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Dictyostelium Development: A Prototypic Wnt Pathway?

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Wnt Signaling

Part of the book series: Methods in Molecular Biology ((MIMB,volume 469))

Abstract

Although Wnt signaling is ubiquitous within the animal phylogenetic group, it is unclear how it evolved. Genes related to the components of Wnt pathway are found in other eukaryotes and one of the most studied of these non-metazoan organisms is the social amoeba Dictyostelium discoideum. This organism contains the enzyme GSK-3 and a β -catenin homolog, Aardvark (Aar). Both are required to regulate pattern formation during multi-cellular stages of Dictyostelium development. Aar is also required for formation of adherens junctions, as seen in animals. Finally, analysis of the completed Dictyostelium genome shows there to be 16 Frizzled (Fz) gene homologs. This chapter discusses Dictyostelium development and the role of these proteins.

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References

  1. Baldauf, S. L., Doolittle, W. F. (1997) Origin and evolution of the slime molds (Mycetozoa) Proc Natl Acad Sci USA 94, 12007–12012.

    Article  PubMed  CAS  Google Scholar 

  2. Eichinger, L., et al. (2005) The genome of the social amoeba Dictyostelium discoideum. Nature 435, 43–57.

    Article  Google Scholar 

  3. Chisholm, R. L. Gaudet, P., Just, E. M., Pilcher, K. E., Fey, P., Merchant, S. N., Kibbe, W. A. (2006) dictyBase, the model organism database for Dictyostelium discoi deum. Nucleic Acids Res 34, D423–427.

    Article  PubMed  CAS  Google Scholar 

  4. Kuspa, A., Loomis, W. F. (1992) Tagging developmental genes in Dictyostelium by restriction enzyme-mediated integration of plasmid DNA. Proc Natl Acad Sci USA 89, 8803–8807.

    Article  PubMed  CAS  Google Scholar 

  5. Morio, T. et al. (1998) The Dictyostelium developmental cDNA project: generation and analysis of expressed sequence tags from the first-finger stage of development. DNA Res 5, 335–340.

    Article  PubMed  CAS  Google Scholar 

  6. Kessin, R. H. (2001) Dictyostelium: Evo lution, Cell Biology, and the Development of Multicellularity. Cambridge University Press, Cambridge, UK.

    Book  Google Scholar 

  7. Watts, D. J., Ashworth, J. M. (1970) Growth of myxameobae of the cellular slime mould Dictyostelium discoideum in axenic culture. Biochem J 119, 171–174.

    PubMed  CAS  Google Scholar 

  8. Zimmerman, W., Weijer, C. J. (1993) Analysis of cell cycle progression during the development of Dictyostelium and its relationship to differentiation. Dev Biol 160, 178–185.

    Article  PubMed  CAS  Google Scholar 

  9. Thompson, C. R., Kay, R. R. (2000) Cell-fate choice in Dictyostelium: intrinsic biases modulate sensitivity to DIF signaling. Dev Biol 227, 56–64.

    Article  PubMed  CAS  Google Scholar 

  10. Iranfar, N., Fuller, D., Loomis, W. F. (2003) Genome-wide expression analyses of gene regulation during early development of Dictyostelium discoideum. Eukaryot Cell 2, 664–670.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  12. Town, C. D., Gross, J. D., Kay, R. R. (1976) Cell differentiation without morphogenesis in Dictyostelium discoideum. Nature 262, 717–719.

    Article  PubMed  CAS  Google Scholar 

  13. Kay, R. R. (1982) cAMP and spore differ entiation in Dictyostelium discoideum. Proc Natl Acad Sci USA 79, 3228–3231.

    Article  PubMed  CAS  Google Scholar 

  14. Early, A. E., Gaskell, M. J., Traynor, D., Williams, J. G. (1993) Two distinct popu lations of prestalk cells within the tip of the migratory Dictyostelium slug with differ ing fates at culmination. Development 118, 353–362.

    PubMed  CAS  Google Scholar 

  15. Jermyn, K., Traynor, D., Williams, J. (1996) The initiation of basal disc forma tion in Dictyostelium discoideum is an early event in culmination. Development 122, 753–760.

    PubMed  CAS  Google Scholar 

  16. Williams, J. G., Duffy, K. T., Lane, D. P., McRobbie, S. J., Harwood, A. J., Traynor, D., Kay, R. R., Jermyn, K. A. (1989) Origins of the prestalk-prespore pattern in Dictyostelium development. Cell 59, 1157–1163.

    Article  PubMed  CAS  Google Scholar 

  17. Dingermann, T., Reindl, N., Werner, H., Hildebrandt, M., Nellen, W., Harwood, A., Williams, J., Nerke, K. (1989) Optimiza tion and in situ detection of Escherichia coli β-galactosidase gene expression in Dictyos telium discoideum. Gene 85, 353–362.

    Article  PubMed  CAS  Google Scholar 

  18. Early, A., McRobbie, S. J., Duffy, K. T., Jermyn, K. A., Tilly, R., Ceccarelli, A., Williams, J. G. (1988) Structural and func tional characterization of genes encoding Dictyostelium prestalk and prespore cell specific proteins. Dev Genet 9, 383–402.

    Article  PubMed  CAS  Google Scholar 

  19. Morris, H. R., Taylor, G. W., Masento, M. S., Jermyn, K. A., Kay, R. R. (1987) Chemical structure of the morphogen differentiation inducing factor from Dictyostelium discoi deum. Nature 328, 811–814.

    Article  PubMed  CAS  Google Scholar 

  20. Masento, M. S., Morris, H. R., Taylor, G. W., Johnson, S. J., Skapski, A. C., Kay, R. R. (1988) Differentiation-inducing factor from the slime mould Dictyostelium discoi deum and its analogues. Synthesis, struc ture and biological activity. Biochem J 256, 23–28.

    PubMed  CAS  Google Scholar 

  21. Thompson, C. R., Kay, R. R. (2000) The role of DIF-1 signaling in Dictyostelium development. Mol Cell 6, 1509–1514.

    Article  PubMed  CAS  Google Scholar 

  22. Richardson, D. L., Loomis, W. F., Kimmel, A. R. (1994) Progression of an inductive signal activates sporulation in Dictyostelium discoideum. Development 120, 2891–2900.

    PubMed  CAS  Google Scholar 

  23. Ryves, W. J., Fryer, L., Dale, T., Harwood, A. J. (1998) An assay for glycogen syn thase kinase 3 (GSK-3) for use in crude cell extracts. Anal Biochem 264, 124–127.

    Article  PubMed  CAS  Google Scholar 

  24. Ryves, W. J., Harwood, A. J. (2001) Lithium inhibits glycogen synthase kinase-3 by com petition for magnesium. Biochem Biophys Res Commun 280, 720–725.

    Article  PubMed  CAS  Google Scholar 

  25. Goldberg, J. M. Manning, G., Liu, A., Fey, P., Pilcher, K. E., Xu, Y., Smith, J. L. (2006) The Dictyostelium kinome – analysis of the protein kinases from a simple model organism. PLoS Genet 2, e38.

    Article  PubMed  Google Scholar 

  26. Fraser, E., Young, N., Dajani, R., Franca Koh, J., Ryves, J., Williams, R. S., Yeo, M., Webster, M. T., Richardson, C., Smalley, M. J., Pearl, L. H, Harwood, A., Dale, T. C. (2002) Identification of the Axin and Frat binding region of glycogen synthase kinase-3. J Biol Chem 277, 2176–2185.

    Article  PubMed  CAS  Google Scholar 

  27. Harwood, A. J., Plyte, S. E., Woodgett, J., Strutt, H., Kay, R. R. (1995) Glycogen synthase kinase 3 regulates cell fate in Dictyostelium. Cell 80, 139–148.

    Article  PubMed  CAS  Google Scholar 

  28. Strmecki, L., Bloomfield, G., Araki, T., Dalton, E., Skelton, J., Schilde, C., Harwood, A., Williams, J. G., Ivens, A., Pears, C. (2007) Proteomic and microarray analyses of the Dictyostelium Zak1-GSK-3 signaling pathway reveal a role in early development. Eukaryot Cell 6, 245–252.

    Article  PubMed  CAS  Google Scholar 

  29. Ginger, R. S., Dalton, E. C., Ryves, W. J., Fukuzawa, M., Williams, J. G., Harwood, A. J. (2000) Glycogen synthase kinase-3 enhances nuclear export of a Dictyostelium STAT protein. EMBO J 19, 5483–5491.

    Article  PubMed  CAS  Google Scholar 

  30. Schilde, C., Araki, T., Williams, H., Harwood, A., Williams, J. G. (2004) GSK3 is a multi functional regulator of Dictyostelium devel opment. Development 131, 4555–4565.

    Article  PubMed  CAS  Google Scholar 

  31. Berks, M., Kay, R. R. (1990) Combinatorial control of cell differentiation by cAMP and DIF-1 during development of Dictyostelium discoideum. Development 110, 977–984.

    PubMed  CAS  Google Scholar 

  32. Plyte, S. E., O'Donovan, E., Woodgett, J. R., Harwood, A. J. (1999) Glycogen synthase kinase-3 (GSK-3) is regulated during Dictyos telium development via the serpentine recep tor cAR3. Development 126, 325–333.

    PubMed  CAS  Google Scholar 

  33. Kim, L., Liu, J., Kimmel, A. R. (1999) The novel tyrosine kinase ZAK1 activates GSK3 to direct cell fate specification. Cell 99, 399–408.

    Article  PubMed  CAS  Google Scholar 

  34. Ginsburg, G. T., Kimmel, A. R. (1997) Autonomous and nonautonomous regula tion of axis formation by antagonistic signal ing via 7-span cAMP receptors and GSK3 in Dictyostelium. Genes Dev 11, 2112–2123.

    Article  PubMed  CAS  Google Scholar 

  35. Louis, J. M., Ginsburg, G. T., Kimmel, A. R. (1994) The cAMP receptor CAR4 regulates axial patterning and cellular dif ferentiation during late development of Dictyostelium. Genes Dev 8, 2086–2096.

    Article  PubMed  CAS  Google Scholar 

  36. Kim, L., Harwood, A., Kimmel, A. R. (2002) Receptor-dependent and tyrosine phos phatase-mediated inhibition of GSK3 regu lates cell fate choice. Dev Cell 3, 523–532.

    Article  PubMed  Google Scholar 

  37. Grimson, M. J., Coates, J. C., Reynolds, J. P., Shipman, M., Blanton, R. L., Harwood, A. J. (2000) Adherens junctions and β -catenin-mediated cell signaling in a non-metazoan organism. Nature 408, 727–731.

    Article  PubMed  CAS  Google Scholar 

  38. Thorpe, C. J., Schlesinger, A., Carter, J. C., Bowerman, B. (1997) Wnt signaling polar izes an early C. elegans blastomere to distin guish endoderm from mesoderm. Cell 90, 695–705.

    Article  PubMed  CAS  Google Scholar 

  39. Lo, M. C., Gay, F., Odom, R., Shi, Y., Lin, R. (2004) Phosphorylation by the beta-catenin/ MAPK complex promotes 14-3-3-mediated nuclear export of TCF/POP-1 in signal responsive cells in C. elegans. Cell 117, 95–106.

    Article  PubMed  CAS  Google Scholar 

  40. Coates, J. C., Grimson, M. J., Williams, R. S., Bergman, W., Blanton, R. L., Harwood, A. J. (2002) Loss of the β -catenin homolog aardvark causes ectopic stalk formation in Dictyostelium. Mech Dev 116, 117–127.

    Article  PubMed  CAS  Google Scholar 

  41. Prabhu, Y., Eichinger, L. (2006) The Dicty ostelium repertoire of seven transmembrane domain receptors. Eur J Cell Biol.

    Google Scholar 

  42. Coates, J. C. (2003) Armadillo repeat pro teins: beyond the animal kingdom. Trends Cell Biol 13, 463–471.

    Article  PubMed  CAS  Google Scholar 

  43. Coates, J. C., Laplaze, L., Haseloff, J. (2006) Armadillo-related proteins promote lateral root development in Arabidopsis. Proc Natl Acad Sci USA 103, 1621–1626.

    Article  PubMed  CAS  Google Scholar 

  44. Eichinger, L., Rivero, F. (2006) Dictyostel ium discoideum Protocols. Humana Press, Totowa, New Jersey.

    Google Scholar 

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Harwood, A.J. (2008). Dictyostelium Development: A Prototypic Wnt Pathway?. In: Vincan, E. (eds) Wnt Signaling. Methods in Molecular Biology, vol 469. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-60327-469-2_2

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  • DOI: https://doi.org/10.1007/978-1-60327-469-2_2

  • Publisher Name: Humana Press, Totowa, NJ

  • Print ISBN: 978-1-60327-468-5

  • Online ISBN: 978-1-60327-469-2

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