Molecular characterization of the evolution of phagosomes

Abstract Amoeba use phagocytosis to internalize bacteria as a source of nutrients, whereas multicellular organisms utilize this process as a defense mechanism to kill microbes and, in vertebrates, initiate a sustained immune response. By using a large‐scale approach to identify and compare the prote...

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Main Authors: Jonathan Boulais, Matthias Trost, Christian R Landry, Régis Dieckmann, Emmanuel D Levy, Thierry Soldati, Stephen W Michnick, Pierre Thibault, Michel Desjardins
Format: Article
Language:English
Published: Springer Nature 2010-10-01
Series:Molecular Systems Biology
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Online Access:https://doi.org/10.1038/msb.2010.80
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author Jonathan Boulais
Matthias Trost
Christian R Landry
Régis Dieckmann
Emmanuel D Levy
Thierry Soldati
Stephen W Michnick
Pierre Thibault
Michel Desjardins
author_facet Jonathan Boulais
Matthias Trost
Christian R Landry
Régis Dieckmann
Emmanuel D Levy
Thierry Soldati
Stephen W Michnick
Pierre Thibault
Michel Desjardins
author_sort Jonathan Boulais
collection DOAJ
description Abstract Amoeba use phagocytosis to internalize bacteria as a source of nutrients, whereas multicellular organisms utilize this process as a defense mechanism to kill microbes and, in vertebrates, initiate a sustained immune response. By using a large‐scale approach to identify and compare the proteome and phosphoproteome of phagosomes isolated from distant organisms, and by comparative analysis over 39 taxa, we identified an ‘ancient’ core of phagosomal proteins around which the immune functions of this organelle have likely organized. Our data indicate that a larger proportion of the phagosome proteome, compared with the whole cell proteome, has been acquired through gene duplication at a period coinciding with the emergence of innate and adaptive immunity. Our study also characterizes in detail the acquisition of novel proteins and the significant remodeling of the phagosome phosphoproteome that contributed to modify the core constituents of this organelle in evolution. Our work thus provides the first thorough analysis of the changes that enabled the transformation of the phagosome from a phagotrophic compartment into an organelle fully competent for antigen presentation.
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publisher Springer Nature
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series Molecular Systems Biology
spelling doaj-art-dedc093817f64871a4e156e6ef64cae32025-08-24T11:59:59ZengSpringer NatureMolecular Systems Biology1744-42922010-10-016111410.1038/msb.2010.80Molecular characterization of the evolution of phagosomesJonathan Boulais0Matthias Trost1Christian R Landry2Régis Dieckmann3Emmanuel D Levy4Thierry Soldati5Stephen W Michnick6Pierre Thibault7Michel Desjardins8Département de Pathologie et Biologie Cellulaire, Université de Montréal, MontréalMRC Protein Phosphorylation Unit, College of Life Sciences, University of DundeeDépartement de Biologie, PROTEO and Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, QuébecDepartment of Biochemistry, University of GenevaDépartement de Biochimie, Université de Montréal, MontréalDepartment of Biochemistry, University of GenevaDépartement de Biochimie, Université de Montréal, MontréalUnité protéomique et spectrométrie de masse bioanalytique, Institut de Recherche en Immunologie et Cancérologie (IRIC), Université de Montréal, MontréalDépartement de Pathologie et Biologie Cellulaire, Université de Montréal, MontréalAbstract Amoeba use phagocytosis to internalize bacteria as a source of nutrients, whereas multicellular organisms utilize this process as a defense mechanism to kill microbes and, in vertebrates, initiate a sustained immune response. By using a large‐scale approach to identify and compare the proteome and phosphoproteome of phagosomes isolated from distant organisms, and by comparative analysis over 39 taxa, we identified an ‘ancient’ core of phagosomal proteins around which the immune functions of this organelle have likely organized. Our data indicate that a larger proportion of the phagosome proteome, compared with the whole cell proteome, has been acquired through gene duplication at a period coinciding with the emergence of innate and adaptive immunity. Our study also characterizes in detail the acquisition of novel proteins and the significant remodeling of the phagosome phosphoproteome that contributed to modify the core constituents of this organelle in evolution. Our work thus provides the first thorough analysis of the changes that enabled the transformation of the phagosome from a phagotrophic compartment into an organelle fully competent for antigen presentation.https://doi.org/10.1038/msb.2010.80evolutionimmunityphosphoproteomicsphylogenyproteomics
spellingShingle Jonathan Boulais
Matthias Trost
Christian R Landry
Régis Dieckmann
Emmanuel D Levy
Thierry Soldati
Stephen W Michnick
Pierre Thibault
Michel Desjardins
Molecular characterization of the evolution of phagosomes
Molecular Systems Biology
evolution
immunity
phosphoproteomics
phylogeny
proteomics
title Molecular characterization of the evolution of phagosomes
title_full Molecular characterization of the evolution of phagosomes
title_fullStr Molecular characterization of the evolution of phagosomes
title_full_unstemmed Molecular characterization of the evolution of phagosomes
title_short Molecular characterization of the evolution of phagosomes
title_sort molecular characterization of the evolution of phagosomes
topic evolution
immunity
phosphoproteomics
phylogeny
proteomics
url https://doi.org/10.1038/msb.2010.80
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AT matthiastrost molecularcharacterizationoftheevolutionofphagosomes
AT christianrlandry molecularcharacterizationoftheevolutionofphagosomes
AT regisdieckmann molecularcharacterizationoftheevolutionofphagosomes
AT emmanueldlevy molecularcharacterizationoftheevolutionofphagosomes
AT thierrysoldati molecularcharacterizationoftheevolutionofphagosomes
AT stephenwmichnick molecularcharacterizationoftheevolutionofphagosomes
AT pierrethibault molecularcharacterizationoftheevolutionofphagosomes
AT micheldesjardins molecularcharacterizationoftheevolutionofphagosomes