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. 1984 Jan;3(1):201–206. doi: 10.1002/j.1460-2075.1984.tb01784.x

Evidence that positional information is used to establish the prestalk-prespore pattern in Dictyostelium discoideum aggregates

Marianne Krefft 1,1,*, Ludwig Voet 1, James H Gregg 1,2, Helga Mairhofer 1, Keith L Williams 1,3
PMCID: PMC557320  PMID: 16453494

Abstract

Two contrasting mechanisms have been proposed for the establishment of the prestalk-prespore pattern in the multicellular aggregate of the simple eukaryote Dictyostelium discoideum. One involves intermingled, non-position-dependent cell differentiation followed by sorting out which produces the pattern of prestalk cells in the anterior region and prespore cells posteriorly. The second mechanism involves patterning according to the position of cells within the aggregate, in which case intermingled cell types are not expected. Here we use a monoclonal antibody (MUD1), recognising a prespore cell surface antigen, to study the initial appearance of prespore cells in aggregates. Quantitative studies were made with a flow cytometer and frozen sections were used to localise the cells expressing the prespore antigen. This antigen first appeared at the onset of tip formation in the centre of aggregates in a position-dependent fashion. The prespore antigen was not detected in the tip region or in streams of cells entering the aggregate. We re-examined the evidence on which the non-position-dependent differentiation model is based. Our results support the positional model for pattern formation.

Keywords: Dictyostelium discoideum, monoclonal antibody, proportion regulation, patterning, morphogenesis

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Durston A. J., Vork F. A cinematographical study of the development of vitally stained Dictyostelium discoideum. J Cell Sci. 1979 Apr;36:261–279. doi: 10.1242/jcs.36.1.261. [DOI] [PubMed] [Google Scholar]
  2. Forman D., Garrod D. R. Pattern formation in Dictyostelium discoideum. II. Differentiation and pattern formation in non-polar aggregates. J Embryol Exp Morphol. 1977 Aug;40:229–243. [PubMed] [Google Scholar]
  3. Garrod D. R., Ashworth I. M. Effect of growth conditions on development of the cellular slime mould, Dictyostelium discoideum. J Embryol Exp Morphol. 1972 Oct;28(2):463–479. [PubMed] [Google Scholar]
  4. Garrod D. R., Nicol A. Cell behaviour and molecular mechanisms of cell-cell adhesion. Biol Rev Camb Philos Soc. 1981 May;56(2):199–242. doi: 10.1111/j.1469-185x.1981.tb00348.x. [DOI] [PubMed] [Google Scholar]
  5. Gregg J. H., Krefft M., Haas-Kraus A., Williams K. L. Antigenic differences detected between prespore cells of Dictyostelium discoideum and Dictyostelium mucoroides using monoclonal antibodies. Exp Cell Res. 1982 Nov;142(1):229–233. doi: 10.1016/0014-4827(82)90427-x. [DOI] [PubMed] [Google Scholar]
  6. Gross J. D., Town C. D., Brookman J. J., Jermyn K. A., Peacey M. J., Kay R. R. Cell patterning in Dictyostelium. Philos Trans R Soc Lond B Biol Sci. 1981 Oct 7;295(1078):497–508. doi: 10.1098/rstb.1981.0156. [DOI] [PubMed] [Google Scholar]
  7. Hames B. D., Ashworth J. M. The metabolism of macromolecules during the differentiation of Myxamoebae of the cellular slime mould Dictyostelium discoideum containing different amounts of glycogen. Biochem J. 1974 Aug;142(2):301–315. doi: 10.1042/bj1420301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Inouye K., Takeuchi I. Correlations between prestalk-prespore tendencies and cAMP-related activities in Dictyostelium discoideum. Exp Cell Res. 1982 Apr;138(2):311–318. doi: 10.1016/0014-4827(82)90180-x. [DOI] [PubMed] [Google Scholar]
  9. Kay R. R., Jermyn K. A. A possible morphogen controlling differentiation in Dictyostelium. Nature. 1983 May 19;303(5914):242–244. doi: 10.1038/303242a0. [DOI] [PubMed] [Google Scholar]
  10. Krefft M., Voet L., Mairhofer H., Williams K. L. Analysis of proportion regulation in slugs of Dictyostelium discoideum using a monoclonal antibody and a FACS-IV. Exp Cell Res. 1983 Aug;147(1):235–239. doi: 10.1016/0014-4827(83)90291-4. [DOI] [PubMed] [Google Scholar]
  11. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  12. Leach C. K., Ashworth J. M., Garrod D. R. Cell sorting out during the differentiation of mixtures of metabolically distinct populations of Dictyostelium discoideum. J Embryol Exp Morphol. 1973 Jun;29(3):647–661. [PubMed] [Google Scholar]
  13. Matsukuma S., Durston A. J. Chemotactic cell sorting in Dictyostelium discoideum. J Embryol Exp Morphol. 1979 Apr;50:243–251. [PubMed] [Google Scholar]
  14. Meinhardt H. A model for the prestalk/prespore patterning in the slug of the slime mold Dictyostelium discoideum. Differentiation. 1983;24(3):191–202. doi: 10.1111/j.1432-0436.1983.tb01319.x. [DOI] [PubMed] [Google Scholar]
  15. Newell P. C., Telser A., Sussman M. Alternative developmental pathways determined by environmental conditions in the cellular slime mold Dictyostelium discoideum. J Bacteriol. 1969 Nov;100(2):763–768. doi: 10.1128/jb.100.2.763-768.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Schaap P., van der Molen L., Konijn T. M. The organisation of fruiting body formation in Dictyostelium minutum. Cell Differ. 1983 May;12(5):287–297. doi: 10.1016/0045-6039(83)90025-8. [DOI] [PubMed] [Google Scholar]
  17. Smith E., Williams K. L. Evidence for tip control of the 'slug/fruit' switch in slugs of Dictyostelium discoideum. J Embryol Exp Morphol. 1980 Jun;57:233–240. [PubMed] [Google Scholar]
  18. Stenhouse F. O., Williams K. L. Patterning in Dictyostelium discoideum: the proportions of the three differentiated cell types (spore, stalk, and basal disk) in the fruiting body. Dev Biol. 1977 Sep;59(2):140–152. doi: 10.1016/0012-1606(77)90249-4. [DOI] [PubMed] [Google Scholar]
  19. TAKEUCHI I. IMMUNOCHEMICAL AND IMMUNOHISTOCHEMICAL STUDIES ON THE DEVELOPMENT OF THE CELLULAR SLIME MOLD DICTYOSTELIUM MUCOROIDES. Dev Biol. 1963 Aug;8:1–26. doi: 10.1016/0012-1606(63)90023-x. [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. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]

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