Immune-like Phagocyte Activity in the Social Amoeba

Social amoebae feed on bacteria in the soil but aggregate when starved to form a migrating slug. We describe a previously unknown cell type in the social amoeba, which appears to provide detoxification and immune-like functions and which we term sentinel (S) cells. S cells were observed to engulf bacteria and sequester toxins while circulating within the slug, eventually being sloughed off. A Toll/interleukin-1 receptor (TIR) domain protein, TirA, was also required for some S cell functions and for vegetative amoebae to feed on live bacteria. This apparent innate immune function in social amoebae, and the use of TirA for bacterial feeding, suggest an ancient cellular foraging mechanism that may have been adapted to defense functions well before the diversification of the animals.

[1]  W. Loomis,et al.  Changing Patterns of Gene Expression in Dictyostelium Prestalk Cell Subtypes Recognized by In Situ Hybridization with Genes from Microarray Analyses , 2003, Eukaryotic Cell.

[2]  C. Anjard,et al.  Evolutionary Analyses of ABC Transporters of Dictyostelium discoideum , 2002, Eukaryotic Cell.

[3]  E. Casademunt,et al.  A gene encoding a novel anti-adhesive protein is expressed in growing cells and restricted to anterior-like cells during development of Dictyostelium. , 2002, Differentiation; research in biological diversity.

[4]  H. Shuman,et al.  Intracellular multiplication of Legionella pneumophila: human pathogen or accidental tourist? , 1998, Current topics in microbiology and immunology.

[5]  David L. Steffen,et al.  The genome of the social amoeba Dictyostelium discoideum , 2005, Nature.

[6]  Jeffrey G. Williams.  Transcriptional regulation of Dictyostelium pattern formation , 2006, EMBO reports.

[7]  Rolf Olsen,et al.  Comparing the Dictyostelium and Entamoeba Genomes Reveals an Ancient Split in the Conosa Lineage , 2005, PLoS Comput. Biol..

[8]  S. Dower,et al.  Identification of Two Major Sites in the Type I Interleukin-1 Receptor Cytoplasmic Region Responsible for Coupling to Pro-inflammatory Signaling Pathways* , 2000, The Journal of Biological Chemistry.

[9]  P. Ronald,et al.  Unique characteristics of Xanthomonas oryzae pv. oryzae AvrXa21 and implications for plant innate immunity , 2006, Proceedings of the National Academy of Sciences.

[10]  S. Fields,et al.  Binding specificity of Toll‐like receptor cytoplasmic domains , 2006, European journal of immunology.

[11]  F. Ausubel.  Are innate immune signaling pathways in plants and animals conserved? , 2005, Nature Immunology.

[12]  C. N. David,et al.  Cell Sorting daring Pattern Formation in Dictyostelium , 1981 .

[13]  O. Anderson,et al.  Legionella Effectors That Promote Nonlytic Release from Protozoa , 2004, Science.

[14]  Thomas Eulgem,et al.  Regulation of the Arabidopsis defense transcriptome. , 2005, Trends in plant science.

[15]  S. Akira,et al.  Pathogen Recognition and Innate Immunity , 2006, Cell.

[16]  J. Cardelli,et al.  Intracellular Growth of Legionella pneumophila in Dictyostelium discoideum, a System for Genetic Analysis of Host-Pathogen Interactions , 2000, Infection and Immunity.

[17]  E. A. van der Biezen,et al.  The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. , 1997, The Plant cell.

[18]  A. Tauber.  Metchnikoff and the phagocytosis theory , 2003, Nature Reviews Molecular Cell Biology.

[19]  W. Doolittle,et al.  Origin and evolution of the slime molds (Mycetozoa) , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[20]  R. Germain.  An innately interesting decade of research in immunology , 2004, Nature Medicine.

[21]  C. Janeway,et al.  An ancient system of host defense. , 1998, Current opinion in immunology.

[22]  S. Dinesh-Kumar,et al.  Correction: A Novel Role for the TIR Domain in Association with Pathogen-Derived Elicitors , 2016, PLoS biology.

[23]  I. Somssich,et al.  Nuclear Activity of MLA Immune Receptors Links Isolate-Specific and Basal Disease-Resistance Responses , 2007, Science.

[24]  L. Tong,et al.  Structural basis for signal transduction by the Toll/interleukin-1 receptor domains , 2000, Nature.

[25]  L. Piater,et al.  Innate immunity in plants and animals: striking similarities and obvious differences , 2004, Immunological reviews.

[26]  A. Kuspa,et al.  Evidence that a cell-type-specific efflux pump regulates cell differentiation in Dictyostelium. , 2000, Developmental biology.

[27]  M. Horwitz.  The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes , 1983, The Journal of experimental medicine.

[28]  Terry Gaasterland,et al.  The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[29]  R. Kessin.  Dictyostelium: Evolution, Cell Biology, and the Development of Multicellularity , 2001 .

[30]  C. Janeway,et al.  Innate immune recognition. , 2002, Annual review of immunology.

[31]  Thomas Winckler,et al.  Molecular Phylogeny and Evolution of Morphology in the Social Amoebas , 2006, Science.