ATP spreads inflammation to other limbs through crosstalk between sensory neurons and interneurons
Neural circuits between lesions are one mechanism through which local inflammation spreads to remote positions. Here, we show the inflammatory signal on one side of the joint is spread to the other side via sensory neuron-interneuron crosstalk, with ATP at the core. Surgical ablation or pharmacologi...
Gespeichert in:
Veröffentlicht in: | The Journal of experimental medicine 2022-06, Vol.219 (6) |
---|---|
Hauptverfasser: | , , , , , , , , , , , , , , , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | |
---|---|
container_issue | 6 |
container_start_page | |
container_title | The Journal of experimental medicine |
container_volume | 219 |
creator | Hasebe, Rie Murakami, Kaoru Harada, Masaya Halaka, Nada Nakagawa, Hiroshi Kawano, Fuminori Ohira, Yoshinobu Kawamoto, Tadafumi Yull, Fiona E Blackwell, Timothy S Nio-Kobayashi, Junko Iwanaga, Toshihiko Watanabe, Masahiko Watanabe, Nobuhiro Hotta, Harumi Yamashita, Toshihide Kamimura, Daisuke Tanaka, Yuki Murakami, Masaaki |
description | Neural circuits between lesions are one mechanism through which local inflammation spreads to remote positions. Here, we show the inflammatory signal on one side of the joint is spread to the other side via sensory neuron-interneuron crosstalk, with ATP at the core. Surgical ablation or pharmacological inhibition of this neural pathway prevented inflammation development on the other side. Mechanistic analysis showed that ATP serves as both a neurotransmitter and an inflammation enhancer, thus acting as an intermediary between the local inflammation and neural pathway that induces inflammation on the other side. These results suggest blockade of this neural pathway, which is named the remote inflammation gateway reflex, may have therapeutic value for inflammatory diseases, particularly those, such as rheumatoid arthritis, in which inflammation spreads to remote positions. |
doi_str_mv | 10.1084/jem.20212019 |
format | Article |
fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9117706</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2665562211</sourcerecordid><originalsourceid>FETCH-LOGICAL-c537t-ba73c3a59c5efc32d2c0fcd951d57f039ca0e4e97258994ce33b1053ccece8343</originalsourceid><addsrcrecordid>eNpVkU1LxDAQhoMouq7ePEuOHqxOkqbdXARZ_AJBD-s5pOnUrbbJmqSK_96qq-hpYOblmWEeQg4YnDCY5adP2J9w4IwDUxtkwmQOmZJitkkmAJxnDKDcIbsxPgGwPJfFNtkRUpaqUPmEVOeLexpXAU0daeuazvS9Sa13NHnq0xID7dq-ijQtgx8el9QGH2My3TOtML0hOhrRRR_eqcMheBepcfVIShjWjT2y1Zgu4v66TsnD5cVifp3d3l3dzM9vMytFmbLKlMIKI5WV2FjBa26hsbWSrJZlA0JZA5ijKrmcKZVbFKJiIIW1aHEmcjElZ9_c1VD1WFt0KZhOr0Lbm_CuvWn1_4lrl_rRv2rFWFlCMQKO1oDgXwaMSfdttNh1xqEfouZFIWXBOWNj9Pg7-vWOgM3vGgb6U4setegfLWP88O9pv-EfD-IDIMyMSQ</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2665562211</pqid></control><display><type>article</type><title>ATP spreads inflammation to other limbs through crosstalk between sensory neurons and interneurons</title><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><creator>Hasebe, Rie ; Murakami, Kaoru ; Harada, Masaya ; Halaka, Nada ; Nakagawa, Hiroshi ; Kawano, Fuminori ; Ohira, Yoshinobu ; Kawamoto, Tadafumi ; Yull, Fiona E ; Blackwell, Timothy S ; Nio-Kobayashi, Junko ; Iwanaga, Toshihiko ; Watanabe, Masahiko ; Watanabe, Nobuhiro ; Hotta, Harumi ; Yamashita, Toshihide ; Kamimura, Daisuke ; Tanaka, Yuki ; Murakami, Masaaki</creator><creatorcontrib>Hasebe, Rie ; Murakami, Kaoru ; Harada, Masaya ; Halaka, Nada ; Nakagawa, Hiroshi ; Kawano, Fuminori ; Ohira, Yoshinobu ; Kawamoto, Tadafumi ; Yull, Fiona E ; Blackwell, Timothy S ; Nio-Kobayashi, Junko ; Iwanaga, Toshihiko ; Watanabe, Masahiko ; Watanabe, Nobuhiro ; Hotta, Harumi ; Yamashita, Toshihide ; Kamimura, Daisuke ; Tanaka, Yuki ; Murakami, Masaaki</creatorcontrib><description>Neural circuits between lesions are one mechanism through which local inflammation spreads to remote positions. Here, we show the inflammatory signal on one side of the joint is spread to the other side via sensory neuron-interneuron crosstalk, with ATP at the core. Surgical ablation or pharmacological inhibition of this neural pathway prevented inflammation development on the other side. Mechanistic analysis showed that ATP serves as both a neurotransmitter and an inflammation enhancer, thus acting as an intermediary between the local inflammation and neural pathway that induces inflammation on the other side. These results suggest blockade of this neural pathway, which is named the remote inflammation gateway reflex, may have therapeutic value for inflammatory diseases, particularly those, such as rheumatoid arthritis, in which inflammation spreads to remote positions.</description><identifier>ISSN: 0022-1007</identifier><identifier>EISSN: 1540-9538</identifier><identifier>DOI: 10.1084/jem.20212019</identifier><identifier>PMID: 35579694</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Brief Definitive Report ; Innate Immunity and Inflammation ; Neuroscience</subject><ispartof>The Journal of experimental medicine, 2022-06, Vol.219 (6)</ispartof><rights>2022 Hasebe et al.</rights><rights>2022 Hasebe et al. 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c537t-ba73c3a59c5efc32d2c0fcd951d57f039ca0e4e97258994ce33b1053ccece8343</citedby><cites>FETCH-LOGICAL-c537t-ba73c3a59c5efc32d2c0fcd951d57f039ca0e4e97258994ce33b1053ccece8343</cites><orcidid>0000-0002-0337-7052 ; 0000-0003-2015-1503 ; 0000-0001-8741-1635 ; 0000-0002-1450-2381 ; 0000-0001-9822-9804 ; 0000-0002-4590-7162 ; 0000-0003-2009-0595 ; 0000-0002-3670-3416 ; 0000-0003-1636-7942 ; 0000-0003-4559-7018 ; 0000-0002-6830-8453 ; 0000-0002-8018-852X ; 0000-0002-1318-3542 ; 0000-0003-3019-2923 ; 0000-0002-3714-0360 ; 0000-0002-0269-8962 ; 0000-0003-1022-4430 ; 0000-0001-5037-7138 ; 0000-0001-7159-7279</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35579694$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hasebe, Rie</creatorcontrib><creatorcontrib>Murakami, Kaoru</creatorcontrib><creatorcontrib>Harada, Masaya</creatorcontrib><creatorcontrib>Halaka, Nada</creatorcontrib><creatorcontrib>Nakagawa, Hiroshi</creatorcontrib><creatorcontrib>Kawano, Fuminori</creatorcontrib><creatorcontrib>Ohira, Yoshinobu</creatorcontrib><creatorcontrib>Kawamoto, Tadafumi</creatorcontrib><creatorcontrib>Yull, Fiona E</creatorcontrib><creatorcontrib>Blackwell, Timothy S</creatorcontrib><creatorcontrib>Nio-Kobayashi, Junko</creatorcontrib><creatorcontrib>Iwanaga, Toshihiko</creatorcontrib><creatorcontrib>Watanabe, Masahiko</creatorcontrib><creatorcontrib>Watanabe, Nobuhiro</creatorcontrib><creatorcontrib>Hotta, Harumi</creatorcontrib><creatorcontrib>Yamashita, Toshihide</creatorcontrib><creatorcontrib>Kamimura, Daisuke</creatorcontrib><creatorcontrib>Tanaka, Yuki</creatorcontrib><creatorcontrib>Murakami, Masaaki</creatorcontrib><title>ATP spreads inflammation to other limbs through crosstalk between sensory neurons and interneurons</title><title>The Journal of experimental medicine</title><addtitle>J Exp Med</addtitle><description>Neural circuits between lesions are one mechanism through which local inflammation spreads to remote positions. Here, we show the inflammatory signal on one side of the joint is spread to the other side via sensory neuron-interneuron crosstalk, with ATP at the core. Surgical ablation or pharmacological inhibition of this neural pathway prevented inflammation development on the other side. Mechanistic analysis showed that ATP serves as both a neurotransmitter and an inflammation enhancer, thus acting as an intermediary between the local inflammation and neural pathway that induces inflammation on the other side. These results suggest blockade of this neural pathway, which is named the remote inflammation gateway reflex, may have therapeutic value for inflammatory diseases, particularly those, such as rheumatoid arthritis, in which inflammation spreads to remote positions.</description><subject>Brief Definitive Report</subject><subject>Innate Immunity and Inflammation</subject><subject>Neuroscience</subject><issn>0022-1007</issn><issn>1540-9538</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNpVkU1LxDAQhoMouq7ePEuOHqxOkqbdXARZ_AJBD-s5pOnUrbbJmqSK_96qq-hpYOblmWEeQg4YnDCY5adP2J9w4IwDUxtkwmQOmZJitkkmAJxnDKDcIbsxPgGwPJfFNtkRUpaqUPmEVOeLexpXAU0daeuazvS9Sa13NHnq0xID7dq-ijQtgx8el9QGH2My3TOtML0hOhrRRR_eqcMheBepcfVIShjWjT2y1Zgu4v66TsnD5cVifp3d3l3dzM9vMytFmbLKlMIKI5WV2FjBa26hsbWSrJZlA0JZA5ijKrmcKZVbFKJiIIW1aHEmcjElZ9_c1VD1WFt0KZhOr0Lbm_CuvWn1_4lrl_rRv2rFWFlCMQKO1oDgXwaMSfdttNh1xqEfouZFIWXBOWNj9Pg7-vWOgM3vGgb6U4setegfLWP88O9pv-EfD-IDIMyMSQ</recordid><startdate>20220606</startdate><enddate>20220606</enddate><creator>Hasebe, Rie</creator><creator>Murakami, Kaoru</creator><creator>Harada, Masaya</creator><creator>Halaka, Nada</creator><creator>Nakagawa, Hiroshi</creator><creator>Kawano, Fuminori</creator><creator>Ohira, Yoshinobu</creator><creator>Kawamoto, Tadafumi</creator><creator>Yull, Fiona E</creator><creator>Blackwell, Timothy S</creator><creator>Nio-Kobayashi, Junko</creator><creator>Iwanaga, Toshihiko</creator><creator>Watanabe, Masahiko</creator><creator>Watanabe, Nobuhiro</creator><creator>Hotta, Harumi</creator><creator>Yamashita, Toshihide</creator><creator>Kamimura, Daisuke</creator><creator>Tanaka, Yuki</creator><creator>Murakami, Masaaki</creator><general>Rockefeller University Press</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0337-7052</orcidid><orcidid>https://orcid.org/0000-0003-2015-1503</orcidid><orcidid>https://orcid.org/0000-0001-8741-1635</orcidid><orcidid>https://orcid.org/0000-0002-1450-2381</orcidid><orcidid>https://orcid.org/0000-0001-9822-9804</orcidid><orcidid>https://orcid.org/0000-0002-4590-7162</orcidid><orcidid>https://orcid.org/0000-0003-2009-0595</orcidid><orcidid>https://orcid.org/0000-0002-3670-3416</orcidid><orcidid>https://orcid.org/0000-0003-1636-7942</orcidid><orcidid>https://orcid.org/0000-0003-4559-7018</orcidid><orcidid>https://orcid.org/0000-0002-6830-8453</orcidid><orcidid>https://orcid.org/0000-0002-8018-852X</orcidid><orcidid>https://orcid.org/0000-0002-1318-3542</orcidid><orcidid>https://orcid.org/0000-0003-3019-2923</orcidid><orcidid>https://orcid.org/0000-0002-3714-0360</orcidid><orcidid>https://orcid.org/0000-0002-0269-8962</orcidid><orcidid>https://orcid.org/0000-0003-1022-4430</orcidid><orcidid>https://orcid.org/0000-0001-5037-7138</orcidid><orcidid>https://orcid.org/0000-0001-7159-7279</orcidid></search><sort><creationdate>20220606</creationdate><title>ATP spreads inflammation to other limbs through crosstalk between sensory neurons and interneurons</title><author>Hasebe, Rie ; Murakami, Kaoru ; Harada, Masaya ; Halaka, Nada ; Nakagawa, Hiroshi ; Kawano, Fuminori ; Ohira, Yoshinobu ; Kawamoto, Tadafumi ; Yull, Fiona E ; Blackwell, Timothy S ; Nio-Kobayashi, Junko ; Iwanaga, Toshihiko ; Watanabe, Masahiko ; Watanabe, Nobuhiro ; Hotta, Harumi ; Yamashita, Toshihide ; Kamimura, Daisuke ; Tanaka, Yuki ; Murakami, Masaaki</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c537t-ba73c3a59c5efc32d2c0fcd951d57f039ca0e4e97258994ce33b1053ccece8343</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Brief Definitive Report</topic><topic>Innate Immunity and Inflammation</topic><topic>Neuroscience</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hasebe, Rie</creatorcontrib><creatorcontrib>Murakami, Kaoru</creatorcontrib><creatorcontrib>Harada, Masaya</creatorcontrib><creatorcontrib>Halaka, Nada</creatorcontrib><creatorcontrib>Nakagawa, Hiroshi</creatorcontrib><creatorcontrib>Kawano, Fuminori</creatorcontrib><creatorcontrib>Ohira, Yoshinobu</creatorcontrib><creatorcontrib>Kawamoto, Tadafumi</creatorcontrib><creatorcontrib>Yull, Fiona E</creatorcontrib><creatorcontrib>Blackwell, Timothy S</creatorcontrib><creatorcontrib>Nio-Kobayashi, Junko</creatorcontrib><creatorcontrib>Iwanaga, Toshihiko</creatorcontrib><creatorcontrib>Watanabe, Masahiko</creatorcontrib><creatorcontrib>Watanabe, Nobuhiro</creatorcontrib><creatorcontrib>Hotta, Harumi</creatorcontrib><creatorcontrib>Yamashita, Toshihide</creatorcontrib><creatorcontrib>Kamimura, Daisuke</creatorcontrib><creatorcontrib>Tanaka, Yuki</creatorcontrib><creatorcontrib>Murakami, Masaaki</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of experimental medicine</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hasebe, Rie</au><au>Murakami, Kaoru</au><au>Harada, Masaya</au><au>Halaka, Nada</au><au>Nakagawa, Hiroshi</au><au>Kawano, Fuminori</au><au>Ohira, Yoshinobu</au><au>Kawamoto, Tadafumi</au><au>Yull, Fiona E</au><au>Blackwell, Timothy S</au><au>Nio-Kobayashi, Junko</au><au>Iwanaga, Toshihiko</au><au>Watanabe, Masahiko</au><au>Watanabe, Nobuhiro</au><au>Hotta, Harumi</au><au>Yamashita, Toshihide</au><au>Kamimura, Daisuke</au><au>Tanaka, Yuki</au><au>Murakami, Masaaki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>ATP spreads inflammation to other limbs through crosstalk between sensory neurons and interneurons</atitle><jtitle>The Journal of experimental medicine</jtitle><addtitle>J Exp Med</addtitle><date>2022-06-06</date><risdate>2022</risdate><volume>219</volume><issue>6</issue><issn>0022-1007</issn><eissn>1540-9538</eissn><abstract>Neural circuits between lesions are one mechanism through which local inflammation spreads to remote positions. Here, we show the inflammatory signal on one side of the joint is spread to the other side via sensory neuron-interneuron crosstalk, with ATP at the core. Surgical ablation or pharmacological inhibition of this neural pathway prevented inflammation development on the other side. Mechanistic analysis showed that ATP serves as both a neurotransmitter and an inflammation enhancer, thus acting as an intermediary between the local inflammation and neural pathway that induces inflammation on the other side. These results suggest blockade of this neural pathway, which is named the remote inflammation gateway reflex, may have therapeutic value for inflammatory diseases, particularly those, such as rheumatoid arthritis, in which inflammation spreads to remote positions.</abstract><cop>United States</cop><pub>Rockefeller University Press</pub><pmid>35579694</pmid><doi>10.1084/jem.20212019</doi><orcidid>https://orcid.org/0000-0002-0337-7052</orcidid><orcidid>https://orcid.org/0000-0003-2015-1503</orcidid><orcidid>https://orcid.org/0000-0001-8741-1635</orcidid><orcidid>https://orcid.org/0000-0002-1450-2381</orcidid><orcidid>https://orcid.org/0000-0001-9822-9804</orcidid><orcidid>https://orcid.org/0000-0002-4590-7162</orcidid><orcidid>https://orcid.org/0000-0003-2009-0595</orcidid><orcidid>https://orcid.org/0000-0002-3670-3416</orcidid><orcidid>https://orcid.org/0000-0003-1636-7942</orcidid><orcidid>https://orcid.org/0000-0003-4559-7018</orcidid><orcidid>https://orcid.org/0000-0002-6830-8453</orcidid><orcidid>https://orcid.org/0000-0002-8018-852X</orcidid><orcidid>https://orcid.org/0000-0002-1318-3542</orcidid><orcidid>https://orcid.org/0000-0003-3019-2923</orcidid><orcidid>https://orcid.org/0000-0002-3714-0360</orcidid><orcidid>https://orcid.org/0000-0002-0269-8962</orcidid><orcidid>https://orcid.org/0000-0003-1022-4430</orcidid><orcidid>https://orcid.org/0000-0001-5037-7138</orcidid><orcidid>https://orcid.org/0000-0001-7159-7279</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0022-1007 |
ispartof | The Journal of experimental medicine, 2022-06, Vol.219 (6) |
issn | 0022-1007 1540-9538 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9117706 |
source | Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals |
subjects | Brief Definitive Report Innate Immunity and Inflammation Neuroscience |
title | ATP spreads inflammation to other limbs through crosstalk between sensory neurons and interneurons |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-03T18%3A03%3A09IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=ATP%20spreads%20inflammation%20to%20other%20limbs%20through%20crosstalk%20between%20sensory%20neurons%20and%20interneurons&rft.jtitle=The%20Journal%20of%20experimental%20medicine&rft.au=Hasebe,%20Rie&rft.date=2022-06-06&rft.volume=219&rft.issue=6&rft.issn=0022-1007&rft.eissn=1540-9538&rft_id=info:doi/10.1084/jem.20212019&rft_dat=%3Cproquest_pubme%3E2665562211%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2665562211&rft_id=info:pmid/35579694&rfr_iscdi=true |