Transmission of trained immunity and heterologous resistance to infections across generations
Intergenerational inheritance of immune traits linked to epigenetic modifications has been demonstrated in plants and invertebrates. Here we provide evidence for transmission of trained immunity across generations to murine progeny that survived a sublethal systemic infection with Candida albicans o...
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| Veröffentlicht in: | Nature immunology 2021-11, Vol.22 (11), p.1382-1390 |
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| creator | Katzmarski, Natalie Domínguez-Andrés, Jorge Cirovic, Branko Renieris, Georgios Ciarlo, Eleonora Le Roy, Didier Lepikhov, Konstantin Kattler, Kathrin Gasparoni, Gilles Händler, Kristian Theis, Heidi Beyer, Marc van der Meer, Jos W. M. Joosten, Leo A. B. Walter, Jörn Schultze, Joachim L. Roger, Thierry Giamarellos-Bourboulis, Evangelos J. Schlitzer, Andreas Netea, Mihai G. |
| description | Intergenerational inheritance of immune traits linked to epigenetic modifications has been demonstrated in plants and invertebrates. Here we provide evidence for transmission of trained immunity across generations to murine progeny that survived a sublethal systemic infection with
Candida albicans
or a zymosan challenge. The progeny of trained mice exhibited cellular, developmental, transcriptional and epigenetic changes associated with the bone marrow-resident myeloid effector and progenitor cell compartment. Moreover, the progeny of trained mice showed enhanced responsiveness to endotoxin challenge, alongside improved protection against systemic heterologous
Escherichia coli
and
Listeria monocytogenes
infections. Sperm DNA of parental male mice intravenously infected with the fungus
C. albicans
showed DNA methylation differences linked to immune gene loci. These results provide evidence for inheritance of trained immunity in mammals, enhancing protection against infections.
Transgenerational transmission of acquired immunological traits has been demonstrated in invertebrates and plants but not mammals. Katzmarski et al. demonstrate that trained immunity that protects against heterologous infections can be transmitted to F2 offspring. |
| doi_str_mv | 10.1038/s41590-021-01052-7 |
| format | Article |
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Candida albicans
or a zymosan challenge. The progeny of trained mice exhibited cellular, developmental, transcriptional and epigenetic changes associated with the bone marrow-resident myeloid effector and progenitor cell compartment. Moreover, the progeny of trained mice showed enhanced responsiveness to endotoxin challenge, alongside improved protection against systemic heterologous
Escherichia coli
and
Listeria monocytogenes
infections. Sperm DNA of parental male mice intravenously infected with the fungus
C. albicans
showed DNA methylation differences linked to immune gene loci. These results provide evidence for inheritance of trained immunity in mammals, enhancing protection against infections.
Transgenerational transmission of acquired immunological traits has been demonstrated in invertebrates and plants but not mammals. Katzmarski et al. demonstrate that trained immunity that protects against heterologous infections can be transmitted to F2 offspring.</description><identifier>ISSN: 1529-2908</identifier><identifier>EISSN: 1529-2916</identifier><identifier>DOI: 10.1038/s41590-021-01052-7</identifier><identifier>PMID: 34663978</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>631/250 ; 631/326 ; 631/337 ; Animals ; Biomedical and Life Sciences ; Biomedicine ; Bone marrow ; Candida albicans ; Candida albicans - immunology ; Candida albicans - pathogenicity ; Candidiasis - genetics ; Candidiasis - immunology ; Candidiasis - metabolism ; Candidiasis - microbiology ; Cells, Cultured ; Deoxyribonucleic acid ; Disease Models, Animal ; Disseminated infection ; DNA ; DNA Methylation ; E coli ; Endotoxins ; Epigenesis, Genetic ; Epigenetic inheritance ; Epigenetics ; Escherichia coli ; Escherichia coli - immunology ; Escherichia coli - pathogenicity ; Escherichia coli Infections - genetics ; Escherichia coli Infections - immunology ; Escherichia coli Infections - metabolism ; Escherichia coli Infections - microbiology ; Genetic aspects ; Health aspects ; Heredity ; Host-Pathogen Interactions ; Immunity ; Immunity, Innate - genetics ; Immunological research ; Immunology ; Infections ; Infectious Diseases ; Intergenerational transmission ; Invertebrates ; Listeria monocytogenes ; Listeria monocytogenes - immunology ; Listeria monocytogenes - pathogenicity ; Listeriosis - genetics ; Listeriosis - immunology ; Listeriosis - metabolism ; Listeriosis - microbiology ; Male ; Mammals ; Mice, Transgenic ; Myeloid Cells - immunology ; Myeloid Cells - metabolism ; Myeloid Cells - microbiology ; Offspring ; Physiological aspects ; Progenitor cells ; Spermatozoa - immunology ; Spermatozoa - metabolism ; Stem cells ; Transcription ; Transcription, Genetic</subject><ispartof>Nature immunology, 2021-11, Vol.22 (11), p.1382-1390</ispartof><rights>The Author(s), under exclusive licence to Springer Nature America, Inc. 2021. corrected publication 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2021. The Author(s), under exclusive licence to Springer Nature America, Inc.</rights><rights>COPYRIGHT 2021 Nature Publishing Group</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c520t-553ddd5fca9fefdaa8dda20648411aceaa1240bc64198ebb9f1b53aa13bdf4573</citedby><cites>FETCH-LOGICAL-c520t-553ddd5fca9fefdaa8dda20648411aceaa1240bc64198ebb9f1b53aa13bdf4573</cites><orcidid>0000-0001-5488-6650 ; 0000-0003-0563-7417 ; 0000-0001-6166-9830 ; 0000-0002-0754-0099 ; 0000-0001-6339-2521 ; 0000-0002-9358-0109 ; 0000-0002-9091-1961 ; 0000-0003-4713-3911 ; 0000-0003-2421-6052 ; 0000-0002-2985-0901</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34663978$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Katzmarski, Natalie</creatorcontrib><creatorcontrib>Domínguez-Andrés, Jorge</creatorcontrib><creatorcontrib>Cirovic, Branko</creatorcontrib><creatorcontrib>Renieris, Georgios</creatorcontrib><creatorcontrib>Ciarlo, Eleonora</creatorcontrib><creatorcontrib>Le Roy, Didier</creatorcontrib><creatorcontrib>Lepikhov, Konstantin</creatorcontrib><creatorcontrib>Kattler, Kathrin</creatorcontrib><creatorcontrib>Gasparoni, Gilles</creatorcontrib><creatorcontrib>Händler, Kristian</creatorcontrib><creatorcontrib>Theis, Heidi</creatorcontrib><creatorcontrib>Beyer, Marc</creatorcontrib><creatorcontrib>van der Meer, Jos W. M.</creatorcontrib><creatorcontrib>Joosten, Leo A. B.</creatorcontrib><creatorcontrib>Walter, Jörn</creatorcontrib><creatorcontrib>Schultze, Joachim L.</creatorcontrib><creatorcontrib>Roger, Thierry</creatorcontrib><creatorcontrib>Giamarellos-Bourboulis, Evangelos J.</creatorcontrib><creatorcontrib>Schlitzer, Andreas</creatorcontrib><creatorcontrib>Netea, Mihai G.</creatorcontrib><title>Transmission of trained immunity and heterologous resistance to infections across generations</title><title>Nature immunology</title><addtitle>Nat Immunol</addtitle><addtitle>Nat Immunol</addtitle><description>Intergenerational inheritance of immune traits linked to epigenetic modifications has been demonstrated in plants and invertebrates. Here we provide evidence for transmission of trained immunity across generations to murine progeny that survived a sublethal systemic infection with
Candida albicans
or a zymosan challenge. The progeny of trained mice exhibited cellular, developmental, transcriptional and epigenetic changes associated with the bone marrow-resident myeloid effector and progenitor cell compartment. Moreover, the progeny of trained mice showed enhanced responsiveness to endotoxin challenge, alongside improved protection against systemic heterologous
Escherichia coli
and
Listeria monocytogenes
infections. Sperm DNA of parental male mice intravenously infected with the fungus
C. albicans
showed DNA methylation differences linked to immune gene loci. These results provide evidence for inheritance of trained immunity in mammals, enhancing protection against infections.
Transgenerational transmission of acquired immunological traits has been demonstrated in invertebrates and plants but not mammals. 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M. ; Joosten, Leo A. 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M.</au><au>Joosten, Leo A. B.</au><au>Walter, Jörn</au><au>Schultze, Joachim L.</au><au>Roger, Thierry</au><au>Giamarellos-Bourboulis, Evangelos J.</au><au>Schlitzer, Andreas</au><au>Netea, Mihai G.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Transmission of trained immunity and heterologous resistance to infections across generations</atitle><jtitle>Nature immunology</jtitle><stitle>Nat Immunol</stitle><addtitle>Nat Immunol</addtitle><date>2021-11-01</date><risdate>2021</risdate><volume>22</volume><issue>11</issue><spage>1382</spage><epage>1390</epage><pages>1382-1390</pages><issn>1529-2908</issn><eissn>1529-2916</eissn><abstract>Intergenerational inheritance of immune traits linked to epigenetic modifications has been demonstrated in plants and invertebrates. Here we provide evidence for transmission of trained immunity across generations to murine progeny that survived a sublethal systemic infection with
Candida albicans
or a zymosan challenge. The progeny of trained mice exhibited cellular, developmental, transcriptional and epigenetic changes associated with the bone marrow-resident myeloid effector and progenitor cell compartment. Moreover, the progeny of trained mice showed enhanced responsiveness to endotoxin challenge, alongside improved protection against systemic heterologous
Escherichia coli
and
Listeria monocytogenes
infections. Sperm DNA of parental male mice intravenously infected with the fungus
C. albicans
showed DNA methylation differences linked to immune gene loci. These results provide evidence for inheritance of trained immunity in mammals, enhancing protection against infections.
Transgenerational transmission of acquired immunological traits has been demonstrated in invertebrates and plants but not mammals. Katzmarski et al. demonstrate that trained immunity that protects against heterologous infections can be transmitted to F2 offspring.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>34663978</pmid><doi>10.1038/s41590-021-01052-7</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0001-5488-6650</orcidid><orcidid>https://orcid.org/0000-0003-0563-7417</orcidid><orcidid>https://orcid.org/0000-0001-6166-9830</orcidid><orcidid>https://orcid.org/0000-0002-0754-0099</orcidid><orcidid>https://orcid.org/0000-0001-6339-2521</orcidid><orcidid>https://orcid.org/0000-0002-9358-0109</orcidid><orcidid>https://orcid.org/0000-0002-9091-1961</orcidid><orcidid>https://orcid.org/0000-0003-4713-3911</orcidid><orcidid>https://orcid.org/0000-0003-2421-6052</orcidid><orcidid>https://orcid.org/0000-0002-2985-0901</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1529-2908 |
| ispartof | Nature immunology, 2021-11, Vol.22 (11), p.1382-1390 |
| issn | 1529-2908 1529-2916 |
| language | eng |
| recordid | cdi_proquest_miscellaneous_2583444730 |
| source | MEDLINE; Nature; Alma/SFX Local Collection |
| subjects | 631/250 631/326 631/337 Animals Biomedical and Life Sciences Biomedicine Bone marrow Candida albicans Candida albicans - immunology Candida albicans - pathogenicity Candidiasis - genetics Candidiasis - immunology Candidiasis - metabolism Candidiasis - microbiology Cells, Cultured Deoxyribonucleic acid Disease Models, Animal Disseminated infection DNA DNA Methylation E coli Endotoxins Epigenesis, Genetic Epigenetic inheritance Epigenetics Escherichia coli Escherichia coli - immunology Escherichia coli - pathogenicity Escherichia coli Infections - genetics Escherichia coli Infections - immunology Escherichia coli Infections - metabolism Escherichia coli Infections - microbiology Genetic aspects Health aspects Heredity Host-Pathogen Interactions Immunity Immunity, Innate - genetics Immunological research Immunology Infections Infectious Diseases Intergenerational transmission Invertebrates Listeria monocytogenes Listeria monocytogenes - immunology Listeria monocytogenes - pathogenicity Listeriosis - genetics Listeriosis - immunology Listeriosis - metabolism Listeriosis - microbiology Male Mammals Mice, Transgenic Myeloid Cells - immunology Myeloid Cells - metabolism Myeloid Cells - microbiology Offspring Physiological aspects Progenitor cells Spermatozoa - immunology Spermatozoa - metabolism Stem cells Transcription Transcription, Genetic |
| title | Transmission of trained immunity and heterologous resistance to infections across generations |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-23T10%3A33%3A23IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_proqu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Transmission%20of%20trained%20immunity%20and%20heterologous%20resistance%20to%20infections%20across%20generations&rft.jtitle=Nature%20immunology&rft.au=Katzmarski,%20Natalie&rft.date=2021-11-01&rft.volume=22&rft.issue=11&rft.spage=1382&rft.epage=1390&rft.pages=1382-1390&rft.issn=1529-2908&rft.eissn=1529-2916&rft_id=info:doi/10.1038/s41590-021-01052-7&rft_dat=%3Cgale_proqu%3EA680626109%3C/gale_proqu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2587482913&rft_id=info:pmid/34663978&rft_galeid=A680626109&rfr_iscdi=true |