{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,5]],"date-time":"2026-05-05T17:08:40Z","timestamp":1778000920123,"version":"3.51.4"},"reference-count":58,"publisher":"Oxford University Press (OUP)","issue":"4","license":[{"start":{"date-parts":[[2016,2,1]],"date-time":"2016-02-01T00:00:00Z","timestamp":1454284800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2016,2,15]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Annexin A1 (AnxA1) is a glucocorticoid-regulated protein endowed with anti-inflammatory and proresolving properties. Intact AnxA1 is a 37-kDa protein that may be cleaved in vivo at the N-terminal region by neutrophil proteases including elastase and proteinase-3, generating the 33-kDa isoform that is largely inactive. In this study, we investigated the dynamics of AnxA1 expression and the effects of synthetic (sivelestat [SIV]; Eglin) and natural (secretory leukocyte protease inhibitor [SLPI]; Elafin) protease inhibitors on the resolution of LPS-induced inflammation. During the settings of LPS inflammation AnxA1 cleavage associated closely with the peak of neutrophil and elastase expression and activity. SLPI expression increased during resolving phase of the pleurisy. Therapeutic treatment of LPS-challenge mice with recombinant human SLPI or Elafin accelerated resolution, an effect associated with increased numbers of apoptotic neutrophils in the pleural exudates, inhibition of elastase, and modulation of the survival-controlling proteins NF-\u03baB and Mcl-1. Similar effects were observed with SIV, which dose-dependently inhibited neutrophil elastase and shortened resolution intervals. Mechanistically, SIV-induced resolution was caspase-dependent, associated to increased levels of intact AnxA1 and decreased expression of NF-\u03baB and Mcl-1. The proresolving effect of antiproteases was also observed in a model of monosodium urate crystals\u2013induced inflammation. SIV skewed macrophages toward resolving phenotypes and enhanced efferocytosis of apoptotic neutrophils. A neutralizing antiserum against AnxA1 and a nonselective antagonist of AnxA1 receptor abolished the accelerated resolution promoted by SIV. Collectively, these results show that elastase inhibition not only inhibits inflammation but actually promotes resolution, and this response is mediated by protection of endogenous intact AnxA1 with ensuing augmentation of neutrophil apoptosis.<\/jats:p>","DOI":"10.4049\/jimmunol.1500886","type":"journal-article","created":{"date-parts":[[2016,1,23]],"date-time":"2016-01-23T03:44:59Z","timestamp":1453520699000},"page":"1922-1932","source":"Crossref","is-referenced-by-count":55,"title":["Proresolving Actions of Synthetic and Natural Protease Inhibitors Are Mediated by Annexin A1"],"prefix":"10.1093","volume":"196","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8188-3738","authenticated-orcid":false,"given":"Juliana P","family":"Vago","sequence":"first","affiliation":[{"name":"Departamento de An\u00e1lises Cl\u00ednicas e Toxicol\u00f3gicas, Faculdade de Farm\u00e1cia, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]},{"name":"Programa de P\u00f3s-Gradua\u00e7\u00e3o em Biologia Celular, Departamento de Morfologia, Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]},{"name":"Laborat\u00f3rio de Imunofarmacologia, Departamento de Bioqu\u00edmica e Imunologia, Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Luciana P","family":"Tavares","sequence":"additional","affiliation":[{"name":"Laborat\u00f3rio de Imunofarmacologia, Departamento de Bioqu\u00edmica e Imunologia, Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4527-6065","authenticated-orcid":false,"given":"Michelle A","family":"Sugimoto","sequence":"additional","affiliation":[{"name":"Departamento de An\u00e1lises Cl\u00ednicas e Toxicol\u00f3gicas, Faculdade de Farm\u00e1cia, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]},{"name":"Programa de P\u00f3s-Gradua\u00e7\u00e3o em Ci\u00eancias Farmac\u00eauticas, Faculdade de Farm\u00e1cia, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Graziele Let\u00edcia N","family":"Lima","sequence":"additional","affiliation":[{"name":"Departamento de An\u00e1lises Cl\u00ednicas e Toxicol\u00f3gicas, Faculdade de Farm\u00e1cia, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]},{"name":"Laborat\u00f3rio de Imunofarmacologia, Departamento de Bioqu\u00edmica e Imunologia, Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Izabela","family":"Galv\u00e3o","sequence":"additional","affiliation":[{"name":"Laborat\u00f3rio de Imunofarmacologia, Departamento de Bioqu\u00edmica e Imunologia, Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3243-8424","authenticated-orcid":false,"given":"Thais R","family":"de Caux","sequence":"additional","affiliation":[{"name":"Departamento de An\u00e1lises Cl\u00ednicas e Toxicol\u00f3gicas, Faculdade de Farm\u00e1cia, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]},{"name":"Laborat\u00f3rio de Imunofarmacologia, Departamento de Bioqu\u00edmica e Imunologia, Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"K\u00e1tia M","family":"Lima","sequence":"additional","affiliation":[{"name":"Departamento de An\u00e1lises Cl\u00ednicas e Toxicol\u00f3gicas, Faculdade de Farm\u00e1cia, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]},{"name":"Programa de P\u00f3s-Gradua\u00e7\u00e3o em Biologia Celular, Departamento de Morfologia, Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]},{"name":"Laborat\u00f3rio de Imunofarmacologia, Departamento de Bioqu\u00edmica e Imunologia, Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ana Lu\u00edza C","family":"Ribeiro","sequence":"additional","affiliation":[{"name":"Departamento de An\u00e1lises Cl\u00ednicas e Toxicol\u00f3gicas, Faculdade de Farm\u00e1cia, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]},{"name":"Laborat\u00f3rio de Imunofarmacologia, Departamento de Bioqu\u00edmica e Imunologia, Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fernanda S","family":"Carneiro","sequence":"additional","affiliation":[{"name":"Departamento de An\u00e1lises Cl\u00ednicas e Toxicol\u00f3gicas, Faculdade de Farm\u00e1cia, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]},{"name":"Laborat\u00f3rio de Imunofarmacologia, Departamento de Bioqu\u00edmica e Imunologia, Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fernanda Freire C","family":"Nunes","sequence":"additional","affiliation":[{"name":"Departamento de An\u00e1lises Cl\u00ednicas e Toxicol\u00f3gicas, Faculdade de Farm\u00e1cia, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1038-2324","authenticated-orcid":false,"given":"Vanessa","family":"Pinho","sequence":"additional","affiliation":[{"name":"Programa de P\u00f3s-Gradua\u00e7\u00e3o em Biologia Celular, Departamento de Morfologia, Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]},{"name":"Laborat\u00f3rio de Imunofarmacologia, Departamento de Bioqu\u00edmica e Imunologia, Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2068-3331","authenticated-orcid":false,"given":"Mauro","family":"Perretti","sequence":"additional","affiliation":[{"name":"William Harvey Research Institute, Barts and The London School of Medicine, Queen Mary University of London , London EC1M 6BQ ,","place":["United Kingdom"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6944-3008","authenticated-orcid":false,"given":"Mauro M","family":"Teixeira","sequence":"additional","affiliation":[{"name":"Laborat\u00f3rio de Imunofarmacologia, Departamento de Bioqu\u00edmica e Imunologia, Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1042-9762","authenticated-orcid":false,"given":"Lirl\u00e2ndia P","family":"Sousa","sequence":"additional","affiliation":[{"name":"Departamento de An\u00e1lises Cl\u00ednicas e Toxicol\u00f3gicas, Faculdade de Farm\u00e1cia, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]},{"name":"Programa de P\u00f3s-Gradua\u00e7\u00e3o em Biologia Celular, Departamento de Morfologia, Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]},{"name":"Laborat\u00f3rio de Imunofarmacologia, Departamento de Bioqu\u00edmica e Imunologia, Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte ,","place":["Brazil"]},{"name":"Programa de P\u00f3s-Gradua\u00e7\u00e3o em Ci\u00eancias Farmac\u00eauticas, Faculdade de Farm\u00e1cia, Universidade Federal de Minas Gerais , 31270-901 Belo Horizonte 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Opin. Hematol."},{"key":"2025030702133751600_r3","doi-asserted-by":"crossref","first-page":"1048","DOI":"10.1111\/j.1476-5381.2009.00448.x","article-title":"Proteases and antiproteases in chronic neutrophilic lung disease - relevance to drug discovery","volume":"158","author":"Greene","year":"2009","journal-title":"Br. J. Pharmacol."},{"key":"2025030702133751600_r4","doi-asserted-by":"crossref","first-page":"1209","DOI":"10.2174\/0929866521666140819123932","article-title":"Inflammation-mediating proteases: structure, function in (patho) physiology and inhibition","volume":"21","author":"Mancek-Keber","year":"2014","journal-title":"Protein Pept. Lett."},{"key":"2025030702133751600_r5","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1186\/rr18","article-title":"The role of secretory leukocyte proteinase inhibitor and elafin (elastase-specific inhibitor\/skin-derived antileukoprotease) as alarm antiproteinases in inflammatory lung disease","volume":"1","author":"Sallenave","year":"2000","journal-title":"Respir. Res."},{"key":"2025030702133751600_r6","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1042\/CS20050115","article-title":"SLPI and elafin: one glove, many fingers","volume":"110","author":"Williams","year":"2006","journal-title":"Clin. Sci."},{"key":"2025030702133751600_r7","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1042\/BST0350273","article-title":"The role of secretory leucoprotease inhibitor in the resolution of inflammatory responses","volume":"35","author":"Weldon","year":"2007","journal-title":"Biochem. Soc. 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Med."},{"key":"2025030702133751600_r9","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1038\/nature13479","article-title":"Pro-resolving lipid mediators are leads for resolution physiology","volume":"510","author":"Serhan","year":"2014","journal-title":"Nature"},{"key":"2025030702133751600_r10","doi-asserted-by":"crossref","first-page":"e60","DOI":"10.1182\/blood-2012-04-423525","article-title":"Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators","volume":"120","author":"Dalli","year":"2012","journal-title":"Blood"},{"key":"2025030702133751600_r11","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1016\/j.coph.2013.03.007","article-title":"Pharmacological strategies to resolve acute inflammation","volume":"13","author":"Sousa","year":"2013","journal-title":"Curr. Opin. Pharmacol."},{"key":"2025030702133751600_r12","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1038\/nri2470","article-title":"Annexin A1 and glucocorticoids as effectors of the resolution of inflammation","volume":"9","author":"Perretti","year":"2009","journal-title":"Nat. Rev. Immunol."},{"key":"2025030702133751600_r13","doi-asserted-by":"crossref","first-page":"29998","DOI":"10.1074\/jbc.M702876200","article-title":"Annexin 1 cleavage in activated neutrophils: a pivotal role for proteinase 3","volume":"282","author":"Vong","year":"2007","journal-title":"J. Biol. Chem."},{"key":"2025030702133751600_r14","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1016\/S0002-9440(10)64002-3","article-title":"Neutrophil interaction with inflamed postcapillary venule endothelium alters annexin 1 expression","volume":"158","author":"Oliani","year":"2001","journal-title":"Am. J. Pathol."},{"key":"2025030702133751600_r15","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1165\/ajrcmb.18.1.2808","article-title":"Degradation of annexin I in bronchoalveolar lavage fluid from patients with cystic fibrosis","volume":"18","author":"Tsao","year":"1998","journal-title":"Am. J. Respir. Cell Mol. Biol."},{"key":"2025030702133751600_r16","doi-asserted-by":"crossref","first-page":"3057","DOI":"10.4049\/jimmunol.1000119","article-title":"A proinflammatory role for proteolytically cleaved annexin A1 in neutrophil transendothelial migration","volume":"185","author":"Williams","year":"2010","journal-title":"J. Immunol."},{"key":"2025030702133751600_r17","doi-asserted-by":"crossref","first-page":"4288","DOI":"10.1182\/blood-2010-02-270520","article-title":"Design and characterization of a cleavage-resistant Annexin A1 mutant to control inflammation in the microvasculature","volume":"116","author":"Pederzoli-Ribeil","year":"2010","journal-title":"Blood"},{"key":"2025030702133751600_r18","doi-asserted-by":"crossref","first-page":"1872","DOI":"10.1136\/annrheumdis-2011-201180","article-title":"The impact of endogenous annexin A1 on glucocorticoid control of inflammatory arthritis","volume":"71","author":"Patel","year":"2012","journal-title":"Ann. Rheum. 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