Antimicrobial histones and DNA traps in invertebrate immunity: evidences in Crassostrea gigas.

Although antimicrobial histones have been isolated from multiple metazoan species, their role in host defense has long remained unanswered. We found here that the hemocytes of the oyster Crassostrea gigas release antimicrobial H1-like and H5-like histones in response to tissue damage and infection....

Full description

Bibliographic Details
Published in:Journal of Biological Chemistry
Main Authors: Poirier, Aurore C., Schmitt, Paulina, Rosa, Rafael D., Vanhove, Audrey S., Kieffer-jaquinod, Sylvie, Rubio, Tristan P., Charriere, Guillaume M., Destoumieux-garzon, Delphine
Format: Article in Journal/Newspaper
Language:English
Published: Amer Soc Biochemistry Molecular Biology Inc 2014
Subjects:
DNA
NET
Online Access:https://archimer.ifremer.fr/doc/00217/32866/31784.pdf
https://doi.org/10.1074/jbc.M114.576546
https://archimer.ifremer.fr/doc/00217/32866/
id ftarchimer:oai:archimer.ifremer.fr:32866
record_format openpolar
spelling ftarchimer:oai:archimer.ifremer.fr:32866 2023-05-15T15:58:01+02:00 Antimicrobial histones and DNA traps in invertebrate immunity: evidences in Crassostrea gigas. Poirier, Aurore C. Schmitt, Paulina Rosa, Rafael D. Vanhove, Audrey S. Kieffer-jaquinod, Sylvie Rubio, Tristan P. Charriere, Guillaume M. Destoumieux-garzon, Delphine 2014-09-05 application/pdf https://archimer.ifremer.fr/doc/00217/32866/31784.pdf https://doi.org/10.1074/jbc.M114.576546 https://archimer.ifremer.fr/doc/00217/32866/ eng eng Amer Soc Biochemistry Molecular Biology Inc https://archimer.ifremer.fr/doc/00217/32866/31784.pdf doi:10.1074/jbc.M114.576546 https://archimer.ifremer.fr/doc/00217/32866/ 2014 by The American Society for Biochemistry and Molecular Biology, Inc. info:eu-repo/semantics/openAccess restricted use Journal Of Biological Chemistry (0021-9258) (Amer Soc Biochemistry Molecular Biology Inc), 2014-09-05 , Vol. 289 , N. 36 , P. 24821-24831 Antimicrobial Peptide (AMP) DNA Innate Immunity Invertebrate Reactive Oxygen Species (ROS) NET Mollusk text Publication info:eu-repo/semantics/article 2014 ftarchimer https://doi.org/10.1074/jbc.M114.576546 2021-09-23T20:25:01Z Although antimicrobial histones have been isolated from multiple metazoan species, their role in host defense has long remained unanswered. We found here that the hemocytes of the oyster Crassostrea gigas release antimicrobial H1-like and H5-like histones in response to tissue damage and infection. These antimicrobial histones were shown to be associated with extracellular DNA networks released by hemocytes, the circulating immune cells of invertebrates, in response to immune challenge. The hemocyte-released DNA was found to surround and entangle vibrios. This defense mechanism is reminiscent of the neutrophil extracellular traps (ETs) recently described in vertebrates. Importantly, oyster ETs were evidenced in vivo in hemocyte-infiltrated interstitial tissues surrounding wounds, whereas they were absent from tissues of unchallenged oysters. Consistently, antimicrobial histones were found to accumulate in oyster tissues following injury or infection with vibrios. Finally, oyster ET formation was highly dependent on the production of reactive oxygen species by hemocytes. This shows that ET formation relies on common cellular and molecular mechanisms from vertebrates to invertebrates. Altogether, our data reveal that ET formation is a defense mechanism triggered by infection and tissue damage, which is shared by relatively distant species suggesting either evolutionary conservation or convergent evolution within Bilateria. Article in Journal/Newspaper Crassostrea gigas Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer) Journal of Biological Chemistry 289 36 24821 24831
institution Open Polar
collection Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer)
op_collection_id ftarchimer
language English
topic Antimicrobial Peptide (AMP)
DNA
Innate Immunity
Invertebrate
Reactive Oxygen Species (ROS)
NET
Mollusk
spellingShingle Antimicrobial Peptide (AMP)
DNA
Innate Immunity
Invertebrate
Reactive Oxygen Species (ROS)
NET
Mollusk
Poirier, Aurore C.
Schmitt, Paulina
Rosa, Rafael D.
Vanhove, Audrey S.
Kieffer-jaquinod, Sylvie
Rubio, Tristan P.
Charriere, Guillaume M.
Destoumieux-garzon, Delphine
Antimicrobial histones and DNA traps in invertebrate immunity: evidences in Crassostrea gigas.
topic_facet Antimicrobial Peptide (AMP)
DNA
Innate Immunity
Invertebrate
Reactive Oxygen Species (ROS)
NET
Mollusk
description Although antimicrobial histones have been isolated from multiple metazoan species, their role in host defense has long remained unanswered. We found here that the hemocytes of the oyster Crassostrea gigas release antimicrobial H1-like and H5-like histones in response to tissue damage and infection. These antimicrobial histones were shown to be associated with extracellular DNA networks released by hemocytes, the circulating immune cells of invertebrates, in response to immune challenge. The hemocyte-released DNA was found to surround and entangle vibrios. This defense mechanism is reminiscent of the neutrophil extracellular traps (ETs) recently described in vertebrates. Importantly, oyster ETs were evidenced in vivo in hemocyte-infiltrated interstitial tissues surrounding wounds, whereas they were absent from tissues of unchallenged oysters. Consistently, antimicrobial histones were found to accumulate in oyster tissues following injury or infection with vibrios. Finally, oyster ET formation was highly dependent on the production of reactive oxygen species by hemocytes. This shows that ET formation relies on common cellular and molecular mechanisms from vertebrates to invertebrates. Altogether, our data reveal that ET formation is a defense mechanism triggered by infection and tissue damage, which is shared by relatively distant species suggesting either evolutionary conservation or convergent evolution within Bilateria.
format Article in Journal/Newspaper
author Poirier, Aurore C.
Schmitt, Paulina
Rosa, Rafael D.
Vanhove, Audrey S.
Kieffer-jaquinod, Sylvie
Rubio, Tristan P.
Charriere, Guillaume M.
Destoumieux-garzon, Delphine
author_facet Poirier, Aurore C.
Schmitt, Paulina
Rosa, Rafael D.
Vanhove, Audrey S.
Kieffer-jaquinod, Sylvie
Rubio, Tristan P.
Charriere, Guillaume M.
Destoumieux-garzon, Delphine
author_sort Poirier, Aurore C.
title Antimicrobial histones and DNA traps in invertebrate immunity: evidences in Crassostrea gigas.
title_short Antimicrobial histones and DNA traps in invertebrate immunity: evidences in Crassostrea gigas.
title_full Antimicrobial histones and DNA traps in invertebrate immunity: evidences in Crassostrea gigas.
title_fullStr Antimicrobial histones and DNA traps in invertebrate immunity: evidences in Crassostrea gigas.
title_full_unstemmed Antimicrobial histones and DNA traps in invertebrate immunity: evidences in Crassostrea gigas.
title_sort antimicrobial histones and dna traps in invertebrate immunity: evidences in crassostrea gigas.
publisher Amer Soc Biochemistry Molecular Biology Inc
publishDate 2014
url https://archimer.ifremer.fr/doc/00217/32866/31784.pdf
https://doi.org/10.1074/jbc.M114.576546
https://archimer.ifremer.fr/doc/00217/32866/
genre Crassostrea gigas
genre_facet Crassostrea gigas
op_source Journal Of Biological Chemistry (0021-9258) (Amer Soc Biochemistry Molecular Biology Inc), 2014-09-05 , Vol. 289 , N. 36 , P. 24821-24831
op_relation https://archimer.ifremer.fr/doc/00217/32866/31784.pdf
doi:10.1074/jbc.M114.576546
https://archimer.ifremer.fr/doc/00217/32866/
op_rights 2014 by The American Society for Biochemistry and Molecular Biology, Inc.
info:eu-repo/semantics/openAccess
restricted use
op_doi https://doi.org/10.1074/jbc.M114.576546
container_title Journal of Biological Chemistry
container_volume 289
container_issue 36
container_start_page 24821
op_container_end_page 24831
_version_ 1766393741596164096