{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,3]],"date-time":"2026-04-03T04:34:12Z","timestamp":1775190852485,"version":"3.50.1"},"reference-count":135,"publisher":"Oxford University Press (OUP)","issue":"5","license":[{"start":{"date-parts":[[2010,12,17]],"date-time":"2010-12-17T00:00:00Z","timestamp":1292544000000},"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":[[2010,12,17]]},"abstract":"<jats:title>ABSTRACT<\/jats:title><jats:p>Macrophages and neutrophils possess overlapping and complementary features associated to their common origin and subsequent specialization during myelopoiesis. That specialization results in macrophage lineage being limited in antimicrobial capacity and cytotoxicity comparatively with the neutrophil lineage. These and other features of mature macrophages and neutrophils, like different lifespan and tissue localization, promote their particular lifestyles and prompt a functional partnership for cooperation in the protective antimicrobial host defense. This partnership includes reciprocal recruitment to infected sites, cooperative effector antimicrobial activities, and pro-resolving anti-inflammatory effects. One modality of the cooperative effector antimicrobial activities involves the phagocytosis by the macrophage of apoptosing neutrophils and of nonapoptosing neutrophils expressing \u201ceat-me\u201d signals. This cooperative interaction results in the enhancement of the comparatively limited macrophage antimicrobial capacity by the acquisition and use of potent neutrophil microbicidal molecules. Here, data are reviewed that suggest that this is a process actively engaging the two professional phagocytes. Phagocytosis of neutrophils by macrophages at inflammatory\/infectious foci accumulates two effects beneficial to the protective host immune response: help in the control of the infection and prevention of neutrophil autolysis, effects that converge to accelerate the resolution of the infection-associated inflammation.<\/jats:p>","DOI":"10.1189\/jlb.0910536","type":"journal-article","created":{"date-parts":[[2010,12,18]],"date-time":"2010-12-18T04:21:56Z","timestamp":1292646116000},"page":"675-683","source":"Crossref","is-referenced-by-count":111,"title":["Macrophage phagocytosis of neutrophils at inflammatory\/infectious foci: a cooperative mechanism in the control of infection and infectious inflammation"],"prefix":"10.1093","volume":"89","author":[{"given":"Manuel T","family":"Silva","sequence":"first","affiliation":[{"name":"Instituto de Biologia Molecular e Celular , Porto, Portugal"}]}],"member":"286","published-online":{"date-parts":[[2010,12,17]]},"reference":[{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1006\/fsim.1998.0139","article-title":"Uptake of neutrophils and neutrophilic components by macrophages in the inflamed peritoneal cavity of rainbow trout (Oncorhynchus mykiss)","volume":"8","author":"Afonso","year":"1998","journal-title":"Fish Shellfish Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"S61","DOI":"10.1017\/S0031182006000862","article-title":"Neutrophils, apoptosis and phagocytic clearance: an innate sequence of cellular responses regulating intramacrophagic parasite infections","volume":"132","author":"Ribeiro-Gomes","year":"2006","journal-title":"Parasitology"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1189\/jlb.0809549","article-title":"When two is better than one: macrophages and neutrophils work in concert in innate immunity as complementary and cooperative partners of a myeloid phagocyte system","volume":"87","author":"Silva","year":"2010","journal-title":"J. Leukoc. Biol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1189\/jlb.1109767","article-title":"Neutrophils and macrophages work in concert as inducers and effectors of adaptive immunity against extracellular and intracellular microbial pathogens","volume":"87","author":"Silva","year":"2010","journal-title":"J. Leukoc. Biol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1038\/35004599","article-title":"A clonogenic common myeloid progenitor that gives rise to all myeloid lineages","volume":"404","author":"Akashi","year":"2000","journal-title":"Nature"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"4410","DOI":"10.4049\/jimmunol.172.7.4410","article-title":"Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response","volume":"172","author":"Sunderk\u00f6tter","year":"2004","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1146\/annurev.immunol.26.021607.090326","article-title":"Monocyte-mediated defense against microbial pathogens","volume":"26","author":"Serbina","year":"2008","journal-title":"Annu. Rev. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1186\/1465-9921-7-143","article-title":"Neutrophil cannibalism\u2013a back up when the macrophage clearance system is insufficient","volume":"7","author":"Rydell-T\u00f6rm\u00e4nen","year":"2006","journal-title":"Respir. Res."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"391","DOI":"10.4049\/jimmunol.0900564","article-title":"Phagocytosis of apoptototic cells by neutrophil granulocytes: diminished proinflammatory neutrophil functions in the presence of apoptotic cells","volume":"184","author":"Esmann","year":"2010","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1038\/nri2294","article-title":"Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators","volume":"8","author":"Serhan","year":"2008","journal-title":"Nat. Rev. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"4079","DOI":"10.2741\/3514","article-title":"Survival of monocytes and macrophages and their role in health and disease","volume":"14","author":"Hunter","year":"2009","journal-title":"Front. Biosci."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"2413","DOI":"10.2741\/3387","article-title":"Regulation of monocytes and macrophages cell fate","volume":"14","author":"Gonzalez-Mejia","year":"2009","journal-title":"Front. Biosci."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"2577","DOI":"10.4049\/jimmunol.157.6.2577","article-title":"In vivo fate of the inflammatory macrophage during the resolution of inflammation: inflammatory macrophages do not die locally, but emigrate to the draining lymph nodes","volume":"157","author":"Bellingan","year":"1996","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"846","DOI":"10.1038\/nature01320","article-title":"Points of control in inflammation","volume":"420","author":"Nathan","year":"2002","journal-title":"Nature"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1615\/CritRevImmunol.v20.i5.30","article-title":"Critical roles of Toll-like receptors in host defense","volume":"20","author":"Kaisho","year":"2000","journal-title":"Crit. Rev. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"2660","DOI":"10.1182\/blood-2003-04-1078","article-title":"Toll-like receptors stimulate human neutrophil function","volume":"102","author":"Hayashi","year":"2003","journal-title":"Blood"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1016\/0882-4010(89)90079-X","article-title":"Neutrophil-macrophage cooperation in the host defense against mycobacterial infections","volume":"6","author":"Silva","year":"1989","journal-title":"Microb. Pathog."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"3988","DOI":"10.4049\/jimmunol.179.6.3988","article-title":"Neutrophils activate macrophages for intracellular killing of Leishmania major through recruitment of TLR4 by neutrophil elastase","volume":"179","author":"Ribeiro-Gomes","year":"2007","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"8088","DOI":"10.4049\/jimmunol.0803720","article-title":"Neutrophils and macrophages cooperate in host resistance against Leishmania braziliensis infection","volume":"183","author":"Novais","year":"2009","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"4176","DOI":"10.4049\/jimmunol.134.6.4176","article-title":"Lactoferrin effects on phagocytic cell function. I. Increased uptake and killing of an intracellular parasite by murine macrophages and human monocytes","volume":"134","author":"Lima","year":"1985","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/S0162-3109(96)00118-X","article-title":"Enhancement of phagocytosis by corticostatin I (CSI) in cultured mouse peritoneal macrophages","volume":"35","author":"Ichinose","year":"1996","journal-title":"Immunopharmacology"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1034\/j.1600-065X.2000.17702.x","article-title":"Leukocyte granule proteins mobilize innate host defenses and adaptive immune responses","volume":"177","author":"Chertov","year":"2000","journal-title":"Immunol. Rev."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1016\/S1471-4906(02)02246-9","article-title":"Mammalian defensins in immunity: more than just microbicidal","volume":"23","author":"Yang","year":"2002","journal-title":"Trends Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"3758","DOI":"10.4049\/jimmunol.172.6.3758","article-title":"The human cationic peptide LL-37 induces activation of the extracellular signal-regulated kinase and p38 kinase pathways in primary human monocytes","volume":"172","author":"Bowdish","year":"2004","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"1251","DOI":"10.1111\/j.1462-5822.2005.00549.x","article-title":"Antimicrobial peptides and endotoxin inhibit cytokine and nitric oxide release but amplify respiratory burst response in human and murine macrophages","volume":"7","author":"Zughaier","year":"2005","journal-title":"Cell. Microbiol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"1157","DOI":"10.1007\/s00109-009-0508-6","article-title":"Direct and alternative antimicrobial mechanisms of neutrophil-derived granule proteins","volume":"87","author":"Soehnlein","year":"2009","journal-title":"J. Mol. Med."},{"key":"2023032914004198400_","first-page":"391","article-title":"Expression of peroxidase-dependent iodination by macrophages ingesting neutrophil debris","volume":"28","author":"Heifets","year":"1980","journal-title":"J. Reticuloendothel. Soc."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1007\/BF00221477","article-title":"Uptake and utilization of human polymorphonuclear leukocyte granule myeloperoxidase by mouse peritoneal macrophages","volume":"257","author":"Leung","year":"1989","journal-title":"Cell Tissue Res."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1126\/science.6301006","article-title":"Neutrophil pseudoplatelets: their discrimination by myeloperoxidase demonstration","volume":"220","author":"Hanker","year":"1983","journal-title":"Science"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"27","DOI":"10.3354\/dao034027","article-title":"Neutrophil and macrophage responses to inflammation in the peritoneal cavity of rainbow trout Oncorhynchus mykiss. A light and electron microscopic cytochemical study","volume":"34","author":"Afonso","year":"1998","journal-title":"Dis. Aquat. Organ."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1006\/fsim.1997.0089","article-title":"The leucocyte population of the unstimulated peritoneal cavity of rainbow trout (Oncorhynchus mykiss)","volume":"7","author":"Afonso","year":"1997","journal-title":"Fish Shellfish Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"1317","DOI":"10.1016\/j.micinf.2003.09.008","article-title":"Neutrophil granules and secretory vesicles in inflammation","volume":"5","author":"Faurschou","year":"2003","journal-title":"Microbes Infect."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"3491","DOI":"10.1172\/JCI35740","article-title":"Neutrophil primary granule proteins HBP and HNP1\u20133 boost bacterial phagocytosis by human and murine macrophages","volume":"118","author":"Soehnlein","year":"2008","journal-title":"J. Clin. Invest."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1183\/09031936.06.00126905","article-title":"Direct evidence of secondary necrosis of neutrophils during intense lung inflammation","volume":"28","author":"Rydell-T\u00f6rm\u00e4nen","year":"2006","journal-title":"Eur. Respir. J."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"780","DOI":"10.1189\/jlb.0208086","article-title":"Neutrophil secondary necrosis is induced by LL-37 derived from cathelicidin","volume":"84","author":"Zhang","year":"2008","journal-title":"J. Leukoc. Biol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"885","DOI":"10.1189\/jlb.0410205","article-title":"Bacteria-induced phagocyte secondary necrosis as a pathogenicity mechanism","volume":"88","author":"Silva","year":"2010","journal-title":"J. Leukoc. Biol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1146\/annurev.immunol.17.1.593","article-title":"Mechanisms of phagocytosis in macrophages","volume":"17","author":"Aderem","year":"1999","journal-title":"Annu. Rev. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1146\/annurev.cellbio.20.010403.102755","article-title":"Phagocytosis: at the crossroads of innate and adaptive immunity","volume":"21","author":"Jutras","year":"2005","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"784","DOI":"10.1038\/35037722","article-title":"Corpse clearance defines the meaning of cell death","volume":"407","author":"Savill","year":"2000","journal-title":"Nature"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1007\/978-1-4419-0901-5_9","article-title":"Pattern recognition in phagocytic clearance of altered self","volume":"653","author":"Nakanishi","year":"2009","journal-title":"Adv. Exp. Med. Biol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1016\/j.it.2006.03.005","article-title":"Apoptotic cell removal in development and tissue homeostasis","volume":"27","author":"Henson","year":"2006","journal-title":"Trends Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1084\/jem.156.2.430","article-title":"Phagocytosis of senescent neutrophils by human monocyte-derived macrophages and rabbit inflammatory macrophages","volume":"156","author":"Newman","year":"1982","journal-title":"J. Exp. Med."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1002\/jlb.65.1.35","article-title":"Macrophage phagocytosis of wound neutrophils","volume":"65","author":"Meszaros","year":"1999","journal-title":"J. Leukoc. Biol."},{"key":"2023032914004198400_","first-page":"278","article-title":"Peritoneal macrophages which phagocytose autologous polymorphonuclear leucocytes in guinea-pigs. I: induction by irritants and microorganisms and inhibition by colchicine","volume":"63","author":"Sanui","year":"1982","journal-title":"Br. J. Exp. Pathol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1042\/bse0390105","article-title":"The final step in programmed cell death: phagocytes carry apoptotic cells to the grave","volume":"39","author":"DeCathelineau","year":"2003","journal-title":"Essays Biochem."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.imlet.2005.11.016","article-title":"Inflammation and the apoptophagocytic system","volume":"104","author":"M\u00e1jai","year":"2006","journal-title":"Immunol. Lett."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1016\/S0960-9822(00)00598-4","article-title":"Differences between the clearance of apoptotic cells by professional and non-professional phagocytes","volume":"10","author":"Parnaik","year":"2000","journal-title":"Curr. Biol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/S0952-7915(99)80009-0","article-title":"Phagocytosis and development: back to the future","volume":"11","author":"Franc","year":"1999","journal-title":"Curr. Opin. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1038\/sj.cdd.4402184","article-title":"Clearance of apoptotic cells by phagocytes","volume":"15","author":"Erwig","year":"2008","journal-title":"Cell Death Differ."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"1545","DOI":"10.1084\/jem.182.5.1545","article-title":"Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl","volume":"182","author":"Martin","year":"1995","journal-title":"J. Exp. Med."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"2207","DOI":"10.4049\/jimmunol.148.7.2207","article-title":"Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages","volume":"148","author":"Fadok","year":"1992","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"33736","DOI":"10.1074\/jbc.M807047200","article-title":"NADPH oxidase-dependent generation of lysophosphatidylserine enhances clearance of activated and dying neutrophils via G2A","volume":"283","author":"Frasch","year":"2008","journal-title":"J. Biol. Chem."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.bbrc.2010.02.106","article-title":"Programmed cell clearance: molecular regulation of the elimination of apoptotic cell corpses and its role in the resolution of inflammation","volume":"396","author":"Fadeel","year":"2010","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1016\/S0092-8674(03)00422-7","article-title":"Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal","volume":"113","author":"Lauber","year":"2003","journal-title":"Cell"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/S0161-5890(03)00109-3","article-title":"\u201cEat me\u201d and \u201cdon't eat me\u201d signals govern the innate immune response and tissue repair in the CNS: emphasis on the critical role of the complement system","volume":"40","author":"Elward","year":"2003","journal-title":"Mol. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"3446","DOI":"10.1128\/iai.60.8.3446-3447.1992","article-title":"Mouse neutrophils lack defensins","volume":"60","author":"Eisenhauer","year":"1992","journal-title":"Infect. Immun."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"4720","DOI":"10.1128\/iai.60.11.4720-4725.1992","article-title":"Activity of defensins from human neutrophilic granulocytes against Mycobacterium avium-Mycobacterium intracellulare","volume":"60","author":"Ogata","year":"1992","journal-title":"Infect. Immun."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"890","DOI":"10.1172\/JCI1112","article-title":"Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine\/paracrine mechanisms involving TGF-\u03b2, PGE2, and PAF","volume":"101","author":"Fadok","year":"1998","journal-title":"J. Clin. Invest."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"6319","DOI":"10.4049\/jimmunol.173.10.6319","article-title":"Pathogen-induced apoptotic neutrophils express heat shock proteins and elicit activation of human macrophages","volume":"173","author":"Zheng","year":"2004","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"4454","DOI":"10.4049\/jimmunol.172.7.4454","article-title":"Macrophage interactions with neutrophils regulate Leishmania major infection","volume":"172","author":"Ribeiro-Gomes","year":"2004","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"2044","DOI":"10.4049\/jimmunol.1000017","article-title":"Proinflammatory clearance of apoptotic neutrophils induces an IL-12lowIL-10high regulatory phenotype in macrophages","volume":"185","author":"Filardy","year":"2010","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"R795","DOI":"10.1016\/S0960-9822(01)00474-2","article-title":"Apoptotic cell removal","volume":"11","author":"Henson","year":"2001","journal-title":"Curr. Biol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1172\/JCI0211638","article-title":"Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-\u03b21 secretion and the resolution of inflammation","volume":"109","author":"Huynh","year":"2002","journal-title":"J. Clin. Invest."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"6358","DOI":"10.4049\/jimmunol.168.12.6358","article-title":"Mycobacterium tuberculosis promotes apoptosis in human neutrophils by activating caspase-3 and altering expression of Bax\/Bcl-xL via an oxygen-dependent pathway","volume":"168","author":"Perskvist","year":"2002","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/j.micinf.2007.11.007","article-title":"Mycobacterium tuberculosis-induced apoptotic neutrophils trigger a pro-inflammatory response in macrophages through release of heat shock protein 72, acting in synergy with the bacteria","volume":"10","author":"Persson","year":"2008","journal-title":"Microbes Infect."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"828","DOI":"10.1016\/j.micinf.2010.05.009","article-title":"Guinea pig neutrophil-macrophage interactions during infection with Mycobacterium tuberculosis","volume":"12","author":"Sawant","year":"2010","journal-title":"Microbes Infect."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1146\/annurev.immunol.23.021704.115653","article-title":"How neutrophils kill microbes","volume":"23","author":"Segal","year":"2005","journal-title":"Annu. Rev. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1172\/JCI112869","article-title":"Tissue injury in inflammation. Oxidants, proteinases, and cationic proteins","volume":"79","author":"Henson","year":"1987","journal-title":"J. Clin. Invest."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1172\/JCI113970","article-title":"Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages","volume":"83","author":"Savill","year":"1989","journal-title":"J. Clin. Invest."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1165\/ajrcmb.12.2.7865221","article-title":"Macrophage engulfment of apoptotic neutrophils contributes to the resolution of acute pulmonary inflammation in vivo","volume":"12","author":"Cox","year":"1995","journal-title":"Am. J. Respir. Cell Mol. Biol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"698","DOI":"10.1189\/jlb.69.5.698","article-title":"Phenotypic and functional change of cytokine-activated neutrophils: inflammatory neutrophils are heterogeneous and enhance adaptive immune responses","volume":"69","author":"Yamashiro","year":"2001","journal-title":"J. Leukoc. Biol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1034\/j.1600-065X.2003.00038.x","article-title":"Neutrophil apoptosis pathways and their modifications in inflammation","volume":"193","author":"Simon","year":"2003","journal-title":"Immunol. Rev."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1016\/S1074-7613(00)80278-2","article-title":"A novel role for the \u03b2 2 integrin CD11b\/CD18 in neutrophil apoptosis: a homeostatic mechanism in inflammation","volume":"5","author":"Coxon","year":"1996","journal-title":"Immunity"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"3986","DOI":"10.4049\/jimmunol.156.10.3986","article-title":"Neutrophils undergo apoptosis following ingestion of Escherichia coli","volume":"156","author":"Watson","year":"1996","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"775","DOI":"10.1189\/jlb.71.5.775","article-title":"Oxidant-mediated phosphatidylserine exposure and macrophage uptake of activated neutrophils: possible impairment in chronic granulomatous disease","volume":"71","author":"Hampton","year":"2002","journal-title":"J. Leukoc. Biol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1007\/s12026-008-8049-6","article-title":"Neutrophil apoptosis and the resolution of infection","volume":"43","author":"Kennedy","year":"2009","journal-title":"Immunol. Res."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1023\/B:APPT.0000031448.64969.fa","article-title":"Modulation of phagocyte apoptosis by bacterial pathogens","volume":"9","author":"DeLeo","year":"2004","journal-title":"Apoptosis"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"435","DOI":"10.4049\/jimmunol.165.1.435","article-title":"Macrophage-induced neutrophil apoptosis","volume":"165","author":"Meszaros","year":"2000","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"3633","DOI":"10.1242\/dev.124.18.3633","article-title":"Macrophages induce apoptosis in normal cells in vivo","volume":"124","author":"Diez-Roux","year":"1997","journal-title":"Development"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"480","DOI":"10.4049\/jimmunol.162.1.480","article-title":"Phagocytosis triggers macrophage release of Fas ligand and induces apoptosis of bystander leukocytes","volume":"162","author":"Brown","year":"1999","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"2772","DOI":"10.1182\/blood.V90.7.2772","article-title":"Regulation of neutrophil apoptosis by tumor necrosis factor-\u03b1 requirement for TNFR55 and TNFR75 for induction of apoptosis in vitro","volume":"90","author":"Murray","year":"1997","journal-title":"Blood"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"2403","DOI":"10.4049\/jimmunol.154.5.2403","article-title":"In vivo regulation of rat neutrophil apoptosis occurring spontaneously or induced with TNF-\u03b1 or cycloheximide","volume":"154","author":"Tsuchida","year":"1995","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"6656","DOI":"10.4049\/jimmunol.176.11.6656","article-title":"Macrophages induce neutrophil apoptosis through membrane TNF, a process amplified by Leishmania major","volume":"176","author":"Allenbach","year":"2006","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"1047","DOI":"10.1084\/jem.179.3.1047","article-title":"bcl-2 inhibits apoptosis of neutrophils but not their engulfment by macrophages","volume":"179","author":"Lagasse","year":"1994","journal-title":"J. Exp. Med."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1006\/cimm.1998.1339","article-title":"Mice deficient in fas ligand (gld) or fas (lpr) show few alterations in granulopoiesis","volume":"188","author":"Fecho","year":"1998","journal-title":"Cell. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1002\/jlb.64.3.373","article-title":"Fas ligand (gld)- and Fas (lpr)-deficient mice do not show alterations in the extravasation or apoptosis of inflammatory neutrophils","volume":"64","author":"Fecho","year":"1998","journal-title":"J. Leukoc. Biol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"8498","DOI":"10.1074\/jbc.M606950200","article-title":"Nitrosative stress inhibits the aminophospholipid translocase resulting in phosphatidylserine externalization and macrophage engulfment: implications for the resolution of inflammation","volume":"282","author":"Tyurina","year":"2007","journal-title":"J. Biol. Chem."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1189\/jlb.0408232","article-title":"Induction of caspase- and reactive oxygen species-independent phosphatidylserine externalization in primary human neutrophils: role in macrophage recognition and engulfment","volume":"85","author":"Jitkaew","year":"2009","journal-title":"J. Leukoc. Biol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"4808","DOI":"10.1182\/blood.V92.12.4808","article-title":"Involvement of caspases in neutrophil apoptosis: regulation by reactive oxygen species","volume":"92","author":"Fadeel","year":"1998","journal-title":"Blood"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"17625","DOI":"10.1074\/jbc.M313414200","article-title":"Phospholipid flip-flop and phospholipid scramblase 1 (PLSCR1) co-localize to uropod rafts in formylated Met-Leu-Phestimulated neutrophils","volume":"279","author":"Frasch","year":"2004","journal-title":"J. Biol. Chem."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"487","DOI":"10.4049\/jimmunol.169.1.487","article-title":"A role for oxidative stress in apoptosis: oxidation and externalization of phosphatidylserine is required for macrophage clearance of cells undergoing Fas-mediated apoptosis","volume":"169","author":"Kagan","year":"2002","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1038\/ni.f.203","article-title":"Protein-glycan interactions in The control of innate and adaptive immune responses","volume":"9","author":"Van Kooyk","year":"2008","journal-title":"Nat. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1023\/B:GLYC.0000014088.21242.e0","article-title":"Galectins as inflammatory mediators","volume":"19","author":"Almkvist","year":"2004","journal-title":"Glycoconj. J."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1038\/nrmicro2146","article-title":"Roles of galectins in infection","volume":"7","author":"Vasta","year":"2009","journal-title":"Nat. Rev. Microbiol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1358\/dnp.2007.20.7.1183933","article-title":"The role of galectin-3 in promotion of the inflammatory response","volume":"20","author":"Liu","year":"2007","journal-title":"Drug News Perspect."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"395","DOI":"10.2353\/ajpath.2008.070870","article-title":"Galectin-3 reduces the severity of pneumococcal pneumonia by augmenting neutrophil function","volume":"172","author":"Farnworth","year":"2008","journal-title":"Am. J. Pathol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"2156","DOI":"10.4049\/jimmunol.165.4.2156","article-title":"Human galectin-3 is a novel chemoat-tractant for monocytes and macrophages","volume":"165","author":"Sano","year":"2000","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"3091","DOI":"10.4049\/jimmunol.180.5.3091","article-title":"Differential roles of galectin-1 and galectin-3 in regulating leukocyte viability and cytokine secretion","volume":"180","author":"Stowell","year":"2008","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1093\/glycob\/cwn104","article-title":"Galectin-3 functions as an opsonin and enhances the macrophage clearance of apoptotic neutrophils","volume":"19","author":"Karlsson","year":"2009","journal-title":"Glycobiology"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"41282","DOI":"10.1074\/jbc.M306624200","article-title":"Dimeric galectin-1 induces surface exposure of phosphatidylserine and phagocytic recognition of leukocytes without inducing apoptosis","volume":"278","author":"Dias-Baruffi","year":"2003","journal-title":"J. Biol. Chem."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"28623","DOI":"10.1074\/jbc.M414140200","article-title":"Contributions of Ca2+ to galectin-1-induced exposure of phosphatidylserine on activated neutrophils","volume":"280","author":"Karmakar","year":"2005","journal-title":"J. Biol. Chem."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1182\/blood-2006-03-007153","article-title":"Human galectin-1, -2, and -4 induce surface exposure of phosphatidylserine in activated human neutrophils but not in activated T cells","volume":"109","author":"Stowell","year":"2007","journal-title":"Blood"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"1408","DOI":"10.1091\/mbc.e08-07-0786","article-title":"Galectin-1 induces reversible phosphatidylserine exposure at the plasma membrane","volume":"20","author":"Stowell","year":"2009","journal-title":"Mol. Biol. Cell"},{"key":"2023032914004198400_","first-page":"1016","article-title":"Expression and function of galectin-3, a \u03b2-galactosidebinding lectin, in human monocytes and macrophages","volume":"147","author":"Liu","year":"1995","journal-title":"Am. J. Pathol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1016\/j.autrev.2009.11.016","article-title":"Scent of dying cells: the role of attraction signals in the clearance of apoptotic cells and its immunological consequences","volume":"9","author":"Mu\u00f1oz","year":"2010","journal-title":"Autoimmun. Rev."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1038\/417182a","article-title":"Identification of a factor that links apoptotic cells to phagocytes","volume":"417","author":"Hanayama","year":"2002","journal-title":"Nature"},{"key":"2023032914004198400_","first-page":"452","article-title":"Intraperitoneal injection of lipopolysaccharide induces dynamic migration of Gr-1high polymorphonuclear neutrophils in the murine abdominal cavity","volume":"11","author":"Miyazaki","year":"2004","journal-title":"Clin. Diagn. Lab. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"943","DOI":"10.1038\/sj.cdd.4401421","article-title":"Milk fat globule epidermal growth factor 8 (MFG-E8) binds to oxidized phosphatidylserine: implications for macrophage clearance of apoptotic cells","volume":"11","author":"Borisenko","year":"2004","journal-title":"Cell Death Differ."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"947","DOI":"10.1111\/j.1476-5381.2009.00386.x","article-title":"Lipoxins: resolutionary road","volume":"158","author":"Maderna","year":"2009","journal-title":"Br. J. Pharmacol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"4595","DOI":"10.4049\/jimmunol.178.7.4595","article-title":"Annexin-1 and peptide derivatives are released by apoptotic cells and stimulate phagocytosis of apoptotic neutrophils by macrophages","volume":"178","author":"Scannell","year":"2007","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1084\/jem.20081880","article-title":"Maresins: novel macrophage mediators with potent antiinflammatory and proresolving actions","volume":"206","author":"Serhan","year":"2009","journal-title":"J. Exp. Med."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"5315","DOI":"10.4049\/jimmunol.0903378","article-title":"Chemerin peptides promote phagocytosis in a ChemR23- and Syk-dependent manner","volume":"184","author":"Cash","year":"2010","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1038\/89759","article-title":"Lipid mediator class switching during acute inflammation: signals in resolution","volume":"2","author":"Levy","year":"2001","journal-title":"Nat. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"1103","DOI":"10.1172\/JCI115409","article-title":"Lactoferrin inhibits or promotes Legionella pneumophila intracellular multiplication in nonactivated and interferon \u03b3-activated human monocytes depending upon its degree of iron saturation. Iron-lactoferrin and nonphysiologic iron chelates reverse monocyte activation against","volume":"88","author":"Byrd","year":"1991","journal-title":"Legionella pneumophila. J. Clin. Invest."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"926","DOI":"10.1128\/iai.64.3.926-932.1996","article-title":"In vitro activity of the antimicrobial peptides human and rabbit defensins and porcine leukocyte protegrin against Mycobacterium tuberculosis","volume":"64","author":"Miyakawa","year":"1996","journal-title":"Infect. Immun."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1089\/107999099314432","article-title":"CRL-1072 enhances antimycobacterial activity of human macrophages through interleukin-8","volume":"19","author":"Jagannath","year":"1999","journal-title":"J. Interferon Cytokine Res."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1034\/j.1399-3003.2000.16a20.x","article-title":"Antibacterial activity of human neutrophil peptide-1 against Mycobacterium tuberculosis H37Rv: in vitro and ex vivo study","volume":"16","author":"Sharma","year":"2000","journal-title":"Eur. Respir. J."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"1864","DOI":"10.4049\/jimmunol.177.3.1864","article-title":"Macrophages acquire neutrophil granules for antimicrobial activity against intracellular pathogens","volume":"177","author":"Tan","year":"2006","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1089\/dna.1996.15.617","article-title":"Uptake of recombinant myeloperoxidase, free or fused to Fc \u03b3, by macrophages enhances killing activity toward micro-organisms","volume":"15","author":"Tournay","year":"1996","journal-title":"DNA Cell Biol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"2750","DOI":"10.1128\/IAI.66.6.2750-2754.1998","article-title":"Augmentation of human macrophage candidacidal capacity by recombinant human myeloperoxidase and granulocyte-macrophage colony-stimulating factor","volume":"66","author":"Marodi","year":"1998","journal-title":"Infect. Immun."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"2375","DOI":"10.1128\/iai.62.6.2375-2378.1994","article-title":"Inhibition of intracellular Histoplasma capsulatum replication by murine macrophages that produce human defensin","volume":"62","author":"Couto","year":"1994","journal-title":"Infect. Immun."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"2692","DOI":"10.1128\/IAI.69.4.2692-2699.2001","article-title":"Antimycobacterial agent based on mRNA encoding human \u03b2-defensin 2 enables primary macrophages to restrict growth of Mycobacterium tuberculosis","volume":"69","author":"Kisich","year":"2001","journal-title":"Infect. Immun."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"3042","DOI":"10.1128\/iai.63.8.3042-3047.1995","article-title":"Exogenous myeloperoxidase enhances bacterial phagocytosis and intracellular killing by macrophages","volume":"63","author":"Lincoln","year":"1995","journal-title":"Infect. Immun."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1007\/BF01923364","article-title":"Bactericidal activity against Pseudomonas aeruginosa is acquired by cultured human monocyte-derived macrophages after uptake of myeloperoxidase","volume":"52","author":"Mathy-Hartert","year":"1996","journal-title":"Experientia"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"2276","DOI":"10.1002\/1529-0131(200010)43:10<2276::AID-ANR15>3.0.CO;2-C","article-title":"Role of macrophages in Staphylococcus aureus-induced arthritis and sepsis","volume":"43","author":"Verdrengh","year":"2000","journal-title":"Arthritis Rheum."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"2956","DOI":"10.1128\/IAI.72.5.2956-2963.2004","article-title":"Role of macrophages in host resistance to group A streptococci","volume":"72","author":"Goldmann","year":"2004","journal-title":"Infect. Immun."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1146\/annurev.micro.61.080706.093305","article-title":"Evolution of intracellular pathogens","volume":"62","author":"Casadevall","year":"2008","journal-title":"Annu. Rev. Microbiol."},{"key":"2023032914004198400_","first-page":"325","volume-title":"Inflammation: Basic Principles and Clinical Correlates Second Edition","author":"van Furth","year":"1992"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"4308","DOI":"10.4049\/jimmunol.180.6.4308","article-title":"Neutrophil chemokines KC and macrophage-inflammatory protein-2 are newly synthesized by tissue macrophages using distinct TLR signaling pathways","volume":"180","author":"De Filippo","year":"2008","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"2131","DOI":"10.1128\/jb.95.6.2131-2138.1968","article-title":"Myeloperoxidase-halide-hydrogen peroxide antibacterial system","volume":"95","author":"Klebanoff","year":"1968","journal-title":"J. Bacteriol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"2122","DOI":"10.4049\/jimmunol.0804187","article-title":"Dying and necrotic neutrophils are anti-inflammatory secondary to the release of \u03b1-defensins","volume":"183","author":"Miles","year":"2009","journal-title":"J. Immunol."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1159\/000284367","article-title":"Neutrophil apoptosis: relevance to the innate immune response and inflammatory disease","volume":"2","author":"Fox","year":"2010","journal-title":"J. Innate Immun."},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"869","DOI":"10.1038\/nature05877","article-title":"Resolvin E1 and protectin D1 activate inflammation-resolution programs","volume":"447","author":"Schwab","year":"2007","journal-title":"Nature"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"1287","DOI":"10.1038\/nature08541","article-title":"Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis","volume":"461","author":"Spite","year":"2009","journal-title":"Nature"},{"key":"2023032914004198400_","doi-asserted-by":"crossref","first-page":"3703","DOI":"10.1128\/IAI.67.8.3703-3713.1999","article-title":"Host-pathogen interactions: redefining the basic concepts of virulence and pathogenicity","volume":"67","author":"Casadevall","year":"1999","journal-title":"Infect. Immun."}],"container-title":["Journal of Leukocyte Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jleukbio\/article-pdf\/89\/5\/675\/49615934\/jlb0675.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jleukbio\/article-pdf\/89\/5\/675\/49615934\/jlb0675.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,4,2]],"date-time":"2024-04-02T04:14:27Z","timestamp":1712031267000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jleukbio\/article\/89\/5\/675\/6960281"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2010,12,17]]},"references-count":135,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2010,12,17]]},"published-print":{"date-parts":[[2010,12,17]]}},"URL":"https:\/\/doi.org\/10.1189\/jlb.0910536","relation":{},"ISSN":["0741-5400","1938-3673"],"issn-type":[{"value":"0741-5400","type":"print"},{"value":"1938-3673","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2011,5]]},"published":{"date-parts":[[2010,12,17]]}}}