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Spiral Waves of the Chemo-Attractant cAMP Organise Multicellular Development in the Social Amoebae Dictyostelium discoideum

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Spirals and Vortices

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Abstract

Development of multicellular organisms requires precise spatial and temporal integration of key cellular behaviours such as cell division, cell differentiation and cell movement to form the complex tissues that make up the organism. These cell behaviours are controlled by highly dynamic cell-cell signalling while these cell behaviours in turn feedback on the cell-cell signalling to result in emergent behaviours at the tissue and organism level. Dictyostelium discoideum is a relatively simple eukaryotic organism that is a widely used to study these interactions between cell-cell signalling and cell behaviours both experimentally and theoretically. This chapter describes our current understanding of how excitable cell-cell signalling results in the formation and propagation of large scale spiral waves of a chemo-attractant. How these chemo-attractant waves control the aggregation of hundreds of thousands of cells into multicellular aggregates and how interactions between excitable cell-cell signalling and cell movement control the transformation of aggregates into mounds and migrating slugs, that then go on to form fruiting bodies.

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References

  1. R. Kessin, Dictyostelium (Cambridge University, Cambridge, 2001)

    Google Scholar 

  2. A.J. Ridley, M.A. Schwartz, K. Burridge, R.A. Firtel, M.H. Ginsberg, G. Borisy, J.T. Parsons, A.R. Horwitz, Cell migration: integrating signals from front to back. Science 302, 1704–1709 (2003)

    Article  ADS  Google Scholar 

  3. P.N. Devreotes, S. Bhattacharya, M. Edwards, P.A. Iglesias, T. Lampert, Y. Miao, Excitable signal transduction networks in directed cell migration. Annu. Rev. Cell Dev. Biol. 33, 103–125 (2017)

    Article  Google Scholar 

  4. A.T. Sasaki, C. Janetopoulos, S. Lee, P.G. Charest, K. Takeda, L.W. Sundheimer, R. Meili, P.N. Devreotes, R.A. Firtel, G protein-independent Ras/PI3K/F-actin circuit regulates basic cell motility. J. Cell Biol. 178, 185–191 (2007)

    Article  Google Scholar 

  5. G.S. Pitt, N. Milona, J. Borleis, K.C. Lin, R.R. Reed, P.N. Devreotes, Structurally distinct and stage-specific adenylyl cyclase genes play different roles in Dictyostelium development. Cell 69, 305–315 (1992)

    Google Scholar 

  6. S. Saran, M.E. Meima, E. Alvarez-Curto, K.E. Weening, D.E. Rozen, P. Schaap, cAMP signaling in Dictyostelium. Complexity of camp synthesis, degradation and detection. J. Muscle Res. Cell Motil. 23, 793–802 (2002)

    Google Scholar 

  7. A.J. Durston, Dictyostelium discoideum aggregation fields as excitable media. J. Theor. Biol. 42, 483–504 (1973)

    Google Scholar 

  8. G.L. Garcia, C.A. Parent, Signal relay during chemotaxis. J. Microsc. 231, 529–534 (2008)

    Article  MathSciNet  Google Scholar 

  9. J. Lauzeral, J. Halloy, A. Goldbeter, Desynchronization of cells on the developmental path triggers the formation of spiral waves of cAMP during Dictyostelium aggregation. Proc. Natl. Acad. Sci. USA 94, 9153–9158 (1997)

    Google Scholar 

  10. F.I. Comer, C.A. Parent, Phosphoinositide 3-kinase activity controls the chemoattractant-mediated activation and adaptation of adenylyl cyclase. Mol. Biol. Cell 17, 357–366 (2006)

    Article  Google Scholar 

  11. T. Gregor, K. Fujimoto, N. Masaki, S. Sawai, The onset of collective behavior in social amoebae. Science 328, 1021–1025 (2010)

    Article  ADS  Google Scholar 

  12. M. Skoge, H. Yue, M. Erickstad, A. Bae, H. Levine, A. Groisman, W.F. Loomis, W.J. Rappel, Cellular memory in eukaryotic chemotaxis. Proc. Natl. Acad. Sci. USA 111, 14448–14453 (2014)

    Article  ADS  Google Scholar 

  13. F. Alcantara, M. Monk, Signal propagation during aggregation in the slime mould Dictyostelium discoideum. J. Gen. Microbiol. 85, 321–334 (1974)

    Google Scholar 

  14. K.J. Tomchik, P.N. Devreotes, Adenosine 3’,5’-monophosphate waves in Dictyostelium discoideum: a demonstration by isotope dilution-fluorography technique. Science 212, 443–446 (1982)

    Google Scholar 

  15. H. Cai, M. Katoh-Kurasawa, T. Muramoto, B. Santhanam, Y. Long, L. Li, M. Ueda, P.A. Iglesias, G. Shaulsky, P.N. Devreotes, Nucleocytoplasmic shuttling of a GATA transcription factor functions as a development timer. Science 343, 1249531 (2014)

    Article  Google Scholar 

  16. A.J. Durston, Pacemaker activity during aggregation in Dictyostelium discoideum. Dev. Biol. 37, 225–235 (1974)

    Google Scholar 

  17. P. Foerster, S.C. Müller, B. Hess, Curvature and spiral geometry in aggregation patterns of Dictyostelium discoideum. Development 109, 11–16 (1990)

    Google Scholar 

  18. A. Theibert, P. Devreotes, Adenosine and its derivatives inhibit the cAMP signaling response in Dictyostelium discoideum. Dev. Biol. 106, 166–173 (1984)

    Google Scholar 

  19. F. Siegert, C. Weijer, Digital image processing of optical density wave propagation in Dictyostelium discoideum and analysis of the effects of caffeine and ammonia. J. Cell Sci. 93, 325–335 (1989)

    Google Scholar 

  20. H. Patel, K. Guo, C. Parent, J. Gross, P.N. Devreotes, C.J. Weijer, A temperature-sensitive adenylyl cyclase mutant of Dictyostelium. EMBO J. 19, 2247–2256 (2000)

    Google Scholar 

  21. S. Sawai, X.J. Guan, A. Kuspa, E.C. Cox, High-throughput analysis of spatio-temporal dynamics in Dictyostelium. Genome Biol. 8, R144 (2007)

    Google Scholar 

  22. C. Beta, D. Wyatt, W.J. Rappel, E. Bodenschatz, Flow photolysis for spatiotemporal stimulation of single cells. Anal. Chem. 79, 3940–3944 (2007)

    Article  Google Scholar 

  23. D. Dormann, J.Y. Kim, P.N. Devreotes, C.J. Weijer, cAMP receptor affinity controls wave dynamics, geometry and morphogenesis in Dictyostelium. J. Cell Sci. 114, 2513–2523 (2001)

    Google Scholar 

  24. P.W. Kriebel, V.A. Barr, C.A. Parent, Adenylyl cyclase localization regulates streaming during chemotaxis. Cell 112, 549–560 (2003)

    Article  Google Scholar 

  25. J. Rietdorf, F. Siegert, C.J. Weijer, Analysis of optical-density wave-propagation and cell-movement during mound formation in Dictyostelium discoideum. Dev. Biol. 177, 427–438 (1996)

    Google Scholar 

  26. J.C. Coates, A.J. Harwood, Cell-cell adhesion and signal transduction during Dictyostelium development. J. Cell Sci. 114, 4349–4358 (2001)

    Google Scholar 

  27. H. Levine, W. Reynolds, Streaming instability of aggregating slime mold amoebae. Phys. Rev. Lett. 66, 2400–2403 (1991)

    Article  ADS  Google Scholar 

  28. G. De Palo, D. Yi, R.G. Endres, A critical-like collective state leads to long-range cell communication in Dictyostelium discoideum aggregation. PLOS Biol. 15, e1002602 (2017)

    Google Scholar 

  29. F. Siegert, C.J. Weijer, Spiral and concentric waves organize multicellular Dictyostelium mounds. Curr. Biol. 5, 937–943 (1995)

    Google Scholar 

  30. G. Weeks, C.J. Weijer, The Dictyostelium cell cycle and its relationship to differentiation. FEMS Microbiol. Lett. 124, 123–130 (1994)

    Google Scholar 

  31. C.J. Weijer, Dictyostelium morphogenesis. Curr. Opin. Genet. Dev. 14, 392–398 (2004)

    Google Scholar 

  32. S. Matsukuma, A.J. Durston, Chemotactic cell sorting in Dictyostelium discoideum. J. Embryol. Exp. Morphol. 50, 243–251 (1979)

    Google Scholar 

  33. H. Patel, K.D. Guo, C. Parent, J. Gross, P.N. Devreotes, C.J. Weijer, A temperature-sensitive adenylyl cyclase mutant of Dictyostelium. EMBO J. 19, 2247–2256 (2000)

    Google Scholar 

  34. D. Dormann, C.J. Weijer, Propagating chemoattractant waves coordinate periodic cell movement in Dictyostelium slugs. Development 128, 4535–4543 (2001)

    Google Scholar 

  35. I. Verkerke-van Wijk, M. Fukuzawa, P.N. Devreotes, P. Schaap, Adenylyl cyclase A expression is tip-specific in Dictyostelium slugs and directs StatA nuclear translocation and CudA gene expression. Dev. Biol. 234, 151–160 (2001)

    Google Scholar 

  36. B. Vasiev, F. Siegert, C.J. Weijer, A hydrodynamic model for Dictyostelium discoideum mound formation. J. Theor. Biol. 184, 441 (1997)

    Google Scholar 

  37. B. Vasiev, C.J. Weijer, Modelling of Dictyostelium discoideum slug migration. J. Theor. Biol. 223, 347–359 (2003)

    Google Scholar 

  38. O. Steinbock, F. Siegert, S.C. Müller, C.J. Weijer, Three-dimensional waves of excitation during Dictyostelium morphogenesis. Proc. Natl. Acad. Sci. USA 90, 7332–7335 (1993)

    Google Scholar 

  39. F. Siegert, C.J. Weijer, Three-dimensional scroll waves organize Dictyostelium slugs. Proc. Natl. Acad. Sci. USA 89, 6433–6437 (1992)

    Google Scholar 

  40. B. Wang, A. Kuspa, Dictyostelium development in the absence of cAMP. Science 277, 251–254 (1997)

    Google Scholar 

  41. T. Umeda, K. Inouye, Possible role of contact following in the generation of coherent motion of Dictyostelium cells. J. Theor. Biol. 219, 301–308 (2002)

    Google Scholar 

  42. A.F.M. Maree, P. Hogeweg, How amoeboids self-organize into a fruiting body: multicellular coordination in Dictyostelium discoideum. Proc. Natl. Acad. Sci. USA 98, 3879–3883 (2001)

    Google Scholar 

  43. A.J. Durston, Dislocation is a developmental mechanism in Dictyostelium and vertebrates. Proc. Natl. Acad. Sci. 110, 19826 (2013)

    Google Scholar 

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Authors and Affiliations

  1. Division of Cell and Developmental Biology, School of Life Sciences, University of Dundee, Dundee, DD1 5EH, UK

    Cornelis J. Weijer

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  1. Cornelis J. Weijer
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Correspondence to Cornelis J. Weijer .

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Editors and Affiliations

  1. Shimadzu Europa GmbH, Duisburg, Germany

    Kinko Tsuji

  2. Institute of Physics, Otto von Guericke University Magdeburg, Magdeburg, Germany

    Stefan C. Müller

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Weijer, C.J. (2019). Spiral Waves of the Chemo-Attractant cAMP Organise Multicellular Development in the Social Amoebae Dictyostelium discoideum . In: Tsuji, K., Müller, S.C. (eds) Spirals and Vortices. The Frontiers Collection. Springer, Cham. https://doi.org/10.1007/978-3-030-05798-5_10

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