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Dissertação Apresentada No Programa De Pós-Graduação Em INSTITUTO NACIONAL DE PESQUISAS DA AMAZÔNIA – INPA PROGRAMA DE PÓS-GRADUAÇÃO EM GENÉTICA, CONSERVAÇÃO E BIOLOGIA EVOLUTIVA - GCBEv EXPRESSÃO DO GENE HIF-1α DURANTE A EXPOSIÇÃO DO CICLÍDEO Astronotus crassipinnis (Heckel, 1840) À HIPÓXIA WALDIR HEINRICHS CALDAS MANAUS/ AM Junho de 2016 WALDIR HEINRICHS CALDAS Expressão do gene HIF-1α durante a exposição do Ciclídeo Astronotus crassipinnis (Heckel, 1840) à hipóxia Orientador: Dra. Vera Maria Fonseca de Almeida-Val Dissertação apresentada no Programa de Pós-Graduação em Genética, Conservação e Biologia Evolutiva (INPA-PPG GCBEv) como parte dos requisitos para a obtenção do título de mestre em Ciências Biológicas, Área de Concentração em Genética, Conservação e Biologia Evolutiva . MANAUS/ AM Junho de 2016 vC145 Caldas, Waldir Heinrichs Expressão do gene HIF-1a durante a exposição do ciclídeo Astronotus crassipinnis (Heckel, 1840) à hipóxia / Waldir Heirichs Caldas. --- Manaus: [s.n.], 2016. ix, 38 f.: il. Dissertação (Mestrado) --- INPA, Manaus, 2016. Orientadora: Vera Maria Fonseca de Almeida e Val Área de concentração: Genética, Conservação e Biologia Evolutiva 1. Acará-açu. 2. Hipóxia. 3. Expressão génica. I. Título. CDD 597.5 SINOPSE: Este trabalho apresenta as variações na expressão do gene HIF-1α em dois tecidos do cichlideo Astronotus crasspinnis exposto à hipóxia, onde se observou um aumento na expressão no fígado, em relação ao controle, enquanto no músculo não houve variação. Estes resultados de expressão condizem com os observados no perfil metabólicos destes dois tecidos e com os resultados da respiração deste animal, demonstrando que este animal ativa seu metabolismo anaeróbico e reduz o aeróbico durante hipóxia, com fortes relações entre a expressão do gene HIF-1α e a inibição da atividade da LDH. Palavras-chave: Hipóxia; Astronotus crasspinnis; Expressão gênica; Metabolismo; Atividade enzimática; LDH. i À minha mãe, Eva de Oliveira Heinrichs Caldas, eterna melhor amiga. ii Agradecimentos À professora Dra. Vera Val por sua orientação, atenção, direcionamento e por sempre trazer estímulo e motivação aos seus alunos. Ao professor Dr. Adalberto Val por sua liderença e exemplo, sempre nos ensinando os caminhos necessários para sermos grandes pesquisadores. À minha “mãezona”, Eva de Oliveira Heinrichs Caldas, por todo amor, companheirismo, ensinamento e incentivo, sendo fundamental para o meu crescimento pessoal e profissional. Ao meu pai, Waldir Caldas Junior, por ser sempre meu amigo, me guiar e ensinar os caminhos da vida, sendo a todo momento um exemplo de “pai de família”, sempre presente nas minhas derrotas e vitórias. À minha noiva e amiga, Allana Negreiros, minha princesa que tanto me incentiva e, com muita paciência, abranda todos meus temores acadêmicos. Sem você nada teria sentido. Ao meu grande amigo, Derek Campos, por toda a ajuda no planejamento e na execução desse projeto, por todas nossas conversas de bar, onde sempre planejamos os trabalhos futuros que vão revolucionar a ciência. À “Naza”, Nazaré Paula, por toda paciência, “puxões de orelha” e ajuda diária fundamental para a execução e conclusão desse trabalho. À minha amiga, Susana Braz, que apesar de gostar de mim “só às vezes”, sempre é uma boa companheira e sempre traz uma grande contribuição intelectual. À toda equipe do LEEM por todos os debates, seminários e conversas de bastidor, além de estar sempre disponível para ajudar com experimentos e análises. A todos meus amigos envolvidos direta e indiretamente na realização desse projeto, incluindo os amigos da turma do GCBEv/2014. Ao INPA por toda a estutura disponível e aos professores e à equipe da coordenação do curso de Genética, Conservação e Biologia Evolutiva, pelo constante interesse na manutenção e evolução do curso. À CAPES, ao CNPq e à FAPEAM pelo financiamento do projeto ADAPTA que custeou esse projeto. iii À FAPEAM pela concessão da bolsa de estudo durante a realização deste projeto. iv “As coisas são semelhantes: isto faz a ciência possível; as coisas são diferentes: isso faz a ciência necessária” (Levins e Lewontin, 1985) v HIF-1α expression during hypoxia exposure and recover of the Amazon cichlid Astronotus crasspinnis (Heckel, 1840) ABSTRACT The aquatic habitats of the Amazon basin present deep oxygen level variation, and many aquatic animals developed biochemical and physiological adaptations to survive such changes. The advanced teleost Astronotus crassipinnis is tolerant to hypoxia and has the ability to depress its metabolic rate (oxygen consumption) and to increase its anaerobic activity when exposed to hypoxia episodes. Hypoxia-inducible factor-1α (HIF-1α) is the first gene related to hypoxia-tolerance, being regulated under these circumstances to maintain regular cellular function and control anaerobic metabolism. In the present work we studied HIF-1α expression and correlated the gene expression with changes in the metabolism of Astronotus crassipinnis exposed to 1, 3, and 5 hours of hypoxia, followed by 3 hours of recovery. The results show that A. crassipinnis presents metabolic depression under hypoxia and increases its anaerobic metabolism, and differentially regulates this gene in each of the studied tissues, with positive relationship with its metabolic profile, suggesting that HIF-1α might be the main factor to regulate responses to hypoxia tolerance. vi Expressão do gene HIF-1α durante a exposição do ciclídeo Astronotus crassipinnis (Heckel, 1840) à hipóxia RESUMO Os ambientes aquáticos da Amazônia apresentam variações profundas, diárias e sazonais, nos níveis de oxigênio. Com isso, vários animais aquáticos desenvolveram adaptações bioquímicas e fisiológicas para sobreviver em tais condições. Astronotus crassipinnis é um teleósteo tolerante à hipóxia e possui a habilidade de diminuir o consumo de oxigênio e aumentar o seu metabolismo anaeróbico. Hypoxia-Inducible factor (HIF) é um gene altamente relacionado à sobrevivência à hipóxia, sendo regulado nessas circunstâncias com o objetivo de manter o funcionamento celular normal e controlar o metabolismo anaeróbico. No presente estudo, foram relacionados os efeitos da expressão do gene HIF-1α com mudanças no perfil metabólico de Astronotus crassipinnis expostos a 1, 3 e 5 horas de hipóxia, seguindo um período de 3 horas de recuperação. Os resultados mostraram que esse animal deprime o seu metabolismo aeróbico e ativa o anaeróbico, aumentando a atividade da enzima LDH, regulando diferencialmente o gene HIF-1α em cada tecido estudado, com relações com seu perfil metabólico, sugerindo que esse gene pode ser um dos principais fatores na regulação de respostas à tolerância à hipóxia. vii SUMÁRIO LISTA DE FIGURAS .................................................................................................... vii LISTA DE TABELAS .................................................................................................... ix 1. Introdução ................................................................................................................. 1 1.1. A hipóxia em ambientes aquáticos ............................................................. 1 1.2. Adaptações da ictiofauna à hipóxia ............................................................ 2 1.3. HIF-1 ........................................................................................................... 4 1.4. Astronotus crassipinnis ............................................................................... 5 2. Objetivos .................................................................................................................... 8 2.1. Objetivo geral .............................................................................................. 8 2.2. Objetivos específicos .................................................................................. 8 CAPÍTULO 1 .................................................................................................................. 9 1. INTRODUCTION …………………………………………………………………..…….. 10 2. MATERIAL AND METHODS ………………………………………………………...… 12 2.1. Study Animals and Acclimation ……………………………………………… 12 2.2. Critical Oxygen Tension and Opercular Movements …………………….... 12 2.3. Experiment and Metabolites ……….…………………………………….. 13 2.4. Enzymatic Assays …………………………………………………………….. 14 2.5. Total RNA Extraction and First-Strand (cDNA) Synthesis …………...…… 14 2.6. Real-time Quantitative PCR …………………………………………………. 15 2.7. Statistical Analysis ……………………………………………………………. 15 3. RESULTS ………………………………………………………………………………… 16 3.1. Respirometry and Opercular Movements ………………………………….. 16 3.2. Metabolites and Enzymatic Activity ………………………………………… 16 3.3. LDH Inhibition Rates ................................................................................ 16 3.4. Gene Expression ……………………………………………………………… 17 4. DISCUSSION …………………………………………………………………………….. 17 5. REFERENCES …………………………………………………………………………… 22 4. Referências ............................................................................................................. 32 viii LISTA DE FÍGURAS INTRODUÇÃO Figura 1. Vista lateral do cichlidae Astronotus crassipinnis. .......................................... 6 CAPÍTULO 1. Figure 1. Opercular movement of Astronotus crassipinnis exposed to graded hypoxia (n= 7, mean ±SEM). MO2 of Astronotus crassipinnis exposed to graded hypoxia (n= 7, -1 mean ±SEM). Line shows expansion of opercular movements (1.8 mg O2 . L ± 0.036) -1 immediately before reaching PO2Crit (PO2crit = 1.26 mg.l ± 0.038). *indicates significantly difference between each O2 concentration (P<0.05)……………………….27 Figure
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