Profiling Humoral Immune Response Against Pre-Erythrocytic and Erythrocytic Antigens of Malaria Parasites Among Neotropical Primates in the Brazilian Atlantic Forest
Human malaria due to zoonotic transmission has been recorded in the Atlantic Forest, an extra-Amazonian area in Brazil, which are a challenge for malaria control. Naturally acquired humoral immune response against pre-erythrocytic and erythrocytic antigens of Neotropical primates (NP) was evaluated...
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Frontiers Media S.A.
2021-05-01
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Series: | Frontiers in Cellular and Infection Microbiology |
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Online Access: | https://www.frontiersin.org/articles/10.3389/fcimb.2021.678996/full |
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language |
English |
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author |
Gabriela Maíra Pereira de Assis Denise Anete Madureira de Alvarenga Matheus de Oliveira Costa Pereira Juan Camilo Sánchez-Arcila Anielle de Pina Costa Anielle de Pina Costa Anielle de Pina Costa Júlio César de Souza Junior Júlio César de Souza Junior Ana Julia Dutra Nunes Ana Julia Dutra Nunes Alcides Pissinatti Alcides Pissinatti Silvia Bahadian Moreira Leticia de Menezes Torres Helena Lott Costa Herlandes da Penha Tinoco Valéria do Socorro Pereira Irene da Silva Soares Taís Nóbrega de Sousa Francis Babila Ntumngia John H. Adams Flora Satiko Kano Zelinda Maria Braga Hirano Zelinda Maria Braga Hirano Cláudio Tadeu Daniel-Ribeiro Cláudio Tadeu Daniel-Ribeiro Joseli Oliveira Ferreira Luzia Helena Carvalho Cristiana Ferreira Alves de Brito |
spellingShingle |
Gabriela Maíra Pereira de Assis Denise Anete Madureira de Alvarenga Matheus de Oliveira Costa Pereira Juan Camilo Sánchez-Arcila Anielle de Pina Costa Anielle de Pina Costa Anielle de Pina Costa Júlio César de Souza Junior Júlio César de Souza Junior Ana Julia Dutra Nunes Ana Julia Dutra Nunes Alcides Pissinatti Alcides Pissinatti Silvia Bahadian Moreira Leticia de Menezes Torres Helena Lott Costa Herlandes da Penha Tinoco Valéria do Socorro Pereira Irene da Silva Soares Taís Nóbrega de Sousa Francis Babila Ntumngia John H. Adams Flora Satiko Kano Zelinda Maria Braga Hirano Zelinda Maria Braga Hirano Cláudio Tadeu Daniel-Ribeiro Cláudio Tadeu Daniel-Ribeiro Joseli Oliveira Ferreira Luzia Helena Carvalho Cristiana Ferreira Alves de Brito Profiling Humoral Immune Response Against Pre-Erythrocytic and Erythrocytic Antigens of Malaria Parasites Among Neotropical Primates in the Brazilian Atlantic Forest Frontiers in Cellular and Infection Microbiology malaria humoral response neotropical primates Atlantic forest pre-erythrocytic antigen erythrocytic antigens |
author_facet |
Gabriela Maíra Pereira de Assis Denise Anete Madureira de Alvarenga Matheus de Oliveira Costa Pereira Juan Camilo Sánchez-Arcila Anielle de Pina Costa Anielle de Pina Costa Anielle de Pina Costa Júlio César de Souza Junior Júlio César de Souza Junior Ana Julia Dutra Nunes Ana Julia Dutra Nunes Alcides Pissinatti Alcides Pissinatti Silvia Bahadian Moreira Leticia de Menezes Torres Helena Lott Costa Herlandes da Penha Tinoco Valéria do Socorro Pereira Irene da Silva Soares Taís Nóbrega de Sousa Francis Babila Ntumngia John H. Adams Flora Satiko Kano Zelinda Maria Braga Hirano Zelinda Maria Braga Hirano Cláudio Tadeu Daniel-Ribeiro Cláudio Tadeu Daniel-Ribeiro Joseli Oliveira Ferreira Luzia Helena Carvalho Cristiana Ferreira Alves de Brito |
author_sort |
Gabriela Maíra Pereira de Assis |
title |
Profiling Humoral Immune Response Against Pre-Erythrocytic and Erythrocytic Antigens of Malaria Parasites Among Neotropical Primates in the Brazilian Atlantic Forest |
title_short |
Profiling Humoral Immune Response Against Pre-Erythrocytic and Erythrocytic Antigens of Malaria Parasites Among Neotropical Primates in the Brazilian Atlantic Forest |
title_full |
Profiling Humoral Immune Response Against Pre-Erythrocytic and Erythrocytic Antigens of Malaria Parasites Among Neotropical Primates in the Brazilian Atlantic Forest |
title_fullStr |
Profiling Humoral Immune Response Against Pre-Erythrocytic and Erythrocytic Antigens of Malaria Parasites Among Neotropical Primates in the Brazilian Atlantic Forest |
title_full_unstemmed |
Profiling Humoral Immune Response Against Pre-Erythrocytic and Erythrocytic Antigens of Malaria Parasites Among Neotropical Primates in the Brazilian Atlantic Forest |
title_sort |
profiling humoral immune response against pre-erythrocytic and erythrocytic antigens of malaria parasites among neotropical primates in the brazilian atlantic forest |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Cellular and Infection Microbiology |
issn |
2235-2988 |
publishDate |
2021-05-01 |
description |
Human malaria due to zoonotic transmission has been recorded in the Atlantic Forest, an extra-Amazonian area in Brazil, which are a challenge for malaria control. Naturally acquired humoral immune response against pre-erythrocytic and erythrocytic antigens of Neotropical primates (NP) was evaluated here to improve the knowledge about the exposure of those animals to the malaria transmission and support the identification of the potential reservoirs of the disease in the Atlantic Forest. Blood samples of 154 monkeys from three areas of the Atlantic Forest were used to identify IgG antibodies against peptides of the repeat region of the major pre-erythrocytic antigen, the circumsporozoite protein (CSP), of Plasmodium vivax (PvCSP), Plasmodium brasilianum/Plasmodium malariae (Pb/PmCSP), and Plasmodium falciparum (PfCSP) by ELISA. Antibodies against erythrocytic recombinant antigens of P. vivax, Apical membrane antigen 1 (PvAMA-1), Erythrocyte binding protein 2 (PvEBP-2) and domain II of Duffy binding protein (PvDBPII) were also evaluated. Parameters, such as age, sex, PCR positivity, and captivity, potentially associated with humoral immune response were analyzed. Eighty-five percent of NP had antibodies against at least one CSP peptide, and 76% against at least one P. vivax erythrocytic antigen. A high percentage of adults compared to non-adults were seropositive and showed increased antibody levels. Neotropical primates with PCR positive for P. simium had a significantly higher frequency of positivity rate for immune response against PvEBP-2, PvDBPII and also higher antibody levels against PvDBPII, compared to PCR negative NPs for this species. Monkeys with PCR positive for P. brasilianum/P. malariae showed higher frequency of seropositivity and antibody levels against Pb/PmCSP. Levels of antibodies against Pb/PmCSP, PvEBP-2 and PvDBPII were higher in free-living than in captive monkeys from the same area. All Platyrrhine families showed antibodies against CSP peptides, however not all showed IgG against erythrocytic antigens. These findings showed a high prevalence of naturally acquired antibodies against CSP repeats in all studied areas, suggesting an intense exposure to infected-mosquitoes bites of NP from all families. However, mainly monkeys of Atelidae family showed antibodies against P. vivax erythrocytic antigens, suggesting blood infection, which might serve as potential reservoirs of malaria in the Atlantic Forest. |
topic |
malaria humoral response neotropical primates Atlantic forest pre-erythrocytic antigen erythrocytic antigens |
url |
https://www.frontiersin.org/articles/10.3389/fcimb.2021.678996/full |
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doaj-71e345f1c2d946c581fe7d2ef715e94e2021-05-13T08:05:04ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882021-05-011110.3389/fcimb.2021.678996678996Profiling Humoral Immune Response Against Pre-Erythrocytic and Erythrocytic Antigens of Malaria Parasites Among Neotropical Primates in the Brazilian Atlantic ForestGabriela Maíra Pereira de Assis0Denise Anete Madureira de Alvarenga1Matheus de Oliveira Costa Pereira2Juan Camilo Sánchez-Arcila3Anielle de Pina Costa4Anielle de Pina Costa5Anielle de Pina Costa6Júlio César de Souza Junior7Júlio César de Souza Junior8Ana Julia Dutra Nunes9Ana Julia Dutra Nunes10Alcides Pissinatti11Alcides Pissinatti12Silvia Bahadian Moreira13Leticia de Menezes Torres14Helena Lott Costa15Herlandes da Penha Tinoco16Valéria do Socorro Pereira17Irene da Silva Soares18Taís Nóbrega de Sousa19Francis Babila Ntumngia20John H. Adams21Flora Satiko Kano22Zelinda Maria Braga Hirano23Zelinda Maria Braga Hirano24Cláudio Tadeu Daniel-Ribeiro25Cláudio Tadeu Daniel-Ribeiro26Joseli Oliveira Ferreira27Luzia Helena Carvalho28Cristiana Ferreira Alves de Brito29Grupo de Pesquisa em Biologia Molecular e Imunologia da malária, Instituto René Rachou/Fiocruz Minas, Belo Horizonte, BrazilGrupo de Pesquisa em Biologia Molecular e Imunologia da malária, Instituto René Rachou/Fiocruz Minas, Belo Horizonte, BrazilGrupo de Pesquisa em Biologia Molecular e Imunologia da malária, Instituto René Rachou/Fiocruz Minas, Belo Horizonte, BrazilLaboratório de Imunoparasitologia, Instituto Oswaldo Cruz (IOC), Fiocruz, Rio de Janeiro, BrazilCentro de Pesquisa, Diagnóstico e Treinamento em Malária (CPD-Mal), Fiocruz, Rio de Janeiro, BrazilAmbulatório de Doenças febris, Instituto Nacional de Infectologia (INI), Ambulatório de Doenças Febris Agudas Fiocruz, Rio de Janeiro, BrazilCentro Universitário Serra dos Órgãos (UNIFESO), Teresópolis, BrazilCentro de Pesquisas Biológicas de Indaial, Indaial, BrazilFundação Universidade Regional de Blumenau (FURB), Blumenau, BrazilCentro de Pesquisas Biológicas de Indaial, Indaial, BrazilPrograma de conservação do Bugio Ruivo, Joinville, BrazilCentro Universitário Serra dos Órgãos (UNIFESO), Teresópolis, BrazilCentro de Primatologia do Rio de Janeiro (CPRJ), Instituto Estadual do Ambiente (INEA), Guapimirim, BrazilCentro de Primatologia do Rio de Janeiro (CPRJ), Instituto Estadual do Ambiente (INEA), Guapimirim, BrazilGrupo de Pesquisa em Biologia Molecular e Imunologia da malária, Instituto René Rachou/Fiocruz Minas, Belo Horizonte, BrazilGrupo de Pesquisa em Biologia Molecular e Imunologia da malária, Instituto René Rachou/Fiocruz Minas, Belo Horizonte, Brazil0Fundação de Parques Municipais e Zoobotânica (FPMZB), Belo Horizonte, Brazil0Fundação de Parques Municipais e Zoobotânica (FPMZB), Belo Horizonte, Brazil1Departamento de Análises Clínicas e Toxicológicas, Faculdade de Ciências Farmacêuticas, Universidade de São Paulo, São Paulo, BrazilGrupo de Pesquisa em Biologia Molecular e Imunologia da malária, Instituto René Rachou/Fiocruz Minas, Belo Horizonte, Brazil2Center for Global Health and Infectious Diseases Research, College of Public Health, University of South Florida, Tampa, FL, United States2Center for Global Health and Infectious Diseases Research, College of Public Health, University of South Florida, Tampa, FL, United StatesGrupo de Pesquisa em Biologia Molecular e Imunologia da malária, Instituto René Rachou/Fiocruz Minas, Belo Horizonte, BrazilCentro de Pesquisas Biológicas de Indaial, Indaial, BrazilFundação Universidade Regional de Blumenau (FURB), Blumenau, BrazilCentro de Pesquisa, Diagnóstico e Treinamento em Malária (CPD-Mal), Fiocruz, Rio de Janeiro, Brazil3Laboratório de Pesquisa em Malária, IOC/Fiocruz, Rio de Janeiro, BrazilLaboratório de Imunoparasitologia, Instituto Oswaldo Cruz (IOC), Fiocruz, Rio de Janeiro, BrazilGrupo de Pesquisa em Biologia Molecular e Imunologia da malária, Instituto René Rachou/Fiocruz Minas, Belo Horizonte, BrazilGrupo de Pesquisa em Biologia Molecular e Imunologia da malária, Instituto René Rachou/Fiocruz Minas, Belo Horizonte, BrazilHuman malaria due to zoonotic transmission has been recorded in the Atlantic Forest, an extra-Amazonian area in Brazil, which are a challenge for malaria control. Naturally acquired humoral immune response against pre-erythrocytic and erythrocytic antigens of Neotropical primates (NP) was evaluated here to improve the knowledge about the exposure of those animals to the malaria transmission and support the identification of the potential reservoirs of the disease in the Atlantic Forest. Blood samples of 154 monkeys from three areas of the Atlantic Forest were used to identify IgG antibodies against peptides of the repeat region of the major pre-erythrocytic antigen, the circumsporozoite protein (CSP), of Plasmodium vivax (PvCSP), Plasmodium brasilianum/Plasmodium malariae (Pb/PmCSP), and Plasmodium falciparum (PfCSP) by ELISA. Antibodies against erythrocytic recombinant antigens of P. vivax, Apical membrane antigen 1 (PvAMA-1), Erythrocyte binding protein 2 (PvEBP-2) and domain II of Duffy binding protein (PvDBPII) were also evaluated. Parameters, such as age, sex, PCR positivity, and captivity, potentially associated with humoral immune response were analyzed. Eighty-five percent of NP had antibodies against at least one CSP peptide, and 76% against at least one P. vivax erythrocytic antigen. A high percentage of adults compared to non-adults were seropositive and showed increased antibody levels. Neotropical primates with PCR positive for P. simium had a significantly higher frequency of positivity rate for immune response against PvEBP-2, PvDBPII and also higher antibody levels against PvDBPII, compared to PCR negative NPs for this species. Monkeys with PCR positive for P. brasilianum/P. malariae showed higher frequency of seropositivity and antibody levels against Pb/PmCSP. Levels of antibodies against Pb/PmCSP, PvEBP-2 and PvDBPII were higher in free-living than in captive monkeys from the same area. All Platyrrhine families showed antibodies against CSP peptides, however not all showed IgG against erythrocytic antigens. These findings showed a high prevalence of naturally acquired antibodies against CSP repeats in all studied areas, suggesting an intense exposure to infected-mosquitoes bites of NP from all families. However, mainly monkeys of Atelidae family showed antibodies against P. vivax erythrocytic antigens, suggesting blood infection, which might serve as potential reservoirs of malaria in the Atlantic Forest.https://www.frontiersin.org/articles/10.3389/fcimb.2021.678996/fullmalariahumoral responseneotropical primatesAtlantic forestpre-erythrocytic antigenerythrocytic antigens |