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Skip to content Um artigo publicado recentemente na revista Nature Communications, pesquisadores afiliados à Universidade de São Paulo (USP) descrevem o papel central desempenhado por uma enzima chamada fosfatidilinositol 3-quinase gama (PI3Kγ) na regulação da resposta imune contra o Trypanosoma cruzi, o parasita protozoário que causa a doença de Chagas. "Nossos resultados mostram que a expressão de PI3Ky aumenta durante a infecção por T. cruzi em camundongos e humanos. Isso parece ser essencial para evitar inflamação excessiva que pode prejudicar o organismo e também para controlar a parasitemia cardíaca", disse Maria Claudia da Silva, principal autor do estudo e pesquisador da Faculdade de Medicina de Ribeirão Preto da Universidade de São Paulo (FMRP-USP).
Segundo os autores, moléculas capazes de modular a via de sinalização celular mediada por essa enzima podem, no futuro, ser testadas como um tratamento para a doença de Chagas, que afeta cerca de 7 milhões de pessoas na América Latina – 2 milhões a 3 milhões apenas no Brasil.
O estudo foi realizado no Centro de Pesquisa em Doenças Inflamatórias (CRID), um dos Centros de Pesquisa, Inovação e Difusão (RIDCs) apoiado pela Fundação de Amparo à Pesquisa do Estado de São Paulo – FAPESP. Foi parte da pesquisa de mestrado e doutorado de Maria Claudia da Silva, orientada por João Santana da Silva e Thiago Mattar Cunha, professores da FMRP-USP.
Transmitido por insetos conhecidos como triatomíneos ou insetos beijadores (principalmente Triatoma infestans na América do Sul), transfusões de sangue de doadores com doença de Chagas e pela ingestão de alimentos contaminados, o T. cruzi permanece com o paciente por toda a vida. A fase aguda inicial da infecção pode ser assintomática ou causar febre, náusea, dor de cabeça, glândulas linfáticas inflamadas e dolorosas, erupção cutânea, pálpebras inchadas e fígado e baço aumentados.
Sem tratamento, complicações podem surgir anos depois na fase crônica. Os mais frequentes são o aumento do ventrículo cardíaco, que afeta aproximadamente 30% dos pacientes e tipicamente leva à insuficiência cardíaca e ao esôfago ou alargamento do cólon, que afeta até 10% dos pacientes e pode levar à perda do movimento peristáltico e à disfunção esfincteriana. A maioria das pessoas infectadas permanece assintomática, mesmo com um grande número de parasitas circulando no organismo.
"Em nosso modelo experimental, usamos uma cepa do parasita que prefere o tecido cardíaco", disse João Santana da Silva. "Os testes iniciais mostraram que camundongos deficientes em PI3Kγ desenvolveram cardiomiopatia grave na fase aguda e morreram após um curto período de tempo, mas não sabíamos por que isso aconteceu."
Em outros testes, os pesquisadores do CRID descobriram que os níveis do parasita no sangue de camundongos geneticamente modificados para não expressar PI3Kγ eram os mesmos dos camundongos selvagens, que poderiam expressar a enzima e sobreviver à infecção.
Segundo Santana da Silva, os ratos que morreram de infecção por T. cruzi deveriam ter mais parasitas em sua corrente sanguínea do que aqueles que sobreviveram. "No entanto, quando olhamos para os seus corações, descobrimos que os ratos com deficiência de PI3Kγ tinham níveis muito mais altos de parasitemia e inflamação muito mais grave [miocardite]", disse ele. "O sistema imunológico estava produzindo moléculas pró-inflamatórias de maneira descontrolada, ferindo o tecido cardíaco e, mesmo assim, não conseguia matar os parasitas eficientemente".
Macrófagos defeituosos Durante a pesquisa de doutorado de Maria Claudia da Silva, o grupo investigou como a resposta imune ao parasita é modificada pela ausência de PI3Kγ. Segundo Cunha, estudos na literatura mostram que a enzima participa de uma via de sinalização que desempenha um papel fundamental na migração de células de defesa para locais de inflamação no organismo.
No caso de infecção por T. cruzi, sob condições normais, as proteínas sinalizadoras chamadas quimiocinas são produzidas pelo parasita quando ele infecta as células hospedeiras. As quimiocinas ativam macrófagos e células dendríticas, linha de frente do sistema imunológico, que migram para o local e matam os invasores.
Embora o mecanismo de defesa não seja 100% eficiente, os pesquisadores explicaram que ele consegue manter baixos os níveis de parasitemia e que a maioria dos indivíduos infectados não apresenta sintomas durante a fase aguda.
"Nossos resultados mostram que quando a via de sinalização mediada por PI3Ky não é ativa em macrófagos, essas células de defesa perdem sua capacidade de matar os parasitas e controlar a inflamação", disse Cunha. "Para provar que o problema residia especificamente em macrófagos, usamos um modelo animal chamado knockout condicional, no qual PI3Ky está ausente apenas em macrófagos."
O grupo CRID não elucidou completamente o mecanismo, mas descobriu que sem a enzima, os macrófagos produzem menos óxido nítrico, o que é necessário para matar os parasitas e atua em conjunto com uma citocina pró-inflamatória chamada interferon gama (IFNγ).
"Se os macrófagos não expressarem PI3Kγ, eles não podem matar os parasitas mesmo na presença de IFNγ", disse Santana da Silva.
Evidências em humanos Em parceria com Edecio Cunha Neto, pesquisador da Faculdade de Medicina da USP em São Paulo (FMUSP), a equipe do CRID estudou tecidos de pacientes que desenvolveram cardiopatia na fase crônica da doença de Chagas e que foram submetidos à biópsia ou transplante cardíaco. Eles também analisaram um banco de dados contendo informações sobre todas as moléculas expressas no tecido cardíaco.
O estudo mostrou que indivíduos com níveis mais altos de PI3Kγ tinham níveis mais baixos de parasitemia cardíaca do que aqueles que expressaram menos PI3Kγ, embora ambos os grupos apresentassem miocardite. Além disso, todos tinham níveis mais elevados de PI3Ky e de todas as moléculas na via mediada por esta enzima do que os pacientes não-chagásicos com insuficiência cardíaca congestiva crônica.
"Essas descobertas sugerem que esta enzima também está envolvida no controle do parasita em humanos", disse Santana da Silva. "Em nossos experimentos in vitro, observamos que macrófagos humanos não conseguiram matar o patógeno intracelular quando infectados com o T. cruzi após o tratamento com o inibidor da PI3Kγ. Como isso acontece é algo que ainda precisamos entender."
Resultados preliminares também mostram que em pacientes que desenvolvem cardiopatia na fase crônica da infecção por T. cruzi, há uma maior incidência de polimorfismo (uma variação no gene que codifica a enzima) que pode estar associado à menor atividade da PI3Kγ em pacientes que desenvolvem doença crônica em outros órgãos, como o baço ou intestino.
"Atualmente estamos escrevendo mais um artigo em que levantamos a hipótese de que pessoas com um certo polimorfismo no gene que codifica PI3Kγ correm um risco maior de desenvolver cardiopatia na fase crônica", disse Cunha.
Outra possível linha de investigação, ele acrescentou, seria determinar se os raros casos de pacientes que morrem de miocardite súbita durante a fase aguda da doença de Chagas estão associados a níveis mais baixos de PI3Kγ, como os pesquisadores observaram em camundongos.
Santana da Silva também está interessada em investigar as vias de sinalização que modulam a produção de PI3Kγ no organismo humano.
"As drogas estão disponíveis para inibir a produção de PI3Kγ, mas não para estimulá-lo", disse ele. "Agora precisamos investigar as vias de regulação mediadas por PI3Kγ em busca de moléculas que induzem a liberação dessas substâncias. Já realizamos testes de laboratório em algumas moléculas que exibem esse tipo de ação. É ciência básica, mas existem potenciais aplicações para o controle da parasitemia nas fases aguda e crônica. "
Segundo Cunha, a ativação da enzima "não é tarefa fácil" e poderia ter implicações para outras condições patológicas. "Inibidores da via PI3Kγ estão sendo testados para o tratamento de câncer e doenças inflamatórias", disse ele.
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