Rosette formation by Plasmodium vivax gametocytes favors the infection in Anopheles aquasalis

Plasmodium vivax is a public health problem and the most common type of malaria outside sub-Saharan Africa. The capacity of cytoadhesion, rosetting, and liver latent phase development could impact treatment and disease control. Although the ability to P. vivax gametocyte develop rosetting is known,...

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Main Authors: Luis Carlos Salazar Alvarez, Vanessa Carneiro Barbosa, Omaira Vera Lizcano, Djane Clarys Baia da Silva, Rosa Amélia Gonçalves Santana, Camila Fabbri, Paulo Filemon Paoluci Pimenta, Wuelton Marcelo Monteiro, Letusa Albrecht, Marcus Vinicius Guimarães de Lacerda, Fabio Trindade Maranhão Costa, Stefanie Costa Pinto Lopes
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-02-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2023.1108348/full
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author Luis Carlos Salazar Alvarez
Luis Carlos Salazar Alvarez
Luis Carlos Salazar Alvarez
Vanessa Carneiro Barbosa
Vanessa Carneiro Barbosa
Omaira Vera Lizcano
Omaira Vera Lizcano
Omaira Vera Lizcano
Djane Clarys Baia da Silva
Djane Clarys Baia da Silva
Djane Clarys Baia da Silva
Djane Clarys Baia da Silva
Djane Clarys Baia da Silva
Rosa Amélia Gonçalves Santana
Rosa Amélia Gonçalves Santana
Rosa Amélia Gonçalves Santana
Camila Fabbri
Camila Fabbri
Camila Fabbri
Paulo Filemon Paoluci Pimenta
Paulo Filemon Paoluci Pimenta
Paulo Filemon Paoluci Pimenta
Wuelton Marcelo Monteiro
Wuelton Marcelo Monteiro
Letusa Albrecht
Letusa Albrecht
Marcus Vinicius Guimarães de Lacerda
Marcus Vinicius Guimarães de Lacerda
Marcus Vinicius Guimarães de Lacerda
Fabio Trindade Maranhão Costa
Fabio Trindade Maranhão Costa
Stefanie Costa Pinto Lopes
Stefanie Costa Pinto Lopes
Stefanie Costa Pinto Lopes
author_facet Luis Carlos Salazar Alvarez
Luis Carlos Salazar Alvarez
Luis Carlos Salazar Alvarez
Vanessa Carneiro Barbosa
Vanessa Carneiro Barbosa
Omaira Vera Lizcano
Omaira Vera Lizcano
Omaira Vera Lizcano
Djane Clarys Baia da Silva
Djane Clarys Baia da Silva
Djane Clarys Baia da Silva
Djane Clarys Baia da Silva
Djane Clarys Baia da Silva
Rosa Amélia Gonçalves Santana
Rosa Amélia Gonçalves Santana
Rosa Amélia Gonçalves Santana
Camila Fabbri
Camila Fabbri
Camila Fabbri
Paulo Filemon Paoluci Pimenta
Paulo Filemon Paoluci Pimenta
Paulo Filemon Paoluci Pimenta
Wuelton Marcelo Monteiro
Wuelton Marcelo Monteiro
Letusa Albrecht
Letusa Albrecht
Marcus Vinicius Guimarães de Lacerda
Marcus Vinicius Guimarães de Lacerda
Marcus Vinicius Guimarães de Lacerda
Fabio Trindade Maranhão Costa
Fabio Trindade Maranhão Costa
Stefanie Costa Pinto Lopes
Stefanie Costa Pinto Lopes
Stefanie Costa Pinto Lopes
author_sort Luis Carlos Salazar Alvarez
collection DOAJ
description Plasmodium vivax is a public health problem and the most common type of malaria outside sub-Saharan Africa. The capacity of cytoadhesion, rosetting, and liver latent phase development could impact treatment and disease control. Although the ability to P. vivax gametocyte develop rosetting is known, it is not yet clear which role it plays during the infection and transmission process to the mosquito. Here, we used ex vivo approaches for evaluate the rosetting P. vivax gametocytes capacity and we have investigated the effect of this adhesive phenotype on the infection process in the vector Anopheles aquasalis mosquito. Rosette assays were performed in 107 isolates, and we have observed an elevated frequency of cytoadhesive phenomena (77,6%). The isolates with more than 10% of rosettes have presented a higher infection rate in Anopheles aquasalis (p=0.0252). Moreover, we found a positive correlation between the frequency of parasites in rosetting with the infection rate (p=0.0017) and intensity (p=0.0387) in the mosquito. The disruption of P. vivax rosette formation through mechanical rupture assay confirmed the previously findings, since the paired comparison showed that isolates with disrupted rosettes have a lower infection rate (p<0.0001) and intensity (p=0.0003) compared to the control group (no disruption). Herein we have demonstrated for the first time a potential effect of the rosette phenomenon on the infection process in the mosquito vector An. aquasalis, favoring its capacity and intensity of infection, thus allowing the perpetuation of the parasite cycle life.
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spelling doaj.art-2d35ca6af73f47ca9425d44afc95f6d12023-02-15T10:05:10ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882023-02-011310.3389/fcimb.2023.11083481108348Rosette formation by Plasmodium vivax gametocytes favors the infection in Anopheles aquasalisLuis Carlos Salazar Alvarez0Luis Carlos Salazar Alvarez1Luis Carlos Salazar Alvarez2Vanessa Carneiro Barbosa3Vanessa Carneiro Barbosa4Omaira Vera Lizcano5Omaira Vera Lizcano6Omaira Vera Lizcano7Djane Clarys Baia da Silva8Djane Clarys Baia da Silva9Djane Clarys Baia da Silva10Djane Clarys Baia da Silva11Djane Clarys Baia da Silva12Rosa Amélia Gonçalves Santana13Rosa Amélia Gonçalves Santana14Rosa Amélia Gonçalves Santana15Camila Fabbri16Camila Fabbri17Camila Fabbri18Paulo Filemon Paoluci Pimenta19Paulo Filemon Paoluci Pimenta20Paulo Filemon Paoluci Pimenta21Wuelton Marcelo Monteiro22Wuelton Marcelo Monteiro23Letusa Albrecht24Letusa Albrecht25Marcus Vinicius Guimarães de Lacerda26Marcus Vinicius Guimarães de Lacerda27Marcus Vinicius Guimarães de Lacerda28Fabio Trindade Maranhão Costa29Fabio Trindade Maranhão Costa30Stefanie Costa Pinto Lopes31Stefanie Costa Pinto Lopes32Stefanie Costa Pinto Lopes33Centro Internacional de Pesquisa Clínica em Malária – CIPCliM, Fundação de Medicina Tropical - Dr. Heitor Vieira Dourado (FMT-HVD), Manaus, BrazilPrograma de Pós-graduação em Medicina Tropical, Universidade do Estado do Amazonas, Manaus, BrazilLaboratory of Tropical Diseases-Prof. Dr. Luiz Jacintho da Silva, Department of Genetics, Evolution, Microbiology and Immunology, University of Campinas-UNICAMP, Campinas, BrazilCentro Internacional de Pesquisa Clínica em Malária – CIPCliM, Fundação de Medicina Tropical - Dr. Heitor Vieira Dourado (FMT-HVD), Manaus, BrazilInstituto Leônidas & Maria Deane (ILMD/Fiocruz Amazônia), Fundação Oswaldo Cruz (FIOCRUZ), Manaus, BrazilCentro Internacional de Pesquisa Clínica em Malária – CIPCliM, Fundação de Medicina Tropical - Dr. Heitor Vieira Dourado (FMT-HVD), Manaus, BrazilLaboratory of Tropical Diseases-Prof. Dr. Luiz Jacintho da Silva, Department of Genetics, Evolution, Microbiology and Immunology, University of Campinas-UNICAMP, Campinas, BrazilGrupo de investigación en Química y Biotecnología (QUIBIO), Facultad de Ciencias Básicas, Universidad Santiago de Cali, Cali, ColombiaCentro Internacional de Pesquisa Clínica em Malária – CIPCliM, Fundação de Medicina Tropical - Dr. Heitor Vieira Dourado (FMT-HVD), Manaus, BrazilPrograma de Pós-graduação em Medicina Tropical, Universidade do Estado do Amazonas, Manaus, BrazilInstituto Leônidas & Maria Deane (ILMD/Fiocruz Amazônia), Fundação Oswaldo Cruz (FIOCRUZ), Manaus, BrazilDepartamento de Saúde Coletiva, Universidade Federal do Amazonas, Manaus, BrazilUniversidade Nilton Lins, Manaus, BrazilCentro Internacional de Pesquisa Clínica em Malária – CIPCliM, Fundação de Medicina Tropical - Dr. Heitor Vieira Dourado (FMT-HVD), Manaus, BrazilPrograma de Pós-graduação em Medicina Tropical, Universidade do Estado do Amazonas, Manaus, BrazilInstituto Leônidas & Maria Deane (ILMD/Fiocruz Amazônia), Fundação Oswaldo Cruz (FIOCRUZ), Manaus, BrazilCentro Internacional de Pesquisa Clínica em Malária – CIPCliM, Fundação de Medicina Tropical - Dr. Heitor Vieira Dourado (FMT-HVD), Manaus, BrazilPrograma de Pós-graduação em Medicina Tropical, Universidade do Estado do Amazonas, Manaus, BrazilInstituto Leônidas & Maria Deane (ILMD/Fiocruz Amazônia), Fundação Oswaldo Cruz (FIOCRUZ), Manaus, BrazilCentro Internacional de Pesquisa Clínica em Malária – CIPCliM, Fundação de Medicina Tropical - Dr. Heitor Vieira Dourado (FMT-HVD), Manaus, BrazilPrograma de Pós-graduação em Medicina Tropical, Universidade do Estado do Amazonas, Manaus, BrazilInstituto de Pesquisas René Rachou (IRR/ Fiocruz Minas), FIOCRUZ, Belo Horizonte, BrazilCentro Internacional de Pesquisa Clínica em Malária – CIPCliM, Fundação de Medicina Tropical - Dr. Heitor Vieira Dourado (FMT-HVD), Manaus, BrazilPrograma de Pós-graduação em Medicina Tropical, Universidade do Estado do Amazonas, Manaus, BrazilLaboratory of Tropical Diseases-Prof. Dr. Luiz Jacintho da Silva, Department of Genetics, Evolution, Microbiology and Immunology, University of Campinas-UNICAMP, Campinas, BrazilInstituto Carlos Chagas (ICC/ Fiocruz Paraná), FIOCRUZ, Curitiba, BrazilCentro Internacional de Pesquisa Clínica em Malária – CIPCliM, Fundação de Medicina Tropical - Dr. Heitor Vieira Dourado (FMT-HVD), Manaus, BrazilPrograma de Pós-graduação em Medicina Tropical, Universidade do Estado do Amazonas, Manaus, BrazilInstituto Leônidas & Maria Deane (ILMD/Fiocruz Amazônia), Fundação Oswaldo Cruz (FIOCRUZ), Manaus, BrazilLaboratory of Tropical Diseases-Prof. Dr. Luiz Jacintho da Silva, Department of Genetics, Evolution, Microbiology and Immunology, University of Campinas-UNICAMP, Campinas, BrazilInstituto Leônidas & Maria Deane (ILMD/Fiocruz Amazônia), Fundação Oswaldo Cruz (FIOCRUZ), Manaus, BrazilCentro Internacional de Pesquisa Clínica em Malária – CIPCliM, Fundação de Medicina Tropical - Dr. Heitor Vieira Dourado (FMT-HVD), Manaus, BrazilPrograma de Pós-graduação em Medicina Tropical, Universidade do Estado do Amazonas, Manaus, BrazilInstituto Leônidas & Maria Deane (ILMD/Fiocruz Amazônia), Fundação Oswaldo Cruz (FIOCRUZ), Manaus, BrazilPlasmodium vivax is a public health problem and the most common type of malaria outside sub-Saharan Africa. The capacity of cytoadhesion, rosetting, and liver latent phase development could impact treatment and disease control. Although the ability to P. vivax gametocyte develop rosetting is known, it is not yet clear which role it plays during the infection and transmission process to the mosquito. Here, we used ex vivo approaches for evaluate the rosetting P. vivax gametocytes capacity and we have investigated the effect of this adhesive phenotype on the infection process in the vector Anopheles aquasalis mosquito. Rosette assays were performed in 107 isolates, and we have observed an elevated frequency of cytoadhesive phenomena (77,6%). The isolates with more than 10% of rosettes have presented a higher infection rate in Anopheles aquasalis (p=0.0252). Moreover, we found a positive correlation between the frequency of parasites in rosetting with the infection rate (p=0.0017) and intensity (p=0.0387) in the mosquito. The disruption of P. vivax rosette formation through mechanical rupture assay confirmed the previously findings, since the paired comparison showed that isolates with disrupted rosettes have a lower infection rate (p<0.0001) and intensity (p=0.0003) compared to the control group (no disruption). Herein we have demonstrated for the first time a potential effect of the rosette phenomenon on the infection process in the mosquito vector An. aquasalis, favoring its capacity and intensity of infection, thus allowing the perpetuation of the parasite cycle life.https://www.frontiersin.org/articles/10.3389/fcimb.2023.1108348/fullmalariagametocyterosettingcytoadhesionPlasmodium vivaxvector
spellingShingle Luis Carlos Salazar Alvarez
Luis Carlos Salazar Alvarez
Luis Carlos Salazar Alvarez
Vanessa Carneiro Barbosa
Vanessa Carneiro Barbosa
Omaira Vera Lizcano
Omaira Vera Lizcano
Omaira Vera Lizcano
Djane Clarys Baia da Silva
Djane Clarys Baia da Silva
Djane Clarys Baia da Silva
Djane Clarys Baia da Silva
Djane Clarys Baia da Silva
Rosa Amélia Gonçalves Santana
Rosa Amélia Gonçalves Santana
Rosa Amélia Gonçalves Santana
Camila Fabbri
Camila Fabbri
Camila Fabbri
Paulo Filemon Paoluci Pimenta
Paulo Filemon Paoluci Pimenta
Paulo Filemon Paoluci Pimenta
Wuelton Marcelo Monteiro
Wuelton Marcelo Monteiro
Letusa Albrecht
Letusa Albrecht
Marcus Vinicius Guimarães de Lacerda
Marcus Vinicius Guimarães de Lacerda
Marcus Vinicius Guimarães de Lacerda
Fabio Trindade Maranhão Costa
Fabio Trindade Maranhão Costa
Stefanie Costa Pinto Lopes
Stefanie Costa Pinto Lopes
Stefanie Costa Pinto Lopes
Rosette formation by Plasmodium vivax gametocytes favors the infection in Anopheles aquasalis
Frontiers in Cellular and Infection Microbiology
malaria
gametocyte
rosetting
cytoadhesion
Plasmodium vivax
vector
title Rosette formation by Plasmodium vivax gametocytes favors the infection in Anopheles aquasalis
title_full Rosette formation by Plasmodium vivax gametocytes favors the infection in Anopheles aquasalis
title_fullStr Rosette formation by Plasmodium vivax gametocytes favors the infection in Anopheles aquasalis
title_full_unstemmed Rosette formation by Plasmodium vivax gametocytes favors the infection in Anopheles aquasalis
title_short Rosette formation by Plasmodium vivax gametocytes favors the infection in Anopheles aquasalis
title_sort rosette formation by plasmodium vivax gametocytes favors the infection in anopheles aquasalis
topic malaria
gametocyte
rosetting
cytoadhesion
Plasmodium vivax
vector
url https://www.frontiersin.org/articles/10.3389/fcimb.2023.1108348/full
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