{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,8]],"date-time":"2026-01-08T16:15:07Z","timestamp":1767888907425,"version":"3.49.0"},"reference-count":53,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2017,11,27]],"date-time":"2017-11-27T00:00:00Z","timestamp":1511740800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004901","name":"FAPEMIG","doi-asserted-by":"crossref","award":["Universal 2014"],"award-info":[{"award-number":["Universal 2014"]}],"id":[{"id":"10.13039\/501100004901","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100003593","name":"CNPq","doi-asserted-by":"crossref","award":["INCT-DT"],"award-info":[{"award-number":["INCT-DT"]}],"id":[{"id":"10.13039\/501100003593","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0188083","type":"journal-article","created":{"date-parts":[[2017,11,27]],"date-time":"2017-11-27T18:40:38Z","timestamp":1511808038000},"page":"e0188083","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":7,"title":["Distinct Trypanosoma cruzi isolates induce activation and apoptosis of human neutrophils"],"prefix":"10.1371","volume":"12","author":[{"given":"Lu\u00edsa M. D.","family":"Magalh\u00e3es","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Agostinho","family":"Viana","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Augusto C.","family":"de Jesus","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Egler","family":"Chiari","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"L\u00facia","family":"Galv\u00e3o","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Juliana A.","family":"Gomes","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kenneth J.","family":"Gollob","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7586-9996","authenticated-orcid":true,"given":"Walderez O.","family":"Dutra","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2017,11,27]]},"reference":[{"issue":"5","key":"ref1","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":"S Yamashiro","year":"2001","journal-title":"J Leukoc Biol"},{"issue":"3\u20134","key":"ref2","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/j.imbio.2007.11.010","article-title":"Neutrophil granulocytes as host cells and transport vehicles for intracellular pathogens: Apoptosis as infection-promoting factor","volume":"213","author":"T Laskay","year":"2008","journal-title":"Immunobiology"},{"issue":"5","key":"ref3","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1016\/S0966-842X(03)00075-1","article-title":"Neutrophil granulocytes-Trojan horses for <italic>Leishmania major<\/italic> and other intracellular microbes?","volume":"11","author":"T Laskay","year":"2003","journal-title":"Trends Microbiol"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1111\/j.1600-065X.2007.00550.x","article-title":"How human neutrophils kill and degrade microbes: an integrated view","volume":"219","author":"WM Nauseef","year":"2007","journal-title":"Immunol Rev"},{"issue":"14","key":"ref5","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":"M Faurschou","year":"2003","journal-title":"Microbes Infect"},{"issue":"2","key":"ref6","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.tim.2006.11.009","article-title":"Neutrophils and intracellular pathogens: beyond phagocytosis and killing","volume":"15","author":"R Appelberg","year":"2007","journal-title":"Trends Microbiol"},{"issue":"3","key":"ref7","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1038\/nri1785","article-title":"Neutrophils and immunity: challenges and opportunities","volume":"6","author":"C Nathan","year":"2006","journal-title":"Nat Rev Immunol"},{"issue":"1","key":"ref8","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1172\/JCI0211638","article-title":"Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-beta1 secretion and the resolution of inflammation","volume":"109","author":"M-LN Huynh","year":"2002","journal-title":"J Clin Invest"},{"issue":"4","key":"ref9","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-beta, PGE2, and PAF","volume":"101","author":"VA Fadok","year":"1998","journal-title":"J Clin Invest"},{"issue":"1","key":"ref10","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.micinf.2007.09.015","article-title":"Fas\/Fas-L expression, apoptosis and low proliferative response are associated with heart failure in patients with chronic Chagas\u2019 disease","volume":"10","author":"V Rodrigues","year":"2008","journal-title":"Microbes Infect"},{"issue":"3","key":"ref11","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1371\/journal.pone.0090582","article-title":"Neutrophils increase or reduce parasite burden in <italic>Trypanosoma cruzi<\/italic>-infected macrophages, depending on host strain: Role of neutrophil elastase","volume":"9","author":"T Luna-Gomes","year":"2014","journal-title":"PLoS One"},{"issue":"9","key":"ref12","doi-asserted-by":"crossref","first-page":"1183","DOI":"10.1292\/jvms.71.1183","article-title":"Overproduction of the pro-apoptotic molecule, programmed cell death 5, in <italic>Toxoplasma gondii<\/italic> leads to increased apoptosis of host macrophages","volume":"71","author":"H Bannai","year":"2009","journal-title":"J Vet Med Sci"},{"issue":"1","key":"ref13","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1046\/j.1365-2249.2001.01657.x","article-title":"West African donors have high percentages of activated cytokine producing T cells that are prone to apoptosis","volume":"126","author":"K Kemp","year":"2001","journal-title":"Clin Exp Immunol"},{"issue":"3","key":"ref14","doi-asserted-by":"crossref","first-page":"1316","DOI":"10.2353\/ajpath.2010.090740","article-title":"Epithelial cell apoptosis facilitates <italic>Entamoeba histolytica<\/italic> infection in the gut","volume":"176","author":"SM Becker","year":"2010","journal-title":"Am J Pathol. American Society for Investigative Pathology"},{"issue":"7","key":"ref15","doi-asserted-by":"crossref","first-page":"4454","DOI":"10.4049\/jimmunol.172.7.4454","article-title":"Macrophage interactions with neutrophils regulate <italic>Leishmania major<\/italic> infection","volume":"172","author":"FL Ribeiro-Gomes","year":"2004","journal-title":"J Immunol"},{"issue":"DEC","key":"ref16","first-page":"1","article-title":"Neutrophils cast extracellular traps in response to protozoan parasites","volume":"3","author":"DS Abi Abdallah","year":"2012","journal-title":"Front Immunol"},{"issue":"3","key":"ref17","first-page":"1504","article-title":"Role of polymorphonuclear cells in Chagas\u2019 disease. I. Uptake and mechanisms of destruction of intracellular (amastigote) forms of <italic>Trypanosoma cruzi<\/italic> by human neutrophils","volume":"131","author":"F Villalta","year":"1983","journal-title":"J Immunol. United States"},{"issue":"5","key":"ref18","first-page":"1703","article-title":"Effects of human colony-stimulating factor on the uptake and destruction of a pathogenic parasite (<italic>Trypanosoma cruzi<\/italic>) by human neutrophils","volume":"137","author":"F Villalta","year":"1986","journal-title":"J Immunol. United States"},{"issue":"10","key":"ref19","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1016\/j.imbio.2012.01.014","article-title":"Impaired phagocytic capacity driven by downregulation of major phagocytosis-related cell surface molecules elicits an overall modulatory cytokine profile in neutrophils and monocytes from the indeterminate clinical form of Chagas disease","volume":"217","author":"J A S Gomes","year":"2012","journal-title":"Immunobiology. Immunobiology"},{"key":"ref20","article-title":"Epidemiology of parasitic protozoa and other pathogens","author":"M Tibayrenc","year":"1999","journal-title":"Genet Epidemiol"},{"issue":"2","key":"ref21","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1016\/j.meegid.2011.12.009","article-title":"The revised <italic>Trypanosoma cruzi<\/italic> subspecific nomenclature: Rationale, epidemiological relevance and research applications","volume":"12","author":"B Zingales","year":"2012","journal-title":"Infect Genet Evol. Elsevier B.V"},{"issue":"7","key":"ref22","doi-asserted-by":"crossref","first-page":"e0003816","DOI":"10.1371\/journal.pntd.0003816","article-title":"Differential activation of human monocytes and lymphocytes by distinct strains of <italic>Trypanosoma cruzi<\/italic>","volume":"9","author":"LMD Magalh\u00e3es","year":"2015","journal-title":"PLoS Negl Trop Dis"},{"issue":"9","key":"ref23","doi-asserted-by":"crossref","first-page":"5283","DOI":"10.1128\/IAI.72.9.5283-5291.2004","article-title":"Monocytes from patients with indeterminate and cardiac forms of Chagas\u2019 disease display distinct phenotypic and functional characteristics associated with morbidity","volume":"72","author":"PE a Souza","year":"2004","journal-title":"Infect Immun"},{"issue":"5","key":"ref24","doi-asserted-by":"crossref","first-page":"1860","DOI":"10.1182\/blood.V100.5.1860.h81702001860_1860_1868","article-title":"Role of toll-like receptor 2 (TLR2) in neutrophil activation: GM-CSF enhances TLR2 expression and TLR2-mediated interleukin 8 responses in neutrophils","volume":"100","author":"E a Kurt-Jones","year":"2002","journal-title":"Blood"},{"issue":"6","key":"ref25","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1002\/jlb.61.6.721","article-title":"Quantitation of surface CD14 on human monocytes and neutrophils","volume":"61","author":"P Antal-Szalmas","year":"1997","journal-title":"J Leukoc Biol"},{"key":"ref26","article-title":"TLR-stimulated neutrophils instruct NK Cells to trigger dendritic cell maturation and promote adaptive T cell responses","author":"RE Riise","year":"2015","journal-title":"J Immunol"},{"issue":"4","key":"ref27","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1002\/ajh.21078","article-title":"Constitutive neutrophil apoptosis: mechanisms and regulation","volume":"83","author":"HR Luo","year":"2008","journal-title":"Am J Hematol"},{"issue":"8","key":"ref28","doi-asserted-by":"crossref","first-page":"2012","DOI":"10.1182\/blood.V80.8.2012.2012","article-title":"Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products","volume":"80","author":"F Colotta","year":"1992","journal-title":"Blood"},{"issue":"Suppl 2","key":"ref29","doi-asserted-by":"crossref","first-page":"81S","DOI":"10.2967\/jnumed.107.045898","article-title":"In vivo detection of apoptosis","volume":"49","author":"FG Blankenberg","year":"2008","journal-title":"J Nucl Med"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"18542","DOI":"10.1016\/S0021-9258(17)46661-0","article-title":"Ligand Passing: The 75-kDa tumor necrosis factor (TNF) receptor recruits TNF for signaling by the 55-kDa TNF receptor","author":"LA Tartaglia","year":"1993","journal-title":"J Biol Chem"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1242\/jcs.37.1.275","article-title":"A morphological study of the interaction between <italic>Trypanosoma cruzi<\/italic> and rat eosinophils, neutrophils and macrophages in vitro","volume":"37","author":"CJ Sanderson","year":"1979","journal-title":"J Cell Sci"},{"issue":"July","key":"ref32","first-page":"2008","article-title":"Neutrophils and macrophages : the main partners of phagocyte cell systems","volume":"3","author":"MT Silva","year":"2012","journal-title":"Neutrophils and macrophages\u202f: the main partners of phagocyte cell systems"},{"key":"ref33","article-title":"Nonimmune cells contribute to crosstalk between immune cells and inflammatory mediators in the innate response to <italic>Trypanosoma cruzi<\/italic> infection","volume":"2012","author":"MP Aoki","year":"2012","journal-title":"J Parasitol Res"},{"key":"ref34","doi-asserted-by":"crossref","DOI":"10.1155\/2012\/507874","article-title":"The immune response to <italic>Trypanosoma cruzi<\/italic>: Role of toll-like receptors and perspectives for vaccine development","volume":"2012","author":"MM Rodrigues","year":"2012","journal-title":"J Parasitol Res"},{"issue":"5","key":"ref35","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0063100","article-title":"Differential use of TLR2 and TLR9 in the regulation of immune responses during the infection with <italic>Trypanosoma cruzi<\/italic>","volume":"8","author":"HD Gravina","year":"2013","journal-title":"PLoS One"},{"issue":"6","key":"ref36","doi-asserted-by":"crossref","first-page":"3515","DOI":"10.4049\/jimmunol.177.6.3515","article-title":"Cutting edge: TLR9 and TLR2 signaling together account for MyD88-dependent control of parasitemia in <italic>Trypanosoma cruzi<\/italic> infection","volume":"177","author":"A Bafica","year":"2006","journal-title":"J Immunol"},{"issue":"4","key":"ref37","doi-asserted-by":"crossref","first-page":"e1000870","DOI":"10.1371\/journal.ppat.1000870","article-title":"Impaired innate immunity in TLR4(-\/-) mice but preserved CD8+ T cell responses against <italic>Trypanosoma cruzi<\/italic> in TLR4-, TLR2-, TLR9- or Myd88-deficient mice","volume":"6","author":"A-C Oliveira","year":"2010","journal-title":"PLoS Pathog"},{"issue":"6","key":"ref38","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1038\/nri3834","article-title":"Regulation of tumour necrosis factor signalling: live or let die","volume":"15","author":"D Brenner","year":"2015","journal-title":"Nat Rev Immunol"},{"issue":"1","key":"ref39","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1186\/s12879-016-1523-1","article-title":"Immunoregulatory mechanisms in Chagas disease: modulation of apoptosis in T-cell mediated immune responses","volume":"16","author":"AT Chaves","year":"2016","journal-title":"BMC Infect Dis. BMC Infectious Diseases"},{"issue":"1","key":"ref40","first-page":"116","article-title":"Neutrophil extracellular traps in physiology and pathology","volume":"39","author":"A Manda","year":"2014","journal-title":"Cent J Immunol \/ Polish Soc Immunol Elev other Cent Immunol Soc"},{"issue":"3","key":"ref41","doi-asserted-by":"crossref","first-page":"e1004651","DOI":"10.1371\/journal.ppat.1004651","article-title":"Neutrophils: between host defence, immune modulation, and tissue injury","volume":"11","author":"P Kruger","year":"2015","journal-title":"PLOS Pathog"},{"issue":"11","key":"ref42","doi-asserted-by":"crossref","first-page":"3966","DOI":"10.1128\/IAI.00770-13","article-title":"Leishmania amazonensis amastigotes trigger neutrophil activation but resist neutrophil microbicidal mechanisms","volume":"81","author":"ED Carlsen","year":"2013","journal-title":"Infect Immun"},{"issue":"3","key":"ref43","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1016\/0022-1759(82)90130-2","article-title":"Elicitation of peritoneal polymorphonuclear neutrophils from mice","volume":"49","author":"EJ Baron","year":"1982","journal-title":"J Immunol Methods"},{"issue":"6766","key":"ref44","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1038\/35003208","article-title":"Uptake of apoptotic cells drives the growth of a pathogenic trypanosome in macrophages","volume":"403","author":"CG Freire-de-Lima","year":"2000","journal-title":"Nature (Internet)"},{"issue":"5","key":"ref45","doi-asserted-by":"crossref","first-page":"e2232","DOI":"10.1038\/cddis.2016.135","article-title":"Apoptotic CD8 T-lymphocytes disable macrophage-mediated immunity to <italic>Trypanosoma cruzi<\/italic> infection","volume":"7","author":"MP Cabral-Piccin","year":"2016","journal-title":"Cell Death Dis"},{"issue":"3","key":"ref46","first-page":"911","article-title":"Human monocyte-derived macrophage phagocytosis of senescent eosinophils undergoing apoptosis. Mediation by alpha v beta 3\/CD36\/thrombospondin recognition mechanism and lack of phlogistic response","volume":"149","author":"M Stern","year":"1996","journal-title":"Am J Pathol"},{"issue":"50","key":"ref47","doi-asserted-by":"crossref","first-page":"38376","DOI":"10.1074\/jbc.M605146200","article-title":"Apoptotic cells, through Transforming Growth Factor-beta, coordinately induce anti-inflammatory and suppress pro-inflammatory eicosanoid and NO synthesis in murine macrophages","volume":"281","author":"CG Freire-de-Lima","year":"2006","journal-title":"J Biol Chem"},{"issue":"4","key":"ref48","doi-asserted-by":"crossref","first-page":"1968","DOI":"10.4049\/jimmunol.168.4.1968","article-title":"Lipopolysaccharide induces rapid production of IL-10 by monocytes in the presence of apoptotic neutrophils","volume":"168","author":"A Byrne","year":"2002","journal-title":"J Immunol"},{"issue":"6658","key":"ref49","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1038\/37022","article-title":"Immunosuppressive effects of apoptotic cells","volume":"390","author":"RE Voll","year":"1997","journal-title":"Nature"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1093\/eurjhf\/hfp105","article-title":"Plasma concentrations of tumour necrosis factor-alpha, tumour necrosis factor-related apoptosis-inducing ligand, and FasLigand \/ CD95L in patients with Chagas cardiomyopathy correlate with left ventricular dysfunction","author":"JF Lula","year":"2009","journal-title":"Eur J Heart Fail"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1590\/S1020-49892009000100012","article-title":"Urban outbreak of acute Chagas disease in Amazon region of Brazil: four-year follow-up after treatment with benznidazole","volume":"25","author":"AYN Pinto","year":"2009","journal-title":"Rev. Pan Salud Publica"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"1397","DOI":"10.1086\/516130","article-title":"Reactivation of Chagas\u2019 Disease in Patients with AIDS: Report of Three New Cases and Review of the Literature","volume":"25","author":"MS Ferreira","year":"1997","journal-title":"Clin Infect Dis"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1086\/598634","article-title":"Chagas disease in patients with kidney transplant: 7 years of experience, 1989\u20131996","volume":"29","author":"A Riarte","year":"1999","journal-title":"Cin Infect Dis"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0188083","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,8,29]],"date-time":"2023-08-29T09:18:51Z","timestamp":1693300731000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0188083"}},"subtitle":[],"editor":[{"given":"Herbert B.","family":"Tanowitz","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2017,11,27]]},"references-count":53,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2017,11,27]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0188083","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,11,27]]}}}