI facilities are supported by the Victorian Government’s Operational Infrastructure Support Program.

References

  1. 1.
    Binder, B.J., Landman, K.A.: Exclusion processes on a growing domain. J. Theor. Biol. 259, 541–551 (2009)MathSciNetCrossRefGoogle Scholar
  2. 2.
    Binder, B.J., Landman, K.A., Simpson, M.J., Mariani, M., Newgreen, D.F.: Modeling proliferative tissue growth: a general approach and an avian case study. Phys. Rev. E 78, 031912 (2008)CrossRefGoogle Scholar
  3. 3.
    Breau, M.A., Pietri, T., Eder, O., Blanche, M., Brakebusch, C., Fassler, R., Thiery, J.P., Dufour, S.: Lack of \(\beta \)1 integrins in enteric neural crest cells leads to a Hirschsprung-like phenotype. Development 33, 1725–1734 (2006)CrossRefGoogle Scholar
  4. 4.
    Chalazonitis, A., Gershon, M.D., Green, L.A.: Cell death and the developing enteric nervous system. Neurochem. Int. 61, 839–847 (2012)CrossRefGoogle Scholar
  5. 5.
    Daub, J.T., Merks, R.M.H.: A cell-based model of extracellular-matrix-guided endothelial cell migration during angiogenesis. Bull. Math. Biol. 75, 1377–1399 (2013)MathSciNetCrossRefzbMATHGoogle Scholar
  6. 6.
    Foty, R.A., Steinberg, M.S.: Cadherin-mediated cell-cell adhesion and tissue segregation in relation to malignancy. Int. J. Dev. Biol. 48, 397–409 (2004)CrossRefGoogle Scholar
  7. 7.
    Foty, R.A., Steinberg, M.S.: The differential adhesion hypothesis: a direct evaluation. Dev. Biol. 278, 255–263 (2005)CrossRefGoogle Scholar
  8. 8.
    Glazier, J.A., Graner, F.: Simulation of the differential adhesion driven rearrangement of biological cells. Phys. Rev. E 47, 2128–2154 (1993)CrossRefGoogle Scholar
  9. 9.
    Graner, F., Glazier, J.A.: Simulation of biological cell sorting using a two-dimensional extended Potts model. Phys. Rev. Lett. 69, 2013–2016 (1992)CrossRefGoogle Scholar
  10. 10.
    Hackett-Jones, E.J., Landman, K.A., Newgreen, D.F., Zhang, D.: On the role of differential adhesion in gangliogenesis in the enteric nervous system. J. Theor. Biol. 287, 148–159 (2011)CrossRefGoogle Scholar
  11. 11.
    Hao, M.M., Anderson, R.B., Kobayashi, K., Whitington, P.M., Young, H.M.: The migratory behaviour of immature enteric neurons. Dev. Neurobiol. 69, 22–35 (2009)Google Scholar
  12. 12.
    Hao, M.M., Anderson, R.B., Young, H.M.: Development of enteric neuron diversity. J. Cell. Mol. Med. 13, 1193–1210 (2009)CrossRefGoogle Scholar
  13. 13.
    Hearn, C.J., Young, H.M., Ciampoli, D., Lomax, A.E., Newgreen, D.F.: Catenary cultures of embryonic gastrointestinal tract support organ morphogenesis, motility, neural crest cell migration, and cell differentiation. Dev. Dyn. 214, 239–247 (1999)CrossRefGoogle Scholar
  14. 14.
    Hendershot, T.J., Liu, H., Sarkar, A.A., Giovannucci, D.R., Clouthier, D.E., Abe, M., Howard, M.J.: Expression of Hand2 is sufficient for neurogenesis and cell type-specific gene expression in the enteric nervous system. Dev. Dyn. 236, 93–105 (2007)CrossRefGoogle Scholar
  15. 15.
    Horton, J.D.: A polynomial-time algorithm to find a shortest cycle basis of a graph. SIAM J. Comput. 16, 359–366 (1987)MathSciNetCrossRefzbMATHGoogle Scholar
  16. 16.
    Hoshen, J., Kopelman, R.: Percolation and cluster distribution. I. Cluster multiple labeling technique and critical density algorithm. Phys. Rev. B 14, 3438–3445 (1976)CrossRefGoogle Scholar
  17. 17.
    Hotta, R., Anderson, R.B., Kobayashi, K., Newgreen, D.F., Young, H.M.: Effects of tissue age, presence of neurones and endothelin-3 on the ability of enteric neurone precursors to colonize recipient gut: implications for cell-based therapies. Neurogastroenterol. Motil. 22, 331–e86 (2010)CrossRefGoogle Scholar
  18. 18.
    Landman, K.A., Fernando, A.E., Zhang, D., Newgreen, D.F.: Building stable chains with motile agents: Insights into the morphology of enteric neural crest cell migration. J. Theor. Biol. 276, 250–268 (2011)CrossRefGoogle Scholar
  19. 19.
    Landman, K.A., Binder, B.J., Newgreen, D.F.: Modeling development and disease in our “second” brain. Lect. Notes Comput. Sci. 7495, 405 (2012)CrossRefGoogle Scholar
  20. 20.
    Longo, D., Peirce, S.M., Skalak, T.C., Davidson, L., Marsden, M., Dzamba, B., DeSimone, D.W.: Multicellular computer simulation of morphogenisis: blastocoel roof thinning and matrix assembly in Xenopus laevis. Dev. Biol. 271, 210–222 (2004)CrossRefGoogle Scholar
  21. 21.
    Mehlhorn, K., Michail, D.: Implementing minimum cycle basis algorithms. J. Exp. Algorithmics 11, 1–14 (2006)MathSciNetzbMATHGoogle Scholar
  22. 22.
    Meier-Ruge, W.A., Bruder, E., Kapur, R.P.: Intestinal neuronal dysplasia type B: one giant ganglion is not good enough. Pediatr. Dev. Pathol. 9, 444–452 (2006)CrossRefGoogle Scholar
  23. 23.
    Merks, R.M.H., Glazier, J.A.: A cell-centered approach to developmental biology. Physica A 352, 113–130 (2005)CrossRefGoogle Scholar
  24. 24.
    Newgreen, D.F., Southwell, B., Hartley, L., Allan, I.J.: Migration of enteric neural crest cells in relation to growth of the gut in avian embryos. Acta Anat. 157, 105–115 (1996)CrossRefGoogle Scholar
  25. 25.
    Newgreen, D., Young, H.M.: Enteric nervous system: development and developmental disturbances-part 1. Pediatr. Dev. Pathol. 5, 224–247 (2002)Google Scholar
  26. 26.
    Peirce, S.M., Van Gieson, E.J., Skalak, T.C.: Multicellular simulation predicts microvascular patterning and in silico tissue assembly. FASEB J. 18(6), 731–733 (2004). https://doi.org/10.1096/fj.03-0933fje
  27. 27.
    Savill, N.J., Sherratt, J.A.: Control of epidermal stem cell clusters by notch-mediated lateral induction. Dev. Biol. 258, 141–153 (2003)CrossRefGoogle Scholar
  28. 28.
    Simpson, M.J., Merrifield, A., Landman, K.A., Hughes, B.D.: Simulating invasion with cellular automata. Phys. Rev. E 76, 021918 (2007)CrossRefGoogle Scholar
  29. 29.
    Simpson, M.J., Zhang, D.C., Mariani, M., Landman, K.A., Newgreen, D.F.: Cell proliferation drives neural crest cell invasion of the intestine. Dev. Biol. 302, 553–568 (2007)CrossRefGoogle Scholar
  30. 30.
    Steinberg, M.S.: Mechanism of tissue reconstruction by dissociated cells.II. Time course of events. Science 137, 762–763 (1962)Google Scholar
  31. 31.
    Steinberg, M.S.: On the mechanism of tissue reconstruction by dissociated cells, III. Free energy relations and the reorganisation of fused, heteronomic tissue fragments. Proc. Natl. Acad. Sci. USA 48, 1769–1776 (1962)Google Scholar
  32. 32.
    Steinberg, M.S.: On the mechanism of tissue reconstruction by dissociated cells, I. population kinetics, differential adhesiveness, and the absence of directed migration. Proc. Natl. Acad. Sci. USA 48, 1577–1582 (1962)Google Scholar
  33. 33.
    Sulsky, D.: A model of cell sorting. J. Theor. Biol. 106, 275–301 (1984)CrossRefGoogle Scholar
  34. 34.
    Townes, P.L., Holtfreter, J.: Directed movements and selective adhesion of embryonic amphibian cells. J. Exp. Zool. 128, 53–120 (1955)CrossRefGoogle Scholar
  35. 35.
    Wedel, T., Roblick, U.J., Ott, V., Eggers, R., Schiedeck, T.H.K., Krammer, H.J., Bruch, H.P.: Oligoneuronal hypoganglionosis in patients with idiopathic slow-transit constipation. Dis. Colon Rectum 45, 54–62 (2002)CrossRefGoogle Scholar
  36. 36.
    Wilson, H.V.: On some phenomena of coalescence and regeneration in sponges. J. Exp. Zool. 5, 245–258 (1907)CrossRefGoogle Scholar
  37. 37.
    Yin, M., King, S.K., Hutson, J.M., Chow, C.W.: Multiple endocrine neoplasia type 2B diagnosed on suction rectal biopsy in infancy: a report of 2 cases. Pediatr. Dev. Pathol. 9, 56–60 (2006)CrossRefGoogle Scholar
  38. 38.
    Young, H.M., Bergner, A.J., Muller, T.: Acquisition of neuronal and glial markers by neural crest-derived cells in the mouse intestine. J. Comp. Neurol. 456, 1–11 (2003)CrossRefGoogle Scholar
  39. 39.
    Young, H.M., Bergner, A.J., Anderson, R.B., Enomoto, H., Milbrandt, J., Newgreen, D.F., Whitington, P.M.: Dynamics of neural crest-derived cell migration in the embryonic mouse gut. Dev. Biol. 270, 455–473 (2004)CrossRefGoogle Scholar
  40. 40.
    Young, H.M., Turner, K.N., Bergner, A.J.: The location and phenotype of proliferating neural-crest-derived cells in the developing mouse gut. Cell Tissue Res. 320, 1–9 (2005)CrossRefGoogle Scholar
  41. 41.
    Zhang, D., Brinas, I.M., Binder, B.J., Landman, K.A., Newgreen, D.F.: Neural crest regionalisation for enteric nervous system formation: implications for Hirschsprung’s Disease and stem cell therapy. Dev. Biol. 339, 280–294 (2010)CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  1. 1.School of Mathematics and Statistics, University of MelbourneParkvilleAustralia
  2. 2.Murdoch Children’s Research Institute, Royal Children’s HospitalParkvilleAustralia

Personalised recommendations