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. 1998 Dec;75(6):2615–2625. doi: 10.1016/S0006-3495(98)77707-0

Possible cooperation of differential adhesion and chemotaxis in mound formation of Dictyostelium.

Y Jiang 1, H Levine 1, J Glazier 1
PMCID: PMC1299937  PMID: 9826586

Abstract

In the mound stage of Dictyostelium discoideum, pre-stalk cells sort and form a tip at the apex. How this pattern forms is as yet unknown. A cellular level model allows us to simulate both differential cell adhesion and chemotaxis, to show that with differential adhesion only, pre-stalk cells move to the surface of the mound but form no tip. With chemotaxis driven by an outgoing circular wave only, a tip forms but contains both pre-stalk and pre-spore cells. Only for a narrow range of relative strengths between differential adhesion and chemotaxis can both mechanisms work in concert to form a tip containing only pre-stalk cells. The simulations provide a method to determine the processes necessary for patterning and suggest a series of further experiments.

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Selected References

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  1. Bozzaro S., Ponte E. Cell adhesion in the life cycle of Dictyostelium. Experientia. 1995 Dec 18;51(12):1175–1188. doi: 10.1007/BF01944735. [DOI] [PubMed] [Google Scholar]
  2. Caterina M. J., Devreotes P. N. Molecular insights into eukaryotic chemotaxis. FASEB J. 1991 Dec;5(15):3078–3085. [PubMed] [Google Scholar]
  3. Doolittle K. W., Reddy I., McNally J. G. 3D analysis of cell movement during normal and myosin-II-null cell morphogenesis in dictyostelium. Dev Biol. 1995 Jan;167(1):118–129. doi: 10.1006/dbio.1995.1011. [DOI] [PubMed] [Google Scholar]
  4. Fisher P. R., Merkl R., Gerisch G. Quantitative analysis of cell motility and chemotaxis in Dictyostelium discoideum by using an image processing system and a novel chemotaxis chamber providing stationary chemical gradients. J Cell Biol. 1989 Mar;108(3):973–984. doi: 10.1083/jcb.108.3.973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Foty R. A., Pfleger C. M., Forgacs G., Steinberg M. S. Surface tensions of embryonic tissues predict their mutual envelopment behavior. Development. 1996 May;122(5):1611–1620. doi: 10.1242/dev.122.5.1611. [DOI] [PubMed] [Google Scholar]
  6. Glazier JA, Graner F. Simulation of the differential adhesion driven rearrangement of biological cells. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics. 1993 Mar;47(3):2128–2154. doi: 10.1103/physreve.47.2128. [DOI] [PubMed] [Google Scholar]
  7. Goldstein RE. Traveling-Wave Chemotaxis. Phys Rev Lett. 1996 Jul 22;77(4):775–778. doi: 10.1103/PhysRevLett.77.775. [DOI] [PubMed] [Google Scholar]
  8. Graner F, Glazier JA. Simulation of biological cell sorting using a two-dimensional extended Potts model. Phys Rev Lett. 1992 Sep 28;69(13):2013–2016. doi: 10.1103/PhysRevLett.69.2013. [DOI] [PubMed] [Google Scholar]
  9. Kessler DA, Levine H. Pattern formation in Dictyostelium via the dynamics of cooperative biological entities. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics. 1993 Dec;48(6):4801–4804. doi: 10.1103/physreve.48.4801. [DOI] [PubMed] [Google Scholar]
  10. Loomis W. F. Lateral inhibition and pattern formation in Dictyostelium. Curr Top Dev Biol. 1993;28:1–46. doi: 10.1016/s0070-2153(08)60208-2. [DOI] [PubMed] [Google Scholar]
  11. Mombach JC, Glazier JA. Single cell motion in aggregates of embryonic cells. Phys Rev Lett. 1996 Apr 15;76(16):3032–3035. doi: 10.1103/PhysRevLett.76.3032. [DOI] [PubMed] [Google Scholar]
  12. Rietdorf J., Siegert F., Weijer C. J. Analysis of optical density wave propagation and cell movement during mound formation in Dictyostelium discoideum. Dev Biol. 1996 Aug 1;177(2):427–438. doi: 10.1006/dbio.1996.0175. [DOI] [PubMed] [Google Scholar]
  13. Rubin J., Robertson A. The tip of the Dictyostelium discoideum pseudoplasmodium as an organizer. J Embryol Exp Morphol. 1975 Feb;33(1):227–241. [PubMed] [Google Scholar]
  14. STEINBERG M. S. Reconstruction of tissues by dissociated cells. Some morphogenetic tissue movements and the sorting out of embryonic cells may have a common explanation. Science. 1963 Aug 2;141(3579):401–408. doi: 10.1126/science.141.3579.401. [DOI] [PubMed] [Google Scholar]
  15. Saxe C. L., 3rd, Ginsburg G. T., Louis J. M., Johnson R., Devreotes P. N., Kimmel A. R. CAR2, a prestalk cAMP receptor required for normal tip formation and late development of Dictyostelium discoideum. Genes Dev. 1993 Feb;7(2):262–272. doi: 10.1101/gad.7.2.262. [DOI] [PubMed] [Google Scholar]
  16. Shaulsky G., Kuspa A., Loomis W. F. A multidrug resistance transporter/serine protease gene is required for prestalk specialization in Dictyostelium. Genes Dev. 1995 May 1;9(9):1111–1122. doi: 10.1101/gad.9.9.1111. [DOI] [PubMed] [Google Scholar]
  17. Siegert F., Weijer C. J. Spiral and concentric waves organize multicellular Dictyostelium mounds. Curr Biol. 1995 Aug 1;5(8):937–943. doi: 10.1016/s0960-9822(95)00184-9. [DOI] [PubMed] [Google Scholar]
  18. Siu C. H., Des Roches B., Lam T. Y. Involvement of a cell-surface glycoprotein in the cell-sorting process of Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1983 Nov;80(21):6596–6600. doi: 10.1073/pnas.80.21.6596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Takeuchi I., Kakutani T., Tasaka M. Cell behavior during formation of prestalk/prespore pattern in submerged agglomerates of Dictyostelium discoideum. Dev Genet. 1988;9(4-5):607–614. doi: 10.1002/dvg.1020090437. [DOI] [PubMed] [Google Scholar]
  20. Tasaka M., Takeuchi I. Role of cell sorting in pattern formation in Dictyostelium discoideum. Differentiation. 1981;18(3):191–196. doi: 10.1111/j.1432-0436.1981.tb01122.x. [DOI] [PubMed] [Google Scholar]
  21. Traynor D., Kessin R. H., Williams J. G. Chemotactic sorting to cAMP in the multicellular stages of Dictyostelium development. Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):8303–8307. doi: 10.1073/pnas.89.17.8303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Varnum B., Edwards K. B., Soll D. R. The developmental regulation of single-cell motility in Dictyostelium discoideum. Dev Biol. 1986 Jan;113(1):218–227. doi: 10.1016/0012-1606(86)90124-7. [DOI] [PubMed] [Google Scholar]
  23. Wang B., Kuspa A. Dictyostelium development in the absence of cAMP. Science. 1997 Jul 11;277(5323):251–254. doi: 10.1126/science.277.5323.251. [DOI] [PubMed] [Google Scholar]
  24. Wessels D., Murray J., Soll D. R. Behavior of Dictyostelium amoebae is regulated primarily by the temporal dynamic of the natural cAMP wave. Cell Motil Cytoskeleton. 1992;23(2):145–156. doi: 10.1002/cm.970230207. [DOI] [PubMed] [Google Scholar]
  25. Williams J. G. Regulation of cellular differentiation during Dictyostelium morphogenesis. Curr Opin Genet Dev. 1991 Oct;1(3):358–362. doi: 10.1016/s0959-437x(05)80300-4. [DOI] [PubMed] [Google Scholar]

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