Neutrophil‐mediated mechanisms of damage and in‐vitro protective effect of colchicine in non‐vascular Behçet’s syndrome
Behçet’s syndrome (BS) is a systemic vasculitis with several clinical manifestations. Neutrophil hyperactivation mediates vascular BS pathogenesis, via both a massive reactive oxygen species (ROS) production and neutrophil extracellular traps (NETs) release. Here, we investigated neutrophil‐mediated...
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| Veröffentlicht in: | Clinical and experimental immunology 2021-12, Vol.206 (3), p.410-421 |
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| creator | Bettiol, Alessandra Becatti, Matteo Silvestri, Elena Argento, Flavia Rita Fini, Eleonora Mannucci, Amanda Galora, Silvia Mattioli, Irene Urban, Maria Letizia Malandrino, Danilo Palermo, Adalgisa Taddei, Niccolò Emmi, Giacomo Prisco, Domenico Fiorillo, Claudia |
| description | Behçet’s syndrome (BS) is a systemic vasculitis with several clinical manifestations. Neutrophil hyperactivation mediates vascular BS pathogenesis, via both a massive reactive oxygen species (ROS) production and neutrophil extracellular traps (NETs) release. Here, we investigated neutrophil‐mediated mechanisms of damage in non‐vascular BS manifestations and explored the in‐vitro effects of colchicine in counteracting these mechanisms. NETs and intracellular ROS production was assessed in blood samples from 80 BS patients (46 with active non‐vascular BS, 34 with inactive disease) and 80 healthy controls. Moreover, isolated neutrophils were incubated for 1 h with an oxidating agent [2,2′‐azobis (2‐amidinopropane) dihydrochloride; 250 nM] and the ability of pure colchicine pretreatment (100 ng/ml) to counteract oxidation‐induced damage was assessed. Patients with active non‐vascular BS showed remarkably increased NET levels [21.2, interquartile range (IQR) = 18.3–25.9 mU/ml] compared to patients with inactive disease (16.8, IQR = 13.3–20.2 mU/ml) and to controls (7.1, IQR = 5.1–8.7 mU/ml, p |
| doi_str_mv | 10.1111/cei.13664 |
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Neutrophil‐mediated mechanisms of damage might be directly involved in non‐vascular Behçet's syndrome. Neutrophil extracellular traps (NETs), more than an impaired redox status, might play a central role in the pathogenesis of mucosal, articular and intestinal BS manifestations. Colchicine might be effective to counteract neutrophils‐mediated damage in Behçet's syndrome, via the inhibition of NETs release.</description><identifier>ISSN: 0009-9104</identifier><identifier>EISSN: 1365-2249</identifier><identifier>DOI: 10.1111/cei.13664</identifier><identifier>PMID: 34562315</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Adult ; Anti-Inflammatory Agents - therapeutic use ; Antioxidants - therapeutic use ; Apoptosis ; autoimmunity ; Behcet Syndrome - drug therapy ; Behcet Syndrome - pathology ; Behcet's syndrome ; Case-Control Studies ; Colchicine ; Colchicine - therapeutic use ; Extracellular Traps - immunology ; Female ; human ; Humans ; Intracellular ; Leukocytes (neutrophilic) ; Male ; Middle Aged ; Mucosa ; Neutrophils ; Neutrophils - immunology ; Original ; ORIGINAL ARTICLES ; Oxidants ; Oxidation ; Oxidative Stress - drug effects ; Pathogenesis ; Patients ; Reactive oxygen species ; Reactive Oxygen Species - blood ; Retrospective Studies ; Systemic vasculitis ; vasculitis ; Vein & artery diseases</subject><ispartof>Clinical and experimental immunology, 2021-12, Vol.206 (3), p.410-421</ispartof><rights>2021 The Authors. published by John Wiley & Sons Ltd on behalf of British Society for Immunology</rights><rights>2021 The Authors. Clinical & Experimental Immunology published by John Wiley & Sons Ltd on behalf of British Society for Immunology.</rights><rights>2021. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4434-65010a4a3306a10c82309d1c1ce0c065c8bd95b079f227e899ba6cc64f9701723</citedby><cites>FETCH-LOGICAL-c4434-65010a4a3306a10c82309d1c1ce0c065c8bd95b079f227e899ba6cc64f9701723</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8561698/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8561698/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34562315$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bettiol, Alessandra</creatorcontrib><creatorcontrib>Becatti, Matteo</creatorcontrib><creatorcontrib>Silvestri, Elena</creatorcontrib><creatorcontrib>Argento, Flavia Rita</creatorcontrib><creatorcontrib>Fini, Eleonora</creatorcontrib><creatorcontrib>Mannucci, Amanda</creatorcontrib><creatorcontrib>Galora, Silvia</creatorcontrib><creatorcontrib>Mattioli, Irene</creatorcontrib><creatorcontrib>Urban, Maria Letizia</creatorcontrib><creatorcontrib>Malandrino, Danilo</creatorcontrib><creatorcontrib>Palermo, Adalgisa</creatorcontrib><creatorcontrib>Taddei, Niccolò</creatorcontrib><creatorcontrib>Emmi, Giacomo</creatorcontrib><creatorcontrib>Prisco, Domenico</creatorcontrib><creatorcontrib>Fiorillo, Claudia</creatorcontrib><title>Neutrophil‐mediated mechanisms of damage and in‐vitro protective effect of colchicine in non‐vascular Behçet’s syndrome</title><title>Clinical and experimental immunology</title><addtitle>Clin Exp Immunol</addtitle><description>Behçet’s syndrome (BS) is a systemic vasculitis with several clinical manifestations. Neutrophil hyperactivation mediates vascular BS pathogenesis, via both a massive reactive oxygen species (ROS) production and neutrophil extracellular traps (NETs) release. Here, we investigated neutrophil‐mediated mechanisms of damage in non‐vascular BS manifestations and explored the in‐vitro effects of colchicine in counteracting these mechanisms. NETs and intracellular ROS production was assessed in blood samples from 80 BS patients (46 with active non‐vascular BS, 34 with inactive disease) and 80 healthy controls. Moreover, isolated neutrophils were incubated for 1 h with an oxidating agent [2,2′‐azobis (2‐amidinopropane) dihydrochloride; 250 nM] and the ability of pure colchicine pretreatment (100 ng/ml) to counteract oxidation‐induced damage was assessed. Patients with active non‐vascular BS showed remarkably increased NET levels [21.2, interquartile range (IQR) = 18.3–25.9 mU/ml] compared to patients with inactive disease (16.8, IQR = 13.3–20.2 mU/ml) and to controls (7.1, IQR = 5.1–8.7 mU/ml, p < 0.001]. Also, intracellular ROS tended to increase in active BS, although not significantly. In active non‐vascular BS, NETs correlated with neutrophil ROS production (p < 0.001) and were particularly increased in patients with active mucosal (p < 0.001), articular (p = 0.004) and gastrointestinal symptoms (p = 0.006). In isolated neutrophils, colchicine significantly reduced oxidation‐induced NET production and cell apoptosis, although not via an anti‐oxidant activity. Neutrophil‐mediated mechanisms might be directly involved in non‐vascular BS, and NETs, more than ROS, might drive the pathogenesis of mucosal, articular and intestinal manifestations. Colchicine might be effective in counteracting neutrophils‐mediated damage in BS, although further studies are needed.
Neutrophil‐mediated mechanisms of damage might be directly involved in non‐vascular Behçet's syndrome. Neutrophil extracellular traps (NETs), more than an impaired redox status, might play a central role in the pathogenesis of mucosal, articular and intestinal BS manifestations. Colchicine might be effective to counteract neutrophils‐mediated damage in Behçet's syndrome, via the inhibition of NETs release.</description><subject>Adult</subject><subject>Anti-Inflammatory Agents - therapeutic use</subject><subject>Antioxidants - therapeutic use</subject><subject>Apoptosis</subject><subject>autoimmunity</subject><subject>Behcet Syndrome - drug therapy</subject><subject>Behcet Syndrome - pathology</subject><subject>Behcet's syndrome</subject><subject>Case-Control Studies</subject><subject>Colchicine</subject><subject>Colchicine - therapeutic use</subject><subject>Extracellular Traps - immunology</subject><subject>Female</subject><subject>human</subject><subject>Humans</subject><subject>Intracellular</subject><subject>Leukocytes (neutrophilic)</subject><subject>Male</subject><subject>Middle Aged</subject><subject>Mucosa</subject><subject>Neutrophils</subject><subject>Neutrophils - immunology</subject><subject>Original</subject><subject>ORIGINAL ARTICLES</subject><subject>Oxidants</subject><subject>Oxidation</subject><subject>Oxidative Stress - drug effects</subject><subject>Pathogenesis</subject><subject>Patients</subject><subject>Reactive oxygen species</subject><subject>Reactive Oxygen Species - blood</subject><subject>Retrospective Studies</subject><subject>Systemic vasculitis</subject><subject>vasculitis</subject><subject>Vein & artery diseases</subject><issn>0009-9104</issn><issn>1365-2249</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNp1kU1uFDEQhS0EIkNgwQWQJTaw6MT_3d4gwShApAg2sLY87uq0o257sLsHzW6OwJYTcBBukpPgyYQIkHAtyiV_9Vylh9BTSk5oOacO_AnlSol7aFGyrBgT-j5aEEJ0pSkRR-hRzlelVEqxh-iIC6kYp3KBdh9gnlJc93643n0bofV2ghaP4HobfB4zjh1u7WgvAdvQYh8KtvGlBa9TnMBNfgMYuq7c9qiLg-u98wEKikO8wW1282ATfgP9zx8wXe--Z5y3oU1xhMfoQWeHDE9u8zH6_Pbs0_J9dfHx3fny9UXlhOCiUpJQYoXlnChLiWsYJ7qljjogjijpmlWr5YrUumOshkbrlVXOKdHpmtCa8WP06qC7nldlTQdhSnYw6-RHm7YmWm_-fgm-N5dxYxqpqNJNEXhxK5DilxnyZEafHQyDDRDnbJislZJcsf1fz_9Br-KcQlmvUMWPEpoX6uWBcinmnKC7G4YSs_fVFF_Nja-Fffbn9HfkbyMLcHoAvvoBtv9XMsuz84PkL55yssI</recordid><startdate>202112</startdate><enddate>202112</enddate><creator>Bettiol, Alessandra</creator><creator>Becatti, Matteo</creator><creator>Silvestri, Elena</creator><creator>Argento, Flavia Rita</creator><creator>Fini, Eleonora</creator><creator>Mannucci, Amanda</creator><creator>Galora, Silvia</creator><creator>Mattioli, Irene</creator><creator>Urban, Maria Letizia</creator><creator>Malandrino, Danilo</creator><creator>Palermo, Adalgisa</creator><creator>Taddei, Niccolò</creator><creator>Emmi, Giacomo</creator><creator>Prisco, Domenico</creator><creator>Fiorillo, Claudia</creator><general>Oxford University Press</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7T5</scope><scope>7U9</scope><scope>H94</scope><scope>M7N</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>202112</creationdate><title>Neutrophil‐mediated mechanisms of damage and in‐vitro protective effect of colchicine in non‐vascular Behçet’s syndrome</title><author>Bettiol, Alessandra ; Becatti, Matteo ; Silvestri, Elena ; Argento, Flavia Rita ; Fini, Eleonora ; Mannucci, Amanda ; Galora, Silvia ; Mattioli, Irene ; Urban, Maria Letizia ; Malandrino, Danilo ; Palermo, Adalgisa ; Taddei, Niccolò ; Emmi, Giacomo ; Prisco, Domenico ; Fiorillo, Claudia</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4434-65010a4a3306a10c82309d1c1ce0c065c8bd95b079f227e899ba6cc64f9701723</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Adult</topic><topic>Anti-Inflammatory Agents - therapeutic use</topic><topic>Antioxidants - therapeutic use</topic><topic>Apoptosis</topic><topic>autoimmunity</topic><topic>Behcet Syndrome - drug therapy</topic><topic>Behcet Syndrome - pathology</topic><topic>Behcet's syndrome</topic><topic>Case-Control Studies</topic><topic>Colchicine</topic><topic>Colchicine - therapeutic use</topic><topic>Extracellular Traps - immunology</topic><topic>Female</topic><topic>human</topic><topic>Humans</topic><topic>Intracellular</topic><topic>Leukocytes (neutrophilic)</topic><topic>Male</topic><topic>Middle Aged</topic><topic>Mucosa</topic><topic>Neutrophils</topic><topic>Neutrophils - immunology</topic><topic>Original</topic><topic>ORIGINAL ARTICLES</topic><topic>Oxidants</topic><topic>Oxidation</topic><topic>Oxidative Stress - drug effects</topic><topic>Pathogenesis</topic><topic>Patients</topic><topic>Reactive oxygen species</topic><topic>Reactive Oxygen Species - blood</topic><topic>Retrospective Studies</topic><topic>Systemic vasculitis</topic><topic>vasculitis</topic><topic>Vein & artery diseases</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bettiol, Alessandra</creatorcontrib><creatorcontrib>Becatti, Matteo</creatorcontrib><creatorcontrib>Silvestri, Elena</creatorcontrib><creatorcontrib>Argento, Flavia Rita</creatorcontrib><creatorcontrib>Fini, Eleonora</creatorcontrib><creatorcontrib>Mannucci, Amanda</creatorcontrib><creatorcontrib>Galora, Silvia</creatorcontrib><creatorcontrib>Mattioli, Irene</creatorcontrib><creatorcontrib>Urban, Maria Letizia</creatorcontrib><creatorcontrib>Malandrino, Danilo</creatorcontrib><creatorcontrib>Palermo, Adalgisa</creatorcontrib><creatorcontrib>Taddei, Niccolò</creatorcontrib><creatorcontrib>Emmi, Giacomo</creatorcontrib><creatorcontrib>Prisco, Domenico</creatorcontrib><creatorcontrib>Fiorillo, Claudia</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Immunology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Clinical and experimental immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bettiol, Alessandra</au><au>Becatti, Matteo</au><au>Silvestri, Elena</au><au>Argento, Flavia Rita</au><au>Fini, Eleonora</au><au>Mannucci, Amanda</au><au>Galora, Silvia</au><au>Mattioli, Irene</au><au>Urban, Maria Letizia</au><au>Malandrino, Danilo</au><au>Palermo, Adalgisa</au><au>Taddei, Niccolò</au><au>Emmi, Giacomo</au><au>Prisco, Domenico</au><au>Fiorillo, Claudia</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Neutrophil‐mediated mechanisms of damage and in‐vitro protective effect of colchicine in non‐vascular Behçet’s syndrome</atitle><jtitle>Clinical and experimental immunology</jtitle><addtitle>Clin Exp Immunol</addtitle><date>2021-12</date><risdate>2021</risdate><volume>206</volume><issue>3</issue><spage>410</spage><epage>421</epage><pages>410-421</pages><issn>0009-9104</issn><eissn>1365-2249</eissn><abstract>Behçet’s syndrome (BS) is a systemic vasculitis with several clinical manifestations. Neutrophil hyperactivation mediates vascular BS pathogenesis, via both a massive reactive oxygen species (ROS) production and neutrophil extracellular traps (NETs) release. Here, we investigated neutrophil‐mediated mechanisms of damage in non‐vascular BS manifestations and explored the in‐vitro effects of colchicine in counteracting these mechanisms. NETs and intracellular ROS production was assessed in blood samples from 80 BS patients (46 with active non‐vascular BS, 34 with inactive disease) and 80 healthy controls. Moreover, isolated neutrophils were incubated for 1 h with an oxidating agent [2,2′‐azobis (2‐amidinopropane) dihydrochloride; 250 nM] and the ability of pure colchicine pretreatment (100 ng/ml) to counteract oxidation‐induced damage was assessed. Patients with active non‐vascular BS showed remarkably increased NET levels [21.2, interquartile range (IQR) = 18.3–25.9 mU/ml] compared to patients with inactive disease (16.8, IQR = 13.3–20.2 mU/ml) and to controls (7.1, IQR = 5.1–8.7 mU/ml, p < 0.001]. Also, intracellular ROS tended to increase in active BS, although not significantly. In active non‐vascular BS, NETs correlated with neutrophil ROS production (p < 0.001) and were particularly increased in patients with active mucosal (p < 0.001), articular (p = 0.004) and gastrointestinal symptoms (p = 0.006). In isolated neutrophils, colchicine significantly reduced oxidation‐induced NET production and cell apoptosis, although not via an anti‐oxidant activity. Neutrophil‐mediated mechanisms might be directly involved in non‐vascular BS, and NETs, more than ROS, might drive the pathogenesis of mucosal, articular and intestinal manifestations. Colchicine might be effective in counteracting neutrophils‐mediated damage in BS, although further studies are needed.
Neutrophil‐mediated mechanisms of damage might be directly involved in non‐vascular Behçet's syndrome. Neutrophil extracellular traps (NETs), more than an impaired redox status, might play a central role in the pathogenesis of mucosal, articular and intestinal BS manifestations. Colchicine might be effective to counteract neutrophils‐mediated damage in Behçet's syndrome, via the inhibition of NETs release.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>34562315</pmid><doi>10.1111/cei.13664</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Clinical and experimental immunology, 2021-12, Vol.206 (3), p.410-421 |
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| source | Oxford University Press Journals All Titles (1996-Current); MEDLINE; EZB-FREE-00999 freely available EZB journals; PubMed Central; Alma/SFX Local Collection |
| subjects | Adult Anti-Inflammatory Agents - therapeutic use Antioxidants - therapeutic use Apoptosis autoimmunity Behcet Syndrome - drug therapy Behcet Syndrome - pathology Behcet's syndrome Case-Control Studies Colchicine Colchicine - therapeutic use Extracellular Traps - immunology Female human Humans Intracellular Leukocytes (neutrophilic) Male Middle Aged Mucosa Neutrophils Neutrophils - immunology Original ORIGINAL ARTICLES Oxidants Oxidation Oxidative Stress - drug effects Pathogenesis Patients Reactive oxygen species Reactive Oxygen Species - blood Retrospective Studies Systemic vasculitis vasculitis Vein & artery diseases |
| title | Neutrophil‐mediated mechanisms of damage and in‐vitro protective effect of colchicine in non‐vascular Behçet’s syndrome |
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