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The extracellular matrix of theDictyostelium discoideum slug

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Abstract

In this review, we detail the current understanding of the extracellular matrix (ECM) of the migratory slug phase of the cellular slime mould,Dictyostelium discoideum. We describe some structural and non-structural molecules which comprise the ECM, and how these molecules reflect both plant and animal ECM systems. We also describe zones of the multicellular slug that are known to make ECM components, including the role of the prestalk cells and the slug epithelium-like layer. Finally, we review the contributions of studies on mutant to our understanding of the ECM ofD. discoideum, and relate this to differentiation and development in more complex eukaryotic systems.

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References

  1. Adams, J. C., and Watt, F. M., Regulation of development and differentiation by the extracellular matrix. Development117 (1993) 1183–1198.

    Article  CAS  PubMed  Google Scholar 

  2. Alexander, S., Smith, E., Davis, L., Gooley, A. A., Por, S. B., Browne, L., and Williams, K. L., Characterization of an antigenically related family of cell-type specific proteins implicated in slug migration inDictyostelium discoideum. Differentiation38 (1988) 82–90.

    Article  CAS  PubMed  Google Scholar 

  3. Blanton, R. L., Prestalk cells in monolayer cultures exhibit two distinct modes of cellulose synthesis during stalk cell differentiation inDictyostelium. Development199 (1993) 703–710.

    Article  Google Scholar 

  4. Bonner, J. T., Davidowski, T. A., Hsu, W.-L., Lapeyrolerie, D. A., and Suthers, H. L. B., The role of surface water and light on differentiation in the cellular slime molds. Differentiation21 (1982) 123–126.

    Article  Google Scholar 

  5. Bonner, J. T., Koontz, P. G., and Paton, D., Size in relation to the rate of migration in the slime mould. Mycologia45 (1953) 235–240.

    Article  Google Scholar 

  6. Breen, E. J., Eliott, S., Vardy, P. H., White A., and Williams, K. L., Length regulation in theDictyostelium discoideum slug is a late event. J. exp. Zool.262 (1992) 299–306.

    Article  CAS  PubMed  Google Scholar 

  7. Breen, E. J., Vardy, P. H., and Williams, K. L., Movement of the multicellular slug stage ofDictyostelium discoideum: an analytical approach. Development101 (1987) 313–321.

    Article  Google Scholar 

  8. Breen, E. J., and Williams, K. L., Movement of theDictyostelium discoideum slug: models, musings and images. Devl Genet.9 (1988) 539–548.

    Article  CAS  Google Scholar 

  9. Breen, E. J., and Williams, K. L., Optical flow analysis of the ventral cellular layer of the migratingDictyostelium discoideum slug. Microbiology140 (1994) 1241–1252.

    Article  PubMed  Google Scholar 

  10. Browne, L. H., and Williams, K. L., Gradients in the expression of cell surface glycoproteins in a simple tissue, theDictyostelium discoideum slug. J. gen. Microbiol.139 (1993) 847–853.

    Article  CAS  Google Scholar 

  11. Carpita, N. C., and Gibeaut, D. M., Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J.3 (1993) 1–30.

    Article  CAS  PubMed  Google Scholar 

  12. Ceccarelli, A., McRobbie, S. J., Jermyn, K. A., Duffy, K., Early, A., and Williams, J. G., Structural and functional characterisation of aDictyostelium gene encoding a DIF inducible, prestalk-enriched mRNA sequence. Nucleic Acids Res.15 (1987) 7463–7476.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Champion, A., Gooley, A. A., Callaghan, M., Carrin, M. I., Bernstein, R. L., Smith, E., and Williams, K. L., Immunodominant carbohydrate determinants in the multicellular stages ofDictyostelium discoideum. J. gen. Microbiol.137 (1991) 2431–2438.

    Article  CAS  PubMed  Google Scholar 

  14. DeLozanne, A., and Spudich, J. A., Disruption of theDictyostelium myosin heavy chain by homologous recombination. Science236 (1987) 1086–1091.

    Article  CAS  Google Scholar 

  15. Dimond, R. L., Farnsworth, P. A., and Loomis, W. F., Isolation and characterisation of mutations affecting UDPG pyrophosphorylase activity inDictyostelium discoideum. Devl Biol.50 (1976) 169–181.

    Article  CAS  Google Scholar 

  16. Farnsworth, P. A., and Loomis, W. F., A gradient in the thickness of the surface sheath in pseudoplasmodia ofDictyostelium discoideum. Devl Biol.46 (1975) 349–357.

    Article  CAS  Google Scholar 

  17. Feit, I. N., Cell prints on the surface of the slug ofDictyostelium discoideum: a Nessler-positive matrix substance. Devl Biol.164 (1994) 345–360.

    Article  CAS  Google Scholar 

  18. Fisher, P. R., and Williams, K. L., Bidirectional phototaxis byDictyostelium discoideum slugs. FEMS Microbiol. Lett.12 (1981) 87–89.

    Article  Google Scholar 

  19. Freeze, H., and Loomis, W. F., Isolation and characterisation of a component of the surface sheath ofDictyostelium discoideum. J. Biol. Chem.252 (1977) 820–824.

    Article  CAS  PubMed  Google Scholar 

  20. Freeze, H., and Loomis, W. F., The role of the fibrillar component of the surface sheath in the morphogenesis ofDictyostelium discoideum. Devl Biol.56 (1977) 184–194.

    Article  CAS  Google Scholar 

  21. Fuchs, M., Cell interactions and the ECM ofDictyostelium discoideum. Ph.D. Thesis, Macquarie University, Sydney, Australia 1993.

    Google Scholar 

  22. Fuchs, M., Jones, M. K., and Williams, K. L., Characterisation of an epithelium-like layer of cells in the multicellularDictyostelium discoideum slug. J. Cell Sci.105 (1993) 243–253.

    Article  PubMed  Google Scholar 

  23. Garrod, D. R., Palmer, J. F., and Wolpert, L., Electrical properties of the slime mould grex. J. Embryol. expl Morph.23 (1970) 311–322.

    CAS  Google Scholar 

  24. George, R. P., Hohl, H. R., and Raper, K. B., Ultrastructural development of stalk producing cells inDictyostelium discoideum, a cellular slime mould. J. gen. Microbiol.70 (1972) 477–489.

    Article  CAS  PubMed  Google Scholar 

  25. Gooley, A. A., Marschalek, R., and Williams, K. L., Size polymorphisms due to changes in the number of O-glycosylated tandem repeats in theDictyostelium discoideum glycoprotein PsA. Genetics130 (1992) 749–756.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Grant, W. N., Welker, D. L., and Williams, K. L., A polymorphic, prespore-specific surface glycoprotein present in the extracellular matrix ofDictyostelium discoideum. Molec. cell. Biol.5 (1985) 2559–2566.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Grant, W. N., and Williams, K. L., Monoclonal antibody characterisation of the slime sheath: the extracellular matrix ofDictyostelium discoideum. EMBO J.2 (1983) 935–940.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Greenburg, G., and Hay, E. D., Cytodifferentiation and tissue phenotype change during transformation of embryonic lens epithelium to mesenchyme-like cells in vitro. Devl Biol.115 (1986) 363–379.

    Article  CAS  Google Scholar 

  29. Greenburg, G., and Hay, E. D., Cytoskeleton and thyroglobulin expression change during transformation of thyroid epithelium to mesenchyme-like cells. Development102 (1988) 605–622.

    Article  CAS  PubMed  Google Scholar 

  30. Harshey, R. M., Bees aren't the only ones—swarming in gram negative bacteria. Molec. Microbiol.13 (1994) 389–394.

    Article  CAS  Google Scholar 

  31. Haynes, P. A., Gooley, A. A., Ferguson, M. A., Redmond, J. W., and Williams, K. L., Post-translational modifications of theDictyostelium discoideum glycoprotein PsA. Eur. J. Biochem.216 (1993) 729–737.

    Article  CAS  PubMed  Google Scholar 

  32. Hohl, H., and Jehli, J., The presence of cellulose microfibrils in proteinaceous slime track ofDictyostelium discoideum. Arch. Mikrobiol.92 (1973) 179–187.

    Article  CAS  PubMed  Google Scholar 

  33. Jermyn, K. A., Berks, M., Kay, R. R., and Williams, J. G., Two distinct classes of pre-stalk enriched mRNA sequences inDictyostelium discoideum. Development100 (1987) 745–755.

    Article  CAS  PubMed  Google Scholar 

  34. Jermyn, K. A., Duffy, K. T. I., and Williams, J. G., A new anatomy of the prestalk zone inDictyostelium. Nature, Lond.340 (1989) 144–146.

    Article  CAS  PubMed  Google Scholar 

  35. Jones, T. H. D., and Gupta, M., A protein inhibitor of cellulases inDictyostelium discoideum. Biochem. biophys. Res. Commun.102 (1981) 1310–1316.

    Article  CAS  PubMed  Google Scholar 

  36. Kramer, J. M., French, R. P., Park, E., and Johnson, J. J., TheCaenorhabditis elegans rol-6 gene, which interacts with thesqt-1 collagen gene to determine organismal morphology, encodes a collagen. Molec cell. Biol.10 (1990) 2081–2089.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Loomis, W. F., Role of the surface sheath in the control of morphogenesis inD. discoideum. Nature New Biol.240 (1972) 6–9.

    Article  PubMed  Google Scholar 

  38. Loomis, W. F., Wheeler, S. A., Springer, W. R., and Barondes, S. H., Adhesion mutants ofDictyostelium discoideum lacking the saccharide determinant recognised by two adhesion-blocking monoclonal antibodies. Devl Biol.109 (1985) 111–117.

    Article  CAS  Google Scholar 

  39. MacWilliams, H. K., and David, C. N., Pattern formation inDictyostelium, in: Microbial Development, Cold Spring Harbor Monograph 16, pp. 225–274. Eds. R. Losick and L. Shapiro. Cold Spring Harbor Laboratory Press, New York 1984.

    Google Scholar 

  40. Maresz-Babczyszyn J., and Sokalska, M., Immunogenic properties of slime produced byPseudomonas aeruginosa. Arch. Immunol. Ther. Exp.27 (1979) 585–589.

    CAS  Google Scholar 

  41. Martinez, J. P., Gil, M. L., Casanova, M., Rico, M., Sentandreu, R., and Ruiz-Herrera, J., Characterization of a proteinaceous extracellular coat synthesized by the ‘slime’ variant ofNeurospora crassa, Archs Microbiol.152 (1989) 25–32.

    Article  CAS  Google Scholar 

  42. McRobbie, S. J., Jermyn, K. A., Duffy, K., Blight, K., and Williams, J. G., Two DIF-inducible, prestalk-specific mRNAs ofDictyostelium encode extracellular matrix proteins of the slug. Development104 (1988) 275–284.

    Article  CAS  PubMed  Google Scholar 

  43. McRobbie, S. J., Tilly, R., Blight, K., Ceccarelli, A., and Williams, J. G., Identification and localization of proteins encoded by two DIF-inducible genes ofDictyostelium. Devl. Biol.125 (1988) 59–63.

    Article  CAS  Google Scholar 

  44. Morris, P. J., The developmental role of the ECM suggests a monophyletic origin of the kingdom animalia. Evolution47 (1993) 152–165.

    Article  PubMed  Google Scholar 

  45. Morrison, A., Blanton, R. L., Grimson, M., Fuchs, M., Williams, K. L., and Williams, J., Disruption of the gene encoding the EcmA, extracellular matrix protein ofDictyostelium, alters slug morphology. Devl Biol.163 (1994) 457–466.

    Article  CAS  Google Scholar 

  46. Newell, P. C., Telser, A., and Sussman, M., Alternative developmental pathways determined by environmental conditions in the cellular slime moldDictyostelium discoideum. J. Bacteriol.100 (1969) 763–768.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Odell, G. M., and Bonner, J. T., How theDictyostelium discoideum grex crawls. Phil. Trans. R. Soc.B312 (1986) 487–525.

    Google Scholar 

  48. Omar, A. S., Weckesser, J., and Mayer, H., Different polysaccharides in the external layers (capsule and slime) of the cell envelope ofRhodopseudomonas capsulata Sp11. Archs Microbiol.136 (1983) 291–296.

    Article  CAS  Google Scholar 

  49. Paddock R. B., The appearance of amoebach tracks in cultures ofDcityostelium discoideum. Science188 (1953) 597–598.

    Article  Google Scholar 

  50. Raper, K. B., Pseudoplasmodium formation and organisation inDictyostelium discoideum. J. Elisha Mitchell Sci. Soc.56 (1940) 241–282.

    Google Scholar 

  51. Raper, K. B., The Dictyostelids. Princeton University Press, New Jersey 1984.

    Book  Google Scholar 

  52. Shaffer, B. M., Cell movement within aggregates of the slime mouldDictyostelium discoideum, revealed by surface markers. J. Embryol. exp. Morph.13 (1965) 97–117.

    CAS  PubMed  Google Scholar 

  53. Siegert, F., Weijer, C. J., Nomura, A., and Miike, H., A gradient method for the quantitative analysis of cell movement and tissue flow and its application to the analysis of multicellularDictyostelium development. J. Cell Sci.107 (1994) 97–104.

    Article  PubMed  Google Scholar 

  54. Smith, E., and Williams, K. L., Preparation of slime sheath fromDictyostelium discoideum. FEMS Microbiol. Lett.6 (1979) 119–122.

    Article  CAS  Google Scholar 

  55. Steinbock, O., Siegert, F., Mueller, S. C., and Weijer, C. J., Three-dimensional waves of excitation duringDictyostelium morphogenesis. Proc. natl Acad. Sci. USA90 (1993) 7332–7335.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Sternfeld, J., and David, C. N., Cell sorting during pattern formation inDictyostelium. Differentiation20 (1981) 10–21.

    Article  CAS  Google Scholar 

  57. Sternfeld, J., and David, C. N., Fate and regulation of anteriorlike cells inDictyostelium slugs. Devl Biol.93 (1982) 111–118.

    Article  CAS  Google Scholar 

  58. Sussman, M., The program of polysaccharide and disaccharide synthesis during development ofDictyostelium discoideum, in: Biochemistry of the Glycosidic Linkage, pp. 431–448. Eds. R. Piras and H. G. Pontis. Academic Press, New York 1972.

    Chapter  Google Scholar 

  59. Tannich, E., Ebert, F., and Horstmann, R. D., Primary structure of the 170-kDa surface lectin of pathogenicEntamoeba histolytica. Proc. natl Acad. Sci. USA.88 (1991) 1849–1853.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Vardy P. H., Fisher, L. R., Smith, E., and Williams, K. L., Traction proteins in the extracellular matrix ofDictyostelium discoideum slugs. Nature, Lond.320 (1986) 526–529.

    Article  CAS  Google Scholar 

  61. Vardy, P. H., The extracellular matrix and locomotion in theDictyostelium discoideum slug. Ph. D. Thesis, Macquarie University, Sydney, Australia 1992.

    Google Scholar 

  62. Voct, L., Krefft, M., Bruderlein, M., and Williams, K.L., Flow cytometer study of anterior-like cells inDictyostelium discoideum. J. Cell Sci.75 (1985) 423–435.

    Article  Google Scholar 

  63. Wallace, J. S., Morrissey, J. H., and Newell, P. C., Monoclonal antibodies specific for stalk differentiation inDictyostelium discoideum. Cell Differ.14 (1984) 205–211.

    Article  CAS  PubMed  Google Scholar 

  64. Watson, N., Williams, K. L., and Alexander, S., A developmentally regulated glycoprotein complex fromDictyostelium discoideum. J. biol. Chem.268 (1993) 22634–22641.

    Article  CAS  PubMed  Google Scholar 

  65. Watts, D. J., and Treffry, T. E., Incorporation of N-acetylglucosamine into the slime sheath of the cellular slime mouldDictyostelium discoideum. FEBS Lett.52 (1975) 262–264.

    Article  CAS  PubMed  Google Scholar 

  66. West, C. M., and Erdos, G. W., Formation of theDictyostelium spore coat. Devl Genet.11 (1990) 492–506.

    Article  CAS  Google Scholar 

  67. West, C. M., and Erdos, G. W., Incorporation of protein into spore coats is not cell autonomous inDictyostelium. J. Cell Biol.116 (1992) 1291–1300.

    Article  CAS  PubMed  Google Scholar 

  68. West, C. M., and Erdos, G. W., The expression of glycoproteins in the extracellular matrix of the cellular slime mouldDictyostelium discoideum. Cell Differ.23 (1988) 1–16.

    Article  CAS  PubMed  Google Scholar 

  69. West, C. M., and Loomis, W. F., Absence of a carbohydrate modification does not affect the level of subcellular localisation of three membrane glycoproteins inmodB mutants ofDictyostelium discoideum. J. biol. Chem.260 (1985) 13803–13809.

    Article  CAS  PubMed  Google Scholar 

  70. Whitfield, F. E., The use of proteolytic and other enzymes in the separation of the slime mould grex. Expl Cell Res.36 (1964) 62–72.

    Article  CAS  Google Scholar 

  71. Wilkinson, B. J., Staphylococcal capsules and slime, in: Staphylococci and Staphylococcus Infections 2, pp. 481–523. Academic Press, London 1983.

    Google Scholar 

  72. Williams, J. G., Ceccarelli, A., McRobbie, S., Mahbubani, H., Kay, R. R., Early, A., Berks, M., and Jermyn, K. A., Direct induction ofDictyostelium prestalk gene expression by DIF provides evidence that DIF is a morphogen. Cell49 (1987) 185–192.

    Article  CAS  PubMed  Google Scholar 

  73. Williams, J. G., and Jermyn, K. A., Cell sorting and positional differentiation duringDictyostelium morphogenesis, in: Cell-Cell Interactions in Early Development, pp. 261–272. Wiley-Liss, Inc. 1991.

  74. Williams, K. L., Vardy, P. H., and Segel, C. A., Cell migrations during morphogenesis: some clues from the slug ofDictyostelium discoideum. BioEssays5 (1986) 148–152.

    Article  CAS  PubMed  Google Scholar 

  75. Wright, I. G., Casu, R., Commins, M. A., Dalrymple, B. P., Gale, K. R., Goodger, B. V., Riddles, P. W., Waltisbuhl, D. J., and Abetz, I., The development of a recombinantBabesia vaccine. Vet. Path.44 (1992) 3–13.

    CAS  Google Scholar 

  76. Wu, L., and Franke, J., A developmentally regulated and cAMP-repressible gene ofDictyostelium discoideum: cloning and expression of the gene encoding cyclic nucleotide phosphodiesterase inhibitor. Gene91 (1990) 51–56.

    Article  CAS  PubMed  Google Scholar 

  77. Yost, H. J., Regulation of vertebrate left-right asymmetries by extracellular matrix. Nature, Lond.357 (1992) 158–161.

    Article  CAS  PubMed  Google Scholar 

  78. Zhou-Chou, A. T., Characterisation of cell surface and ECM glycoproteins inDictyostelium discoideum. Ph. D. Thesis, Macquarie University, Sydney, Australia.

  79. Zhou-Chou, A. T., Wilkins, M. R., Vardy, P. H., Gooley, A. A., and Williams, K. L., Glycoprotein complexes interacting with cellulose in the ‘cell print’ zones of theDictyostelium discoideum extracellular matrix. Devl Biol.168 (1995) 332–341.

    Article  CAS  Google Scholar 

  80. Zuk, A., Matlin, K. S., and Hay, E. D., Type I collagen gel induces Madin-Darby canine kidney cells to become fusiform in shape and lose apical-basal polarity. J. Cell Biol.108 (1989) 903–920.

    Article  CAS  PubMed  Google Scholar 

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  1. School of Biological Sciences, Macquarie University, 2109, Sydney, N.S.W., Australia

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Wilkins, M.R., Williams, K.L. The extracellular matrix of theDictyostelium discoideum slug. Experientia 51, 1189–1196 (1995). https://doi.org/10.1007/BF01944736

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