Advertisement

Addressing Interdisciplinary Difficulties in Developmental Biology/Mathematical Collaborations: A Neural Crest Example

  • Donald F. NewgreenEmail author
  • Kerry A. Landman
  • James M. Osborne
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1976)

Abstract

Mathematical modeling can allow insight into the biological processes that can be difficult to access by conventional biological means alone. Such projects are becoming increasingly attractive with the appearance of faster and more powerful quantitative techniques in both biological data acquisition and data storage, manipulation, and presentation. However, as is frequent in interdisciplinary research, the main hurdles are not within the mindset and techniques of each discipline but are usually encountered in attempting to meld the different disciplines together. Based upon our experience in applying mathematical methods to investigate how neural crest cells interact to form the enteric nervous system, we present our views on how to pursue biomathematical modeling projects, what difficulties to expect, and how to overcome, or at least survive, these hurdles. The main advice being: persevere.

Key words

Mathematical model Computational model Systems biology Collaboration Morphogenesis 

References

  1. 1.
    Thompson DW (1917) On growth and form, vol xiv, 1st edn. Cambridge University Press, London and Edinburgh, p 793Google Scholar
  2. 2.
    Longo DL, Drazen JM (2016) Data Sharing. N Engl J Med 374(3):276–277PubMedGoogle Scholar
  3. 3.
    Landman KA (2016) An interaction with biologists: insights into development and disease. In: Anderssen RS et al (eds) Applications + practical conceptualization + mathematics = fruitful innovation: proceedings of the forum of mathematics for industry 2014. Springer Japan, Tokyo, pp 51–60Google Scholar
  4. 4.
    Newgreen DF et al (2013) Simple rules for a "simple" nervous system? Molecular and biomathematical approaches to enteric nervous system formation and malformation. Dev Biol 382(1):305–319PubMedPubMedCentralGoogle Scholar
  5. 5.
    Landman KA, Simpson MJ, Newgreen DF (2007) Mathematical and experimental insights into the development of the enteric nervous system and Hirschsprung's disease. Develop Growth Differ 49(4):277–286Google Scholar
  6. 6.
    Landman KA, Binder BJ, Newgreen DF (2012) In: Bandini GCSaS (ed) Modeling development and disease in our “Second” brain. ACRI 2012, LNCS 7495 ed. 10th International Conference on Cellular Automata for Research and Industry. Springer-Verlag, Berlin HeidelbergGoogle Scholar
  7. 7.
    Landman KA, Binder B, Newgreen DF (2014) Modeling development and disease in the enteric nervous system. J Cellular Automata 9:95–109Google Scholar
  8. 8.
    Ouzounis CA (2012) Rise and demise of bioinformatics? Promise and progress. PLoS Comput Biol 8(4):e1002487PubMedPubMedCentralGoogle Scholar
  9. 9.
    Luscombe NM, Greenbaum D, Gerstein M (2001) What is bioinformatics? A proposed definition and overview of the field. Methods Inf Med 40(4):346–358PubMedGoogle Scholar
  10. 10.
    Whitacre JM (2012) Biological robustness: paradigms, mechanisms, and systems principles. Front Genet 3:67PubMedPubMedCentralGoogle Scholar
  11. 11.
    Mayer J, Khairy K, Howard J (2010) Drawing an elephant with four complex parameters. Am J Phys 78:648–649Google Scholar
  12. 12.
    Fanelli D (2009) How many scientists fabricate and falsify research? A systematic review and meta-analysis of survey data. PLoS One 4(5):e5738PubMedPubMedCentralGoogle Scholar
  13. 13.
    Vanden Berghe P (2016) Advanced 3D optical microscopy in ENS research. Adv Exp Med Biol 891:193–199Google Scholar
  14. 14.
    Bissell MJ (2017) Goodbye flat biology—time for the 3rd and the 4th dimensions. J Cell Sci 130(1):3–5PubMedGoogle Scholar
  15. 15.
    Newgreen D, Young HM (2002) Enteric nervous system: development and developmental disturbances-part 1. Pediatr Dev Pathol 5(3):224–247PubMedGoogle Scholar
  16. 16.
    Newgreen D, Young HM (2002) Enteric nervous system: development and developmental disturbances-part 2. Pediatr Dev Pathol 5:329–349PubMedGoogle Scholar
  17. 17.
    Simpson MJ et al (2007) Cell proliferation drives neural crest cell invasion of the intestine. Dev Biol 302(2):553–568PubMedGoogle Scholar
  18. 18.
    Hackett-Jones EJ et al (2011) On the role of differential adhesion in gangliogenesis in the enteric nervous system. J Theor Biol 287:148–159PubMedGoogle Scholar
  19. 19.
    Newgreen DF et al (1996) Migration of enteric neural crest cells in relation to growth of the gut in avian embryos. Acta Anat (Basel) 157(2):105–115Google Scholar
  20. 20.
    Chaturvedi R et al (2005) On multiscale approaches to three-dimensional modelling of morphogenesis. J R Soc Interface 2(3):237–253PubMedPubMedCentralGoogle Scholar
  21. 21.
    Izaguirre JA et al (2004) CompuCell, a multi-model framework for simulation of morphogenesis. Bioinformatics 20(7):1129–1137PubMedGoogle Scholar
  22. 22.
    Osborne JM et al (2017) Comparing individual-based approaches to modelling the self-organization of multicellular tissues. PLoS Comput Biol 13(2):e1005387PubMedPubMedCentralGoogle Scholar
  23. 23.
    Simpson MJ et al (2007) Simulating invasion with cellular automata: connecting cell-scale and population-scale properties. Phys Rev E Stat Nonlinear Soft Matter Phys 76(2 Pt 1):021918Google Scholar
  24. 24.
    Cheeseman BL et al (2014) Cell lineage tracing in the developing enteric nervous system: superstars revealed by experiment and simulation. J R Soc Interface 11(93):20130815PubMedPubMedCentralGoogle Scholar
  25. 25.
    Cheeseman BL, Newgreen DF, Landman KA (2014) Spatial and temporal dynamics of cell generations within an invasion wave: a link to cell lineage tracing. J Theor Biol 363:344–356PubMedGoogle Scholar
  26. 26.
    Binder BJ et al (2008) Modeling proliferative tissue growth: a general approach and an avian case study. Phys Rev E Stat Nonlinear Soft Matter Phys 78(3 Pt 1):031912Google Scholar
  27. 27.
    Simpson MJ, Landman KA, Newgreen DF (2006) Chemotactic and diffusive migration on a non-uniformly growing domain: numerical algorithm development and applications. J Computat and App Math 192:282–300Google Scholar
  28. 28.
    Wang X et al (2011) Analysis of the sacral neural crest cell contribution to the hindgut enteric nervous system in the mouse embryo. Gastroenterology 141(3):992–1002. e1-6PubMedGoogle Scholar
  29. 29.
    Nagy N et al (2007) Pelvic plexus contributes ganglion cells to the hindgut enteric nervous system. Dev Dyn 236(1):73–83PubMedGoogle Scholar
  30. 30.
    Uesaka T, Nagashimada M, Enomoto H (2015) Neuronal differentiation in Schwann cell lineage underlies postnatal neurogenesis in the enteric nervous system. J Neurosci 35(27):9879–9888PubMedGoogle Scholar
  31. 31.
    Landman KA et al (2011) Building stable chains with motile agents: insights into the morphology of enteric neural crest cell migration. J Theor Biol 276(1):250–268PubMedGoogle Scholar
  32. 32.
    Young HM et al (2014) Colonizing while migrating: how do individual enteric neural crest cells behave? BMC Biol 12(1):23PubMedPubMedCentralGoogle Scholar
  33. 33.
    Allan IJ, Newgreen DF (1980) The origin and differentiation of enteric neurons of the intestine of the fowl embryo. Am J Anat 157(2):137–154PubMedGoogle Scholar
  34. 34.
    Young HM et al (1998) A single rostrocaudal colonization of the rodent intestine by enteric neuron precursors is revealed by the expression of Phox2b, Ret, and p75 and by explants grown under the kidney capsule or in organ culture. Dev Biol 202(1):67–84PubMedGoogle Scholar
  35. 35.
    Young HM et al (2004) Dynamics of neural crest-derived cell migration in the embryonic mouse gut. Dev Biol 270(2):455–473PubMedGoogle Scholar
  36. 36.
    Stramer BM et al (2013) Rediscovering contact inhibition in the embryo. J Microsc 251(3):206–211PubMedGoogle Scholar
  37. 37.
    Young HM et al (2001) GDNF is a chemoattractant for enteric neural cells. Dev Biol 229(2):503–516PubMedGoogle Scholar
  38. 38.
    Simpson MJ et al (2006) Looking inside an invasion wave of cells using continuum models: proliferation is the key. J Theor Biol 243(3):343–360PubMedGoogle Scholar
  39. 39.
    Nishiyama C et al (2012) Trans-mesenteric neural crest cells are the principal source of the colonic enteric nervous system. Nat Neurosci 15(9):1211–1218PubMedGoogle Scholar
  40. 40.
    Harrison C, Wabbersen T, Shepherd IT (2014) In vivo visualization of the development of the enteric nervous system using a Tg(−8.3bphox2b:Kaede) transgenic zebrafish. Genesis 52(12):985–990PubMedPubMedCentralGoogle Scholar
  41. 41.
    Kulesa PM et al (2008) Neural crest invasion is a spatially-ordered progression into the head with higher cell proliferation at the migratory front as revealed by the photoactivatable protein, KikGR. Dev Biol 316(2):275–287PubMedPubMedCentralGoogle Scholar
  42. 42.
    Binder BJ et al (2012) Spatial analysis of multi-species exclusion processes: application to neural crest cell migration in the embryonic gut. Bull Math Biol 74(2):474–490PubMedGoogle Scholar
  43. 43.
    Barlow AJ et al (2008) Critical numbers of neural crest cells are required in the pathways from the neural tube to the foregut to ensure complete enteric nervous system formation. Development 135(9):1681–1691PubMedGoogle Scholar
  44. 44.
    Newgreen DF et al (2017) Differential clonal expansion in an invading cell population: clonal advantage or dumb luck? Cells Tissues Organs 203(2):105–113PubMedGoogle Scholar
  45. 45.
    Jung PM (1995) Hirschsprung's disease: one surgeon's experience in one institution. J Pediatr Surg 30(5):646–651PubMedGoogle Scholar
  46. 46.
    Binder BJ et al (2015) Incomplete penetrance: the role of stochasticity in developmental cell colonization. J Theor Biol 380:309–314PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Donald F. Newgreen
    • 1
    Email author
  • Kerry A. Landman
    • 2
  • James M. Osborne
    • 2
  1. 1.Murdoch Children’s Research InstituteRoyal Children’s HospitalParkvilleAustralia
  2. 2.School of Mathematics and StatisticsUniversity of MelbourneParkvilleAustralia

Personalised recommendations