Heme Drives Oxidative Stress-Associated Cell Death in Human Neutrophils Infected with Leishmania infantum
| Main Author: | |
|---|---|
| Publication Date: | 2017 |
| Other Authors: | , , , , , , , , , , , , , |
| Format: | Article |
| Language: | eng |
| Source: | Repositório Institucional da FIOCRUZ (ARCA) |
| DOI: | 10.3389/fimmu.2017.01620 |
| Download full: | https://arca.fiocruz.br/handle/icict/24775 |
Summary: | Fundação de Amparo à Pesquisa do Estado da Bahia-FAPESB (RED0018/2013 to VB) and from Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq (478480/2013-0 to VB, 552721/2011-5 and 019.203.02712/2009-8 FAPITEC/CNPq to RA). RA also received a grant from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES: 23038.005304/2011-01). GQ-C received a fellowship from FAPESB. |
| id |
CRUZ_6f4f7b147d475c202cad7d8320f45e64 |
|---|---|
| oai_identifier_str |
oai:arca.fiocruz.br:icict/24775 |
| network_acronym_str |
CRUZ |
| network_name_str |
Repositório Institucional da FIOCRUZ (ARCA) |
| repository_id_str |
2135 |
| spelling |
Carvalho, Graziele QuintelaLuz, Nívea FariasCeles, Fabiana SantanaZanette, Dalila LucíolaAndrade, Daniela RodriguesMenezes, Diego SilvaTavares, Natália M.Brodskyn, Claudia IdaPrates, Deboraci BritoGonçalves, Marilda de SouzaOliveira, Camila Indiani deAlmeida, Roque Pacheco deBozza, Marcelo TorresAndrade, Bruno de BezerrilBorges, Valeria de Matos2018-02-08T14:05:11Z2018-02-08T14:05:11Z2017CARVALHO, G. Q. et al. Heme Drives Oxidative Stress-Associated Cell Death in Human Neutrophils Infected with Leishmania infantum. Frontiers in Immunology, v. 8, p.1620, 2017.1664-3224https://arca.fiocruz.br/handle/icict/2477510.3389/fimmu.2017.01620Fundação de Amparo à Pesquisa do Estado da Bahia-FAPESB (RED0018/2013 to VB) and from Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq (478480/2013-0 to VB, 552721/2011-5 and 019.203.02712/2009-8 FAPITEC/CNPq to RA). RA also received a grant from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES: 23038.005304/2011-01). GQ-C received a fellowship from FAPESB.Fundação Oswaldo Cruz. Instituto Gonçalo Moniz. Salvador, BA, Brasil / Universidade Federal da Bahia. Faculdade de Medicina. Salvador, BA, Brasil / Instituto Federal de Educação, Ciência e Tecnologia Baiano. Santa Inês, Ba, BrasilFundação Oswaldo Cruz. Instituto Gonçalo Moniz. Salvador, BA, BrasilFundação Oswaldo Cruz. Instituto Gonçalo Moniz. Salvador, BA, Brasil / Universidade Federal da Bahia. Faculdade de Medicina. Salvador, BA, BrasilFundação Oswaldo Cruz. Instituto Gonçalo Moniz. Salvador, BA, BrasilFundação Oswaldo Cruz. Instituto Gonçalo Moniz. Salvador, BA, BrasilInstituto de Tecnologia e Pesquisa. Aracaju, SE, BrasilFundação Oswaldo Cruz. Instituto Gonçalo Moniz. Salvador, BA, Brasil / Universidade Federal da Bahia. Faculdade de Medicina. Salvador, BA, BrasilFundação Oswaldo Cruz. Instituto Gonçalo Moniz. Salvador, BA, Brasil / Universidade Federal da Bahia. Faculdade de Medicina. Salvador, BA, BrasilUniversidade Federal da Bahia. Instituto de Ciências da Saúde. Departamento de Biomorfologia. Salvador, BA, BrasilFundação Oswaldo Cruz. Instituto Gonçalo Moniz. Salvador, BA, Brasil / Universidade Federal da Bahia. Faculdade de Medicina. Salvador, BA, BrasilFundação Oswaldo Cruz. Instituto Gonçalo Moniz. Salvador, BA, Brasil / Universidade Federal da Bahia. Faculdade de Medicina. Salvador, BA, BrasilUniversidade Federal de Sergipe. Hospital Universitário. Departamento de Medicina. Aracaju, SE, BrasilUniversidade Federal do Rio de Janeiro. Departamento de Imunologia. Rio de Janeiro, RJ, BrasilFundação Oswaldo Cruz. Instituto Gonçalo Moniz. Salvador, BA, Brasil / Multinational Organization Network Sponsoring Translational and Epidemiological Research Initiative. Salvador, BA, Brazil / Universidade Salvador. Laureate Universities. Salvador, BA, Brazil / Escola Bahiana de Medicina e Saúde Pública. Salvador, BA, BrasilFundação Oswaldo Cruz. Instituto Gonçalo Moniz. Salvador, BA, Brasil / Universidade Federal da Bahia. Faculdade de Medicina. Salvador, BA, BrasilFree heme is an inflammatory molecule capable of inducing migration and activation of neutrophils. Here, we examine the heme-driven oxidative stress-associated cell death mechanisms in human neutrophils infected with Leishmania infantum, an etiologic agent of visceral leishmaniasis (VL). We first performed exploratory analyses in a population of well characterized treatment-naïve VL patients as well as uninfected controls, who were part of previously reported studies. We noted a positive correlation between serum concentrations of heme with heme oxygenase-1 (HO-1) and lactate deydrogenase, as well as, a negative correlation between heme values and peripheral blood neutrophils counts. Moreover, in vitro infection with L. infantum in the presence of heme enhanced parasite burden in neutrophils, while increasing the production of reactive oxygen species and release of neutrophilic enzymes. Additional experiments demonstrated that treatment of infected neutrophils with ferrous iron (Fe+2), a key component of the heme molecule, resulted in increased parasite survival without affecting neutrophil activation status. Furthermore, stimulation of infected neutrophils with heme triggered substantial increases in HO-1 mRNA expression as well as in superoxide dismutase-1 enzymatic activity. Heme, but not Fe+2, induced oxidative stress-associated cell death. These findings indicate that heme promotes intracellular L. infantum survival via activation of neutrophil function and oxidative stress. This study opens new perspectives for the understanding of immunopathogenic mechanisms involving neutrophils in VL.engFrontiers MediaLeishmania infantumHemeFerroNeutrófilosMorte celularHeme oxigenase 1Leishmania infantumHemeIronNeutrophilsCell deathHeme oxygenase 1Heme Drives Oxidative Stress-Associated Cell Death in Human Neutrophils Infected with Leishmania infantuminfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleinfo:eu-repo/semantics/openAccessreponame:Repositório Institucional da FIOCRUZ (ARCA)instname:Fundação Oswaldo Cruz (FIOCRUZ)instacron:FIOCRUZLICENSElicense.txtlicense.txttext/plain; charset=utf-82991https://arca.fiocruz.br/bitstreams/d47b4aa0-ab15-4d78-9c3e-da42686a3433/download5a560609d32a3863062d77ff32785d58MD51falseAnonymousREADORIGINALCarvalho GQ Heme drives oxidative stress-associated....pdfCarvalho GQ Heme drives oxidative stress-associated....pdfapplication/pdf2605040https://arca.fiocruz.br/bitstreams/4ca14337-84f3-4a11-950e-f953351a654f/downloadf722a973abb1f03727da17d4145e3a82MD52trueAnonymousREADTEXTCarvalho GQ Heme drives oxidative stress-associated....pdf.txtCarvalho GQ Heme drives oxidative stress-associated....pdf.txtExtracted texttext/plain65756https://arca.fiocruz.br/bitstreams/9afc2397-f4e5-4ebf-b5ec-8e4fa0a50487/downloadf2fceedc1c91d22af4a3e1dc55e53867MD55falseAnonymousREADTHUMBNAILCarvalho GQ Heme drives oxidative stress-associated....pdf.jpgCarvalho GQ Heme drives oxidative stress-associated....pdf.jpgGenerated Thumbnailimage/jpeg5561https://arca.fiocruz.br/bitstreams/259d56fb-30e4-4d9f-b07b-57f65ea41bfd/download03f1b71c81d06e0644c9717fb271cdd3MD56falseAnonymousREADicict/247752025-07-30 01:34:29.803open.accessoai:arca.fiocruz.br:icict/24775https://arca.fiocruz.brRepositório InstitucionalPUBhttps://www.arca.fiocruz.br/oai/requestrepositorio.arca@fiocruz.bropendoar:21352025-07-30T04:34:29Repositório Institucional da FIOCRUZ (ARCA) - Fundação Oswaldo Cruz (FIOCRUZ)falseQ0VTU8ODTyBOw4NPIEVYQ0xVU0lWQSBERSBESVJFSVRPUyBBVVRPUkFJUwoKQW8gYWNlaXRhciBvcyBURVJNT1MgZSBDT05EScOHw5VFUyBkZXN0YSBDRVNTw4NPLCBvIEFVVE9SIGUvb3UgVElUVUxBUiBkZSBkaXJlaXRvcwphdXRvcmFpcyBzb2JyZSBhIE9CUkEgZGUgcXVlIHRyYXRhIGVzdGUgZG9jdW1lbnRvOgoKKDEpIENFREUgZSBUUkFOU0ZFUkUsIHRvdGFsIGUgZ3JhdHVpdGFtZW50ZSwgw6AgRklPQ1JVWiAtIEZVTkRBw4fDg08gT1NXQUxETyBDUlVaLCBlbQpjYXLDoXRlciBwZXJtYW5lbnRlLCBpcnJldm9nw6F2ZWwgZSBOw4NPIEVYQ0xVU0lWTywgdG9kb3Mgb3MgZGlyZWl0b3MgcGF0cmltb25pYWlzIE7Dg08KQ09NRVJDSUFJUyBkZSB1dGlsaXphw6fDo28gZGEgT0JSQSBhcnTDrXN0aWNhIGUvb3UgY2llbnTDrWZpY2EgaW5kaWNhZGEgYWNpbWEsIGluY2x1c2l2ZSBvcyBkaXJlaXRvcwpkZSB2b3ogZSBpbWFnZW0gdmluY3VsYWRvcyDDoCBPQlJBLCBkdXJhbnRlIHRvZG8gbyBwcmF6byBkZSBkdXJhw6fDo28gZG9zIGRpcmVpdG9zIGF1dG9yYWlzLCBlbQpxdWFscXVlciBpZGlvbWEgZSBlbSB0b2RvcyBvcyBwYcOtc2VzOwoKKDIpIEFDRUlUQSBxdWUgYSBjZXNzw6NvIHRvdGFsIG7Do28gZXhjbHVzaXZhLCBwZXJtYW5lbnRlIGUgaXJyZXZvZ8OhdmVsIGRvcyBkaXJlaXRvcyBhdXRvcmFpcwpwYXRyaW1vbmlhaXMgbsOjbyBjb21lcmNpYWlzIGRlIHV0aWxpemHDp8OjbyBkZSBxdWUgdHJhdGEgZXN0ZSBkb2N1bWVudG8gaW5jbHVpLCBleGVtcGxpZmljYXRpdmFtZW50ZSwKb3MgZGlyZWl0b3MgZGUgZGlzcG9uaWJpbGl6YcOnw6NvIGUgY29tdW5pY2HDp8OjbyBww7pibGljYSBkYSBPQlJBLCBlbSBxdWFscXVlciBtZWlvIG91IHZlw61jdWxvLAppbmNsdXNpdmUgZW0gUmVwb3NpdMOzcmlvcyBEaWdpdGFpcywgYmVtIGNvbW8gb3MgZGlyZWl0b3MgZGUgcmVwcm9kdcOnw6NvLCBleGliacOnw6NvLCBleGVjdcOnw6NvLApkZWNsYW1hw6fDo28sIHJlY2l0YcOnw6NvLCBleHBvc2nDp8OjbywgYXJxdWl2YW1lbnRvLCBpbmNsdXPDo28gZW0gYmFuY28gZGUgZGFkb3MsIHByZXNlcnZhw6fDo28sIGRpZnVzw6NvLApkaXN0cmlidWnDp8OjbywgZGl2dWxnYcOnw6NvLCBlbXByw6lzdGltbywgdHJhZHXDp8OjbywgZHVibGFnZW0sIGxlZ2VuZGFnZW0sIGluY2x1c8OjbyBlbSBub3ZhcyBvYnJhcyBvdQpjb2xldMOibmVhcywgcmV1dGlsaXphw6fDo28sIGVkacOnw6NvLCBwcm9kdcOnw6NvIGRlIG1hdGVyaWFsIGRpZMOhdGljbyBlIGN1cnNvcyBvdSBxdWFscXVlciBmb3JtYSBkZQp1dGlsaXphw6fDo28gbsOjbyBjb21lcmNpYWw7CgooMykgUkVDT05IRUNFIHF1ZSBhIGNlc3PDo28gYXF1aSBlc3BlY2lmaWNhZGEgY29uY2VkZSDDoCBGSU9DUlVaIC0gRlVOREHDh8ODTyBPU1dBTERPCkNSVVogbyBkaXJlaXRvIGRlIGF1dG9yaXphciBxdWFscXVlciBwZXNzb2Eg4oCTIGbDrXNpY2Egb3UganVyw61kaWNhLCBww7pibGljYSBvdSBwcml2YWRhLCBuYWNpb25hbCBvdQplc3RyYW5nZWlyYSDigJMgYSBhY2Vzc2FyIGUgdXRpbGl6YXIgYW1wbGFtZW50ZSBhIE9CUkEsIHNlbSBleGNsdXNpdmlkYWRlLCBwYXJhIHF1YWlzcXVlcgpmaW5hbGlkYWRlcyBuw6NvIGNvbWVyY2lhaXM7CgooNCkgREVDTEFSQSBxdWUgYSBvYnJhIMOpIGNyaWHDp8OjbyBvcmlnaW5hbCBlIHF1ZSDDqSBvIHRpdHVsYXIgZG9zIGRpcmVpdG9zIGFxdWkgY2VkaWRvcyBlIGF1dG9yaXphZG9zLApyZXNwb25zYWJpbGl6YW5kby1zZSBpbnRlZ3JhbG1lbnRlIHBlbG8gY29udGXDumRvIGUgb3V0cm9zIGVsZW1lbnRvcyBxdWUgZmF6ZW0gcGFydGUgZGEgT0JSQSwKaW5jbHVzaXZlIG9zIGRpcmVpdG9zIGRlIHZveiBlIGltYWdlbSB2aW5jdWxhZG9zIMOgIE9CUkEsIG9icmlnYW5kby1zZSBhIGluZGVuaXphciB0ZXJjZWlyb3MgcG9yCmRhbm9zLCBiZW0gY29tbyBpbmRlbml6YXIgZSByZXNzYXJjaXIgYSBGSU9DUlVaIC0gRlVOREHDh8ODTyBPU1dBTERPIENSVVogZGUKZXZlbnR1YWlzIGRlc3Blc2FzIHF1ZSB2aWVyZW0gYSBzdXBvcnRhciwgZW0gcmF6w6NvIGRlIHF1YWxxdWVyIG9mZW5zYSBhIGRpcmVpdG9zIGF1dG9yYWlzIG91CmRpcmVpdG9zIGRlIHZveiBvdSBpbWFnZW0sIHByaW5jaXBhbG1lbnRlIG5vIHF1ZSBkaXogcmVzcGVpdG8gYSBwbMOhZ2lvIGUgdmlvbGHDp8O1ZXMgZGUgZGlyZWl0b3M7CgooNSkgQUZJUk1BIHF1ZSBjb25oZWNlIGEgUG9sw610aWNhIEluc3RpdHVjaW9uYWwgZGUgQWNlc3NvIEFiZXJ0byBkYSBGSU9DUlVaIC0gRlVOREHDh8ODTwpPU1dBTERPIENSVVogZSBhcyBkaXJldHJpemVzIHBhcmEgbyBmdW5jaW9uYW1lbnRvIGRvIHJlcG9zaXTDs3JpbyBpbnN0aXR1Y2lvbmFsIEFSQ0EuCgpBIFBvbMOtdGljYSBJbnN0aXR1Y2lvbmFsIGRlIEFjZXNzbyBBYmVydG8gZGEgRklPQ1JVWiAtIEZVTkRBw4fDg08gT1NXQUxETyBDUlVaIHJlc2VydmEKZXhjbHVzaXZhbWVudGUgYW8gQVVUT1Igb3MgZGlyZWl0b3MgbW9yYWlzIGUgb3MgdXNvcyBjb21lcmNpYWlzIHNvYnJlIGFzIG9icmFzIGRlIHN1YSBhdXRvcmlhCmUvb3UgdGl0dWxhcmlkYWRlLCBzZW5kbyBvcyB0ZXJjZWlyb3MgdXN1w6FyaW9zIHJlc3BvbnPDoXZlaXMgcGVsYSBhdHJpYnVpw6fDo28gZGUgYXV0b3JpYSBlIG1hbnV0ZW7Dp8OjbwpkYSBpbnRlZ3JpZGFkZSBkYSBPQlJBIGVtIHF1YWxxdWVyIHV0aWxpemHDp8Ojby4KCkEgUG9sw610aWNhIEluc3RpdHVjaW9uYWwgZGUgQWNlc3NvIEFiZXJ0byBkYSBGSU9DUlVaIC0gRlVOREHDh8ODTyBPU1dBTERPIENSVVoKcmVzcGVpdGEgb3MgY29udHJhdG9zIGUgYWNvcmRvcyBwcmVleGlzdGVudGVzIGRvcyBBdXRvcmVzIGNvbSB0ZXJjZWlyb3MsIGNhYmVuZG8gYW9zIEF1dG9yZXMKaW5mb3JtYXIgw6AgSW5zdGl0dWnDp8OjbyBhcyBjb25kacOnw7VlcyBlIG91dHJhcyByZXN0cmnDp8O1ZXMgaW1wb3N0YXMgcG9yIGVzdGVzIGluc3RydW1lbnRvcy4K |
| dc.title.none.fl_str_mv |
Heme Drives Oxidative Stress-Associated Cell Death in Human Neutrophils Infected with Leishmania infantum |
| title |
Heme Drives Oxidative Stress-Associated Cell Death in Human Neutrophils Infected with Leishmania infantum |
| spellingShingle |
Heme Drives Oxidative Stress-Associated Cell Death in Human Neutrophils Infected with Leishmania infantum Carvalho, Graziele Quintela Leishmania infantum Heme Ferro Neutrófilos Morte celular Heme oxigenase 1 Leishmania infantum Heme Iron Neutrophils Cell death Heme oxygenase 1 |
| title_short |
Heme Drives Oxidative Stress-Associated Cell Death in Human Neutrophils Infected with Leishmania infantum |
| title_full |
Heme Drives Oxidative Stress-Associated Cell Death in Human Neutrophils Infected with Leishmania infantum |
| title_fullStr |
Heme Drives Oxidative Stress-Associated Cell Death in Human Neutrophils Infected with Leishmania infantum |
| title_full_unstemmed |
Heme Drives Oxidative Stress-Associated Cell Death in Human Neutrophils Infected with Leishmania infantum |
| title_sort |
Heme Drives Oxidative Stress-Associated Cell Death in Human Neutrophils Infected with Leishmania infantum |
| author |
Carvalho, Graziele Quintela |
| author_facet |
Carvalho, Graziele Quintela Luz, Nívea Farias Celes, Fabiana Santana Zanette, Dalila Lucíola Andrade, Daniela Rodrigues Menezes, Diego Silva Tavares, Natália M. Brodskyn, Claudia Ida Prates, Deboraci Brito Gonçalves, Marilda de Souza Oliveira, Camila Indiani de Almeida, Roque Pacheco de Bozza, Marcelo Torres Andrade, Bruno de Bezerril Borges, Valeria de Matos |
| author_role |
author |
| author2 |
Luz, Nívea Farias Celes, Fabiana Santana Zanette, Dalila Lucíola Andrade, Daniela Rodrigues Menezes, Diego Silva Tavares, Natália M. Brodskyn, Claudia Ida Prates, Deboraci Brito Gonçalves, Marilda de Souza Oliveira, Camila Indiani de Almeida, Roque Pacheco de Bozza, Marcelo Torres Andrade, Bruno de Bezerril Borges, Valeria de Matos |
| author2_role |
author author author author author author author author author author author author author author |
| dc.contributor.author.fl_str_mv |
Carvalho, Graziele Quintela Luz, Nívea Farias Celes, Fabiana Santana Zanette, Dalila Lucíola Andrade, Daniela Rodrigues Menezes, Diego Silva Tavares, Natália M. Brodskyn, Claudia Ida Prates, Deboraci Brito Gonçalves, Marilda de Souza Oliveira, Camila Indiani de Almeida, Roque Pacheco de Bozza, Marcelo Torres Andrade, Bruno de Bezerril Borges, Valeria de Matos |
| dc.subject.other.none.fl_str_mv |
Leishmania infantum Heme Ferro Neutrófilos Morte celular Heme oxigenase 1 |
| topic |
Leishmania infantum Heme Ferro Neutrófilos Morte celular Heme oxigenase 1 Leishmania infantum Heme Iron Neutrophils Cell death Heme oxygenase 1 |
| dc.subject.en.none.fl_str_mv |
Leishmania infantum Heme Iron Neutrophils Cell death Heme oxygenase 1 |
| description |
Fundação de Amparo à Pesquisa do Estado da Bahia-FAPESB (RED0018/2013 to VB) and from Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq (478480/2013-0 to VB, 552721/2011-5 and 019.203.02712/2009-8 FAPITEC/CNPq to RA). RA also received a grant from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES: 23038.005304/2011-01). GQ-C received a fellowship from FAPESB. |
| publishDate |
2017 |
| dc.date.issued.fl_str_mv |
2017 |
| dc.date.accessioned.fl_str_mv |
2018-02-08T14:05:11Z |
| dc.date.available.fl_str_mv |
2018-02-08T14:05:11Z |
| dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
| dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
| format |
article |
| status_str |
publishedVersion |
| dc.identifier.citation.fl_str_mv |
CARVALHO, G. Q. et al. Heme Drives Oxidative Stress-Associated Cell Death in Human Neutrophils Infected with Leishmania infantum. Frontiers in Immunology, v. 8, p.1620, 2017. |
| dc.identifier.uri.fl_str_mv |
https://arca.fiocruz.br/handle/icict/24775 |
| dc.identifier.issn.none.fl_str_mv |
1664-3224 |
| dc.identifier.doi.none.fl_str_mv |
10.3389/fimmu.2017.01620 |
| identifier_str_mv |
CARVALHO, G. Q. et al. Heme Drives Oxidative Stress-Associated Cell Death in Human Neutrophils Infected with Leishmania infantum. Frontiers in Immunology, v. 8, p.1620, 2017. 1664-3224 10.3389/fimmu.2017.01620 |
| url |
https://arca.fiocruz.br/handle/icict/24775 |
| dc.language.iso.fl_str_mv |
eng |
| language |
eng |
| dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
| eu_rights_str_mv |
openAccess |
| dc.publisher.none.fl_str_mv |
Frontiers Media |
| publisher.none.fl_str_mv |
Frontiers Media |
| dc.source.none.fl_str_mv |
reponame:Repositório Institucional da FIOCRUZ (ARCA) instname:Fundação Oswaldo Cruz (FIOCRUZ) instacron:FIOCRUZ |
| instname_str |
Fundação Oswaldo Cruz (FIOCRUZ) |
| instacron_str |
FIOCRUZ |
| institution |
FIOCRUZ |
| reponame_str |
Repositório Institucional da FIOCRUZ (ARCA) |
| collection |
Repositório Institucional da FIOCRUZ (ARCA) |
| bitstream.url.fl_str_mv |
https://arca.fiocruz.br/bitstreams/d47b4aa0-ab15-4d78-9c3e-da42686a3433/download https://arca.fiocruz.br/bitstreams/4ca14337-84f3-4a11-950e-f953351a654f/download https://arca.fiocruz.br/bitstreams/9afc2397-f4e5-4ebf-b5ec-8e4fa0a50487/download https://arca.fiocruz.br/bitstreams/259d56fb-30e4-4d9f-b07b-57f65ea41bfd/download |
| bitstream.checksum.fl_str_mv |
5a560609d32a3863062d77ff32785d58 f722a973abb1f03727da17d4145e3a82 f2fceedc1c91d22af4a3e1dc55e53867 03f1b71c81d06e0644c9717fb271cdd3 |
| bitstream.checksumAlgorithm.fl_str_mv |
MD5 MD5 MD5 MD5 |
| repository.name.fl_str_mv |
Repositório Institucional da FIOCRUZ (ARCA) - Fundação Oswaldo Cruz (FIOCRUZ) |
| repository.mail.fl_str_mv |
repositorio.arca@fiocruz.br |
| _version_ |
1839716383026315264 |