1887

Abstract

This paper describes the serendipitous discovery and first characterization of a new resistant cell type from , for which the name aspidocyte (from : Greek for shield) is proposed. These cells are induced from amoebae by a range of toxins including heavy metals and antibiotics, and were first detected by their striking resistance to detergent lysis. Aspidocytes are separate, rounded or irregular-shaped cells, which are immotile but remain fully viable; once the toxic stress is removed, they revert to amoeboid cells within an hour. Induction takes a few hours and is completely blocked by the protein synthesis inhibitor cycloheximide. Aspidocytes lack a cell wall and their resistance to detergent lysis is active, requiring continued energy metabolism, and may be assisted by a complete cessation of endocytosis, as measured by uptake of the dye FM1-43. Microarray analysis shows that aspidocytes have a distinct pattern of gene expression, with a number of genes up-regulated that are predicted to be involved in lipid metabolism. Aspidocytes were initially detected in a hypersensitive mutant, in which the AMP deaminase gene is disrupted, suggesting that the inductive pathway involves AMP levels or metabolism. Since aspidocytes can also be induced from wild-type cells and are much more resistant than amoebae to a membrane-disrupting antibiotic, it is possible that they are an adaptation allowing cells to survive a sudden onslaught of toxins in the wild.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2006/000562-0
2007-02-01
2020-07-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/2/619.html?itemId=/content/journal/micro/10.1099/mic.0.2006/000562-0&mimeType=html&fmt=ahah

References

  1. Aguado-Velasco C., Bretscher M. S.. 1999; Circulation of the plasma membrane in Dictyostelium . Mol Biol Cell10:4419–4427[CrossRef]
    [Google Scholar]
  2. Araki T., Tsujioka M., Abe T., Fukuzawa M., Meima M., Schaap P., Morio T., Urushihara H., Katoh M.. other authors 2003; A STAT-regulated, stress-induced signalling pathway in Dictyostelium . J Cell Sci116:2907–2915[CrossRef]
    [Google Scholar]
  3. Austin M. B., Saito T., Bowman M. E., Haydock S., Kato A., Moore B. S., Kay R. R., Noel J. P.. 2006; Biosynthesis of Dictyostelium Differentiation Inducing Factor by a hybrid type I fatty acid-type III polyketide synthase. Nat Chem Biol2:494–502[CrossRef]
    [Google Scholar]
  4. Balaban N. Q., Merrin J., Chait R., Kowalik L., Leibler S.. 2004; Bacterial persistence as a phenotypic switch. Science305:1622–1625[CrossRef]
    [Google Scholar]
  5. Benjamini Y., Hochberg Y.. 1995; Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B57:289–300
    [Google Scholar]
  6. Burlando B., Evangelisti V., Dondero F., Pons G., Camakaris J., Viarengo A.. 2002; Occurrence of Cu-ATPase in Dictyostelium : possible role in resistance to copper. Biochem Biophys Res Commun291:476–483[CrossRef]
    [Google Scholar]
  7. Chae S. C., Fuller D., Loomis W. F.. 2002; Altered cell-type proportioning in Dictyostelium lacking adenosine monophosphate deaminase. Dev Biol241:183–194[CrossRef]
    [Google Scholar]
  8. Eichinger L., Pachebat J. A., Glockner G.. other authors 2005; The genome of the social amoeba Dictyostelium discoideum . Nature435:43–57[CrossRef]
    [Google Scholar]
  9. Errington J.. 2003; Regulation of endospore formation in Bacillus subtilis . Nat Rev Microbiol1:117–126[CrossRef]
    [Google Scholar]
  10. Felsenstein J.. 2005; phylip – Phylogeny Inference Package, version 3.65. Distributed by the author University of Washington; Seattle, USA:
    [Google Scholar]
  11. Firtel R., Baxter L., Lodish H.. 1973; Actinomycin D and the regulation of enzyme biosynthesis during development of Dictyostelium discoideum . J Mol Biol79:315–327[CrossRef]
    [Google Scholar]
  12. Fukuzawa M., Araki T., Adrian I., Williams J. G.. 2001; Tyrosine phosphorylation-independent nuclear translocation of a Dictyostelium STAT in response to DIF signaling. Mol Cell7:779–788[CrossRef]
    [Google Scholar]
  13. Gentleman R. C., Carey V. J., Bates D. M.. other authors 2004; Bioconductor: open software development for computational biology and bioinformatics. Genome Biol5:R80[CrossRef]
    [Google Scholar]
  14. Gross J. D., Bradbury J., Kay R. R., Peacey M. J.. 1983; Intracellular pH and the control of cell differentiation in Dictyostelium discoideum . Nature303:244–245[CrossRef]
    [Google Scholar]
  15. Gross J. D., Peacey M. J., Pogge von Strandmann R.. 1988; Plasma membrane proton pump inhibition and stalk cell differentiation in Dictyostelium discoideum . Differentiation38:91–98[CrossRef]
    [Google Scholar]
  16. Hall-Stoodley L., Costerton J. W., Stoodley P.. 2004; Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol2:95–108[CrossRef]
    [Google Scholar]
  17. Hardie D. G., Hawley S. A.. 2001; AMP-activated protein kinase: the energy charge hypothesis revisited. Bioessays23:1112–1119[CrossRef]
    [Google Scholar]
  18. Hartsel S., Bolard J.. 1996; Amphotericin B: new life for an old drug. Trends Pharmacol Sci17:445–449[CrossRef]
    [Google Scholar]
  19. Hoffman L. R., D'Argenio D. A., MacCoss M. J., Zhang Z., Jones R. A., Miller S. I.. 2005; Aminoglycoside antibiotics induce bacterial biofilm formation. Nature436:1171–1175[CrossRef]
    [Google Scholar]
  20. Horn E. G.. 1971; Food competition among the cellular slime molds (Acrasiae. Ecology52:475–484[CrossRef]
    [Google Scholar]
  21. Huang E., Blagg S. L., Keller T., Katoh M., Shaulsky G., Thompson C. R.. 2006; bZIP transcription factor interactions regulate DIF responses in Dictyostelium . Development133:449–458[CrossRef]
    [Google Scholar]
  22. Huss M. J.. 1989; Dispersal of cellular slime moulds by two soil invertebrates. Mycologia81:677–682[CrossRef]
    [Google Scholar]
  23. Insall R., Kay R. R.. 1990; A specific DIF binding protein in Dictyostelium . EMBO J9:3323–3328
    [Google Scholar]
  24. Jahngen E. G. E., Rossomando E. F.. 1986; AMP deaminase in Dictyostelium discoideum : increase in activity following nutrient deprivation induced by starvation or hadacidin. Mol Cell Biochem71:71–78
    [Google Scholar]
  25. Kay R. R.. 1987; Cell differentiation in monolayers and the investigation of slime mold morphogens. Methods Cell Biol28:433–448
    [Google Scholar]
  26. Kay R. R.. 1989; Evidence that elevated intracellular cyclic AMP triggers spore maturation in Dictyostelium . Development105:753–759
    [Google Scholar]
  27. Kay R. R.. 1998; The biosynthesis of differentiation-inducing factor, a chlorinated signal molecule regulating Dictyostelium development. J Biol Chem273:2669–2675[CrossRef]
    [Google Scholar]
  28. Kay R. R., Gadian D. G., Williams S. R.. 1986; Intracellular pH in Dictyostelium : a 31P nuclear magnetic resonance study of its regulation and possible role in controlling cell differentiation. J Cell Sci83:165–179
    [Google Scholar]
  29. Keim M., Williams R. S., Harwood A. J.. 2004; An inverse PCR technique to rapidly isolate the flanking DNA of Dictyostelium insertion mutants. Mol Biotechnol26:221–224[CrossRef]
    [Google Scholar]
  30. Kessin R. H.. 2001; Dictyostelium Cambridge: Cambridge University Press;
    [Google Scholar]
  31. Ketcham R. B., Levitan D. R., Shenk M. A., Eisenberg R. M.. 1988; Do interactions of cellular slime mold species regulate their densities in soil?. Ecology69:193–199[CrossRef]
    [Google Scholar]
  32. Kooperberg C., Fazzio T. G., Delrow J. J., Tsukiyama T.. 2002; Improved background correction for spotted DNA microarrays. J Comput Biol9:55–66[CrossRef]
    [Google Scholar]
  33. Kosta A., Roisin-Bouffay C., Luciani M. F., Otto G. P., Kessin R. H., Golstein P.. 2004; Autophagy gene disruption reveals a non-vacuolar cell death pathway in Dictyostelium . J Biol Chem279:48404–48409[CrossRef]
    [Google Scholar]
  34. Kuspa A., Loomis W. F.. 1992; Tagging developmental genes in Dictyostelium by restriction enzyme-mediated integration of plasmid DNA. Proc Natl Acad Sci U S A89:8803–8807[CrossRef]
    [Google Scholar]
  35. Lupetti A., Danesi R., Campa M., Del Tacca M., Kelly S.. 2002; Molecular basis of resistance to azole antifungals. Trends Mol Med8:76–81[CrossRef]
    [Google Scholar]
  36. 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 discoideum and its analogues. Biochem J256:23–28
    [Google Scholar]
  37. Mizukami Y., Iwabuchi M.. 1970; Effects of actinomycin D and cycloheximide on the morphogenesis and synthesis of RNA and protein in the cellular slime mold, Dictyostelium discoideum . Exp Cell Res63:317–324[CrossRef]
    [Google Scholar]
  38. 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 discoideum . Nature328:811–814[CrossRef]
    [Google Scholar]
  39. Nellen W., Silan C., Firtel R. A.. 1984; DNA-mediated transformation in Dictyostelium discoideum : regulated expression of an actin gene fusion. Mol Cell Biol4:2890–2898
    [Google Scholar]
  40. Pang K. M., Lee E., Knecht D. A.. 1998; Use of a fusion protein between GFP and an actin-binding domain to visualize transient filamentous-actin structures. Curr Biol8:405–408[CrossRef]
    [Google Scholar]
  41. Patterson B., Spudich J. A.. 1995; A novel positive selection for identifying cold-sensitive myosin II mutants in Dictyostelium . Genetics140:505–515
    [Google Scholar]
  42. Pogge-von Strandmann R., Kay R. R., Dufour J.-P.. 1984; An electrogenic proton pump in plasma membranes from the cellular slime mould Dictyostelium discoideum . FEBS Lett175:422–427[CrossRef]
    [Google Scholar]
  43. Raper K. B.. 1984; The Dictyostelids Princeton, NJ: Princeton University Press;
    [Google Scholar]
  44. Schuster F. L., Visvesvara G. S.. 2004; Free-living amoebae as opportunistic and non-opportunistic pathogens of humans and animals. Int J Parasitol34:1001–1027[CrossRef]
    [Google Scholar]
  45. Serafimidis I., Kay R. R.. 2005; New prestalk and prespore inducing signals in Dictyostelium . Dev Biol282:432–441[CrossRef]
    [Google Scholar]
  46. Shaulsky G., Loomis W. F.. 1995; Mitochondrial DNA replication but no nuclear DNA replication during development of Dictyostelium . Proc Natl Acad Sci U S A92:5660–5663[CrossRef]
    [Google Scholar]
  47. Smyth G. K.. 2004; Linear models and empirical Bayes methods for assessing differential expression in microarray experiments.Stat Appl Genet Mol Biol 3, Article 3.
  48. Smyth G. K.. 2005; Limma: linear models for microarray data. In Bioinformatics and Computational Biology Solutions using R and Bioconductor Edited by Gentleman V. C. R., Dudoit S., Irizarry R., Huber W.. New York: Springer;
    [Google Scholar]
  49. Thompson C. R., Fu Q., Buhay C., Kay R. R., Shaulsky G.. 2004; A bZIP/bRLZ transcription factor required for DIF signaling in Dictyostelium . Development131:513–523[CrossRef]
    [Google Scholar]
  50. Wallace M. A., Raper K. B.. 1979; Genetic exchanges in the macrocysts of Dictyostelium discoideum . J Gen Microbiol113:327–337[CrossRef]
    [Google Scholar]
  51. Wang M., Roelfsema J. H., Williams J. G., Schaap P.. 1990; Cytoplasmic acidification facilitates but does not mediate DIF-induced prestalk gene expression in Dictyostelium discoideum . Dev Biol140:182–188[CrossRef]
    [Google Scholar]
  52. Watts D. J., Ashworth J. M.. 1970; Growth of myxamoebae of the cellular slime mould Dictyostelium discoideum in axenic culture. Biochem J119:171–174
    [Google Scholar]
  53. Welker D. L., Williams K. L.. 1980; Mitotic arrest and chromosome doubling using thiabendazole, cambendazole, nocodazole, and benlate in the slime mould Dictyostelium discoideum . J Gen Microbiol116:397–407
    [Google Scholar]
  54. Wurster B., Kay R. R.. 1990; New roles for DIF? Effects on early development in Dictyostelium . Dev Biol140:189–195[CrossRef]
    [Google Scholar]
  55. Zischka H., Oehme F., Pintsch T., Ott A., Keller H., Kellermann J., Schuster S. C.. 1999; Rearrangement of cortex proteins constitutes an osmoprotective mechanism in Dictyostelium . EMBO J18:4241–4249[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2006/000562-0
Loading
/content/journal/micro/10.1099/mic.0.2006/000562-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error