The importance of structured noise in the generation of self-organizing tissue patterns through contact-mediated cell-cell signalling

Journal of the Royal Society Interface

Volumn 8, Issue 59, 2011, Pages 787-798

  Cohen, Michael ^a   Baum, Buzz ^a   Miodownik, Mark ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Cellular automata; Filopodia; Lateral inhibition; Noise; Patterning; Signalling

Indexed keywords

CELLULAR AUTOMATA; PATTERN RECOGNITION SYSTEMS; PROTEINS; TISSUE;

FILOPODIA; LATERAL INHIBITION; NOISE; PATTERNING; SIGNALLING;

CELLS;

ANIMAL CELL; ARTICLE; CELL COMMUNICATION; DROSOPHILA MELANOGASTER; DYNAMICS; LATERAL INHIBITION; MODEL; MORPHOGENESIS; NOISE; NONHUMAN; SIGNAL DETECTION; SIGNAL NOISE RATIO; SIGNAL TRANSDUCTION;

DROSOPHILA MELANOGASTER; MICROCHAETE;

EID: 79955740063     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2010.0488     Document Type: Article

References (50)

1. Classen, A. K., Anderson, K. I., Marois, E. & Eaton, S. 2005 Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. Dev. Cell 9, 805-817. (doi:10.1016/j.devcel.2005.10.016)
2. Cohen, M., Georgiou, M., Stevenson, N. L., Miodownik, M. & Baum, B. 2010 Dynamic filopodia drive pattern refinement via intermittent N-Dl signalling. Dev. Cell 19, 78-89. (doi:10.1016/j.devcel.2010.06.006)
3. Maini, P. K., Baker, R. E. & Chuong, C.-M. 2006 Developmental biology. The Turing model comes of molecular age. Science 314, 1397-1398. (doi:10.1126/science.1136396)
4. Webb, S. D. & Owen, M. R. 2004 Oscillations and patterns in spatially discrete models for developmental ligand-receptor interactions. J. Math. Biol. 48, 444-476. (doi:10.1007/s00285-003-0247-1)
5. Amoyel, M., Cheng, Y. C., Jiang, Y.-J. & Wilkinson, D. G. 2005 Wnt1 regulates neurogenesis and mediates lateral inhibition of boundary cell specification in the zebrafish hindbrain. Development 132, 775-785. (doi:10.1242/dev.01616)
6. Baker, N. E., Yu, S. & Han, D. 1996 Evolution of proneural atonal expression during distinct regulatory phases in the developing Drosophila eye. Curr. Biol. 6, 1290-1301. (doi:10.1016/S0960-9822(02)70715-X)
7. Bender, L. B., Kooh, P. J. & Muskavitch, M. A. T. 1993 Complex function and expression of Delta during Drosophila oogenesis. Genetics 133, 967-978. (Pubitemid 23097281)
8. Cobellis, L., Caprio, F., Trabucco, E., Mastrogiacomo, A., Coppola, G., Manente, L., Colacurci, N., De Falco, M. & De Luca, A. 2008 The pattern of expression of Notch protein members in normal and pathological endometrium. J. Anat. 213, 464-472. (doi:10.1111/j.1469-7580.2008.00963.x)
9. Gerhardt, H. et al. 2003 VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell. Biol. 161, 1163-1177. (doi:10.1083/jcb.200302047)
10. High, F. A. & Epstein, J. A. 2008 The multifaceted role of Notch in cardiac development and disease. Nat. Rev. Genet. 9, 49-61. (doi:10.1038/ nrg2279)
11. Lewis, A. K., Frantz, G. D., Carpenter, D. A., de Sauvage, F. J. & Gao, W. Q. 1998 Distinct expression patterns of notch family receptors and ligands during development of the mammalian inner ear. Mech. Dev. 78, 159-163. (doi:10.1016/S0925-4773(98)00165-8)
12. Lewis, J. 1998 Notch signalling and the control of cell fate choices in vertebrates. Semin. Cell. Dev. Biol. 9, 583-589. (doi:10.1006/scdb.1998.0266)
13. Ma, E. Y., Rubel, E. W. & Raible, D. W. 2008 Notch signaling regulates the extent of hair cell regeneration in the zebrafish lateral line. J. Neurosci. 28, 2261-2273. (doi:10.1523/JNEUROSCI.4372-07.2008)
14. Munteanu, A. & Sole, R. V. 2008 Neutrality and robustness in evo-devo: emergence of lateral inhibition. PLoS Comput. Biol. 4, e1000226. (doi:10.1371/journal.pcbi.1000226)
15. Murtaugh, L. C., Stanger, B. Z., Kwan, K. M. & Melton, D. A. 2003 Notch signaling controls multiple steps of pancreatic differentiation. Proc. Natl Acad. Sci. USA 100, 14 920-14 925. (doi:10.1073/pnas.2436557100)
16. Noramly, S. & Morgan, B. A. 1998 BMPs mediate lateral inhibition at successive stages in feather tract development. Development 125, 3775-3787. (Pubitemid 28488353)
17. Reed, R. D. 2004 Evidence for Notch-mediated lateral inhibition in organizing butterfly wing scales. Dev. Genes Evol. 214, 43-46. (doi:10.1007/s00427-003-0366-0)
18. Schellmann, S., Schnittger, A., Kirik, V., Wada, T., Okada, K., Beermann, A., Thumfahrt, J., Jürgens, G. & Hülskamp, M. 2002 TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J. 21, 5036-5046. (doi:10.1093/emboj/cdf524)
19. Wang, M. & Sternberg, P. W. 2001 Pattern formation during C. elegans vulval induction. Curr. Top. Dev. Biol. 51, 189-220. (doi:10.1016/S0070-2153(01) 51006-6)
20. Bray, S. J. 2006 Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell. Biol. 7, 678-689. (doi:10.1038/nrm2009)
21. Collier, J. R., Monk, N. A., Maini, P. K. & Lewis, J. H. 1996 Pattern formation by lateral inhibition with feedback: a mathematical model of delta-notch intercellular signalling. J. Theor. Biol. 183, 429-446. (doi:10.1006/jtbi.1996.0233)
22. Artavanis-Tsakonas, S., Rand, M. D. & Lake, R. J. 1999 Notch signaling: cell fate control and signal integration in development. Science 284, 770-776. (doi:10.1126/science.284.5415.770)
23. Simpson, P., Woehl, R. & Usui, K. 1999 The development and evolution of bristle patterns in Diptera. Development 126, 1349-1364. (Pubitemid 29195225)
24. Usui, K. & Kimura, K. 1993 Sequential emergence of the evenly spaced microchaetes on the notum of Drosophila. Dev. Biol. 203, 151-158.
25. Wigglesworth, V. B. 1940 Local and general factors in the development of 'pattern' in Rhodnius prolixus. J. Exp. Biol. 17, 180-200.
26. Heitzler, P. & Simpson, P. 1991 The choice of cell fate in the epidermis of Drosophila. Cell 64, 1083-1092. (doi:10.1016/0092-8674(91)90263-X)
27. Ahimou, F., Mok, L. & Bardot, B. 2004 The adhesion force of Notch with Delta and the rate of Notch signaling. J. Cell Biol. 167, 1217-1229. (doi:10.1083/jcb.200407100)
28. Sun, X. & Artavanis-Tsakonas, S. 1997 Secreted forms of DELTA and SERRATE define antagonists of Notch signaling in Drosophila. Development 124, 3439-3448. (Pubitemid 27440458)
29. Ghosh, R. & Tomlin, C. 2001 Lateral inhibition through Delta-Notch signaling: a piecewise affine hybrid model. LNCS 2034, 232-246. (Pubitemid 33256421)
30. Hwang, I., Balakrishnan, H., Ghosh, R. & Tomlin, C. J. 2002 Reachability analysis of Delta-Notch lateral inhibition using predicate abstraction. In Proc. Int. Conf. High Performance Computing, Bangalore, India, 18-21 December 2002, Berlin, Germany: Springer-Verlag.
31. Marnellos, G., Deblandre, G., Mjolsness, E. & Kintner, C. 2000 Delta-Notch lateral inhibitory patterning in the emergence of ciliated cells in Xenopus: experimental observations and a gene network model. Pac. Symp. Biocomput. 5, 329-340.
32. Podgorski, G. J., Bansal, M. & Flann, N. S. 2007 Regular mosaic pattern development: a study of the interplay between lateral inhibition, apoptosis and differential adhesion. Theor. Biol. Med. Model 4, 43. (doi:10.1186/1742-4682-4-43)
33. Matsumoto, K. & Tsuda, I. 1983 Noise-induced order. J. Stat. Phys. 31, 87-106. (doi:10.1007/BF01010923)
34. Pikovsky, A. S. 1992 Discrete model of spatially mixing system. Phys. Lett. A 168, 276-279. (doi:10.1016/0375-9601(92)91131-A)
35. McDonnell, M. D. & Abbott, D. 2009 What is stochastic resonance? Definitions, misconceptions, debates, and its relevance to biology. Plos Comput. Biol. 5, e1000348. (doi:10.1371/journal.pcbi.1000348)
36. Moss, F., Pierson, D. & Gorman, D. Ó. 1994 Stochastic resonance: tutorial and update. Int. J. Bifurcation Chaos 4, 1383-1397. (doi:10.1142/S0218127494001118)
37. Hecht, I., Kessler, D. A. & Levine, H. 2010 Transient localized patterns in noise-driven reaction-diffusion systems. Phys. Rev. Lett. 104, 158301. (doi:10.1103/PhysRevLett.104.158301)
38. Singh, A. & Weinberger, L. S. 2009 Stochastic gene expression as a molecular switch for viral latency. Curr. Opin. Microbiol. 12, 460-466. (doi:10.1016/j.mib.2009.06.016)
39. Suel, G. M., Kulkarni, R. P., Dworkin, J., Garcia-Ojalvo, J. & Elowitz, M. B. 2007 Tunability and noise dependence in differentiation dynamics. Science 315, 1716-1719. (doi:10.1126/science.1137455)
40. Murray, J. D. 1993 Mathematical biology. Berlin, Germany: Springer.
41. Aulehla, A. & Pourquie, O. 2008 Oscillating signaling pathways during embryonic development. Curr. Opin. Cell. Biol. 20, 632-637. (doi:10.1016/j.ceb.2008.09.002)
42. Kageyama, R., Niwa, Y. & Shimoja, H. 2009 Rhythmic gene expression in somite formation and neural development. Mol. Cells 27, 497-502. (doi:10.1007/s10059-009-0068-1)
43. Shimojo, H., Ohtsuka, T. & Kageyama, R. 2008 Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58, 52-64. (doi:10.1016/j.neuron.2008.02.014)
44. Levine, H. & Rappel, W. J. 2005 Membrane-bound Turing patterns. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 72, 061 912.
45. Plahte, E. 2001 Pattern formation in discrete cell lattices. J. Math. Biol. 43, 411-445. (doi:10.1007/s002850100105)
46. Kondo, S. & Asai, R. 1995 A reaction-diffusion wave on the skin of the marine angelfish pomacanthus. Nature 376, 765-768. (doi:10.1038/376765a0)
47. Kondo, S., Iwashita, M. & Yamaguchi, M. 2009 How animals get their skin patterns: fish pigment pattern as a live Turing wave. Int. J. Dev. Biol. 53, 851-856. (doi:10.1387/ijdb.072502sk)
48. Miodownik, M. A. 2001 Grain growth, uniform. In Encyclopedia of materials: science and technology, vol. 4, pp. 3636-3541. Amsterdam, The Netherlands: Elsevier.
49. Miodownik, M. A. 2009 Monte Carlo models for grain growth and recrystallisation. In ASM handbook series, modelling and simulation: processing of metalilic materials, vol. 22A, article 3J. Materials Park, OH: ASM International.
50. Miodownik, M. A., Smereka, P., Srolovitz, D. J. & Holm, E. A. 2001 Scaling of dislocation cell structures: diffusion in orientation space. Proc. R. Soc. Lond. A 457, 1807-1819. (doi:10.1098/rspa.2001.0794)