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Fragaria Vesca Leaf As a Source of Bioactive Phytochemicals - a Focus on Ellagitannins

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Joana Manuela Torres Liberal FRAGARIA VESCA LEAF AS A SOURCE OF BIOACTIVE PHYTOCHEMICALS - A FOCUS ON ELLAGITANNINS AND THEIR HUMAN MICROFLORA METABOLITES Tese de doutoramento em Ciências Farmacêuticas, Especialidade de Biologia Celular Molecular, orientada por Maria Teresa Pereira Marques Batista e Maria Teresa Teixeira Cruz Rosete e apresentada à Faculdade de Farmácia da Universidade de Coimbra Dezembro de 2015 FRAGARIA VESCA LEAF AS A SOURCE OF BIOACTIVE PHYTOCHEMICALS - A FOCUS ON ELLAGITANNINS AND THEIR HUMAN MICROFLORA METABOLITES Joana Manuela Torres Liberal Universidade de Coimbra 2015 Capa: Imagem elaborada por João Jesus. FRAGARIA VESCA LEAF AS A SOURCE OF BIOACTIVE PHYTOCHEMICALS - A FOCUS ON ELLAGITANNINS AND THEIR HUMAN MICROFLORA METABOLITES Joana Manuela Torres Liberal Dissertação apresentada à Faculdade de Farmácia da Universidade de Coimbra para prestação de Provas de Doutoramento em Ciências Farmacêuticas, na Especialidade de Biologia Celular e Molecular. Este trabalho foi realizado no Centro de Neurociências e Biologia Celular e na Faculdade de Farmácia da Universidade de Coimbra, sob orientação da Doutora Maria Teresa Batista e co-orientação da Doutora Maria Teresa Cruz, ao abrigo de uma bolsa de Doutoramento SFRH/BD/72918/2010 atribuída pela Fundação para a Ciência e Tecnologia. Universidade de Coimbra 2015 Ao meu Avô Joaquim AGRADECIMENTOS Este espaço é dedicado a todos os que contribuíram para que esta dissertação fosse realizada. A todos eles expresso aqui o meu mais sincero agradecimento. Às minhas orientadoras, Doutora Teresa Batista e Doutora Teresa Cruz, pela oportunidade de trabalhar com ambas dado que são para mim uma referência e inspiração no mundo da ciência. Por todo o apoio, incentivo e por todas as sugestões e discussões que levaram à produção deste trabalho. Pela confiança e pela liberdade de acção concedidas, as quais foram decisivas para o meu desenvolvimento científico e pessoal. E por último, e não menos importante, pela amizade, por todos os momentos extra-laboratório, pelas conversas e gargalhadas, e por estarem sempre disponíveis para mim. A Carmen García-Rodríguez por haberme aceptado y recibido tan bien en el Instituto de Biología y Genética Molecular de la Universidad de Valladolid, por toda su amabilidad y ayuda. Muchas gracias también a Cris, Andrea, Patri, Maribel y Saray por su constante ayuda y buena disposición y por convertir mi paso por España en una experiencia tan agradable. Aos Directores e Chefes de Grupo dos laboratórios onde desenvolvi este trabalho, por me terem proporcionado as condições necessárias à realização deste projecto. À Doutora Anália, ao Doutor Henrique Girão, à Doutora Carla Marques e à Doutora Célia Gomes pelas sugestões e discussão deste trabalho, e pela disponibilidade, ajuda e simpatia ao longo desta etapa. A todos os elementos da Universidade de Aveiro que colaboraram na realização dos ensaios de proteómica, ao Doutor Rui Vitorino, à Doutora Rosário Domingues e ao Doutor Pedro Domingues. Aos elementos do laboratório de Farmacognosia, em particular àqueles que contribuíram para a obtenção e análise das amostras fitoquímicas, o Gustavo, a Tânia e o Doutor Artur Figueirinha, pela disponibilidade, ajuda e simpatia. Um agradecimento especial à Doutora Teresa Amaral pela disponibilidade e generosidade com que veio para o laboratório realizar e ensinar as técnicas de extracção e fraccionamento da planta usada neste estudo. Aos meus colegas e sobretudo AMIGOS do laboratório, À Ana Rufino, à Mónica, à Cátia, à Isabel, à Verinha, ao João Ferreira, à Madalena, à Joana, à Ana Silva, ao João Martins, ao Bruno, à Su e à Doutora Alexandrina. Obrigada pelo espirito de união, por toda ajuda e disponibilidade. Estou grata pelas nossas conversas mais sérias e pelas mais risonhas. Vocês fizeram com que este percurso custasse menos e fosse bem mais divertido. Obrigada por me fazerem sair do laboratório com um sorriso de orelha à orelha. Não posso ainda deixar de agradecer aos meus antigos colegas de laboratório e que ainda hoje são bons amigos, a Áurea, a Célia, o Ermelindo, a Filipa, a Joana, o João e a Paula, pelos lanchinhos e jantares e por estarem sempre por perto, mesmo os que estão mais longe. Aos meus amigos, em particular à Ana Lúcia que teve sempre uma enorme paciência para me ouvir, pela amizade incondicional e pelo apoio. À minha família, À Rita, ao Bé, ao Bruno, ao Hugo, à Tia Emília, à Bela, à Nela e a todos os outros que sempre me acompanharam e se interessaram por este meu percurso e que compreenderam as minhas ausências. À minha querida Avó Maria, obrigada por me fazeres rir e chorar de comoção e por todas as velinhas que acendeste para iluminar o meu caminho. Um agradecimento muito especial ao Nuno, que foi o meu grande apoio ao longo destes anos, partilhando as minhas alegrias e confortando-me nos momentos menos positivos. Obrigada por acreditares em mim, por aturares os meus caprichos e teimosia e por me dares força, ânimo e carinho. Contigo torna-se tudo mais simples! Acima de tudo quero agradecer aos meus pais e à minha irmã. Vocês são a minha maior inspiração. Obrigada por estarem sempre presentes, por me incentivarem, por me ouvirem e por partilharem as minhas conquistas e derrotas. Sem vocês sei que não chegaria tão longe e este projecto também é vosso! PUBLICAÇÕES The results presented in this dissertation are published, were submitted or will be submitted for publication in peer-reviewed scientific journals, as follows: Joana Liberal, Vera Francisco, Gustavo Costa, Artur Figueirinha, M. Teresa Amaral, Carla Marques, Henrique Girão, M. Celeste Lopes, M Teresa Cruz, M. Teresa Batista. (2014) Bioactivity of Fragaria vesca leaves through inflammation, proteasome and autophagy modulation. Journal of Ethnopharmacology 12/2014;158:1131-22. Joana Liberal, Gustavo Costa, Anália Carmo, Rui Vitorino, Carla Marques, M. Rosário Domingues, Pedro Domingues, Ana C. Gonçalves, Raquel Alves, Ana Bela Sarmento-Ribeiro, Henrique Girão, M. Teresa Cruz, M. Teresa Batista. (2015) Chemical characterization and cytotoxic potential of an ellagitannin-enriched fraction from Fragaria vesca leaves. Arabian Journal of Chemistry. In Press. Joana Liberal, Anália Carmo, Célia Gomes, M. Teresa Cruz, Maria Teresa Batista In vitro antiproliferative activity of the ellagitannins metabolites, urolithins, on human tumor cell lines – emphasis on UMUC3 bladder cancer cells. Submitted to Molecular Nutrition & Food Research Joana Liberal, Anália Carmo, Célia Gomes, M. Teresa Cruz, Maria Teresa Batista In vitro antiproliferative effects of urolithins on human osteosarcoma cells. Manuscript in preparation. Note: The results presented in this dissertation, included in Chapters 2-5, are formatted according to the style of the journal where the papers were published or submitted for publication, with minor modifications. TABLE OF CONTENTS Abbreviations .............................................................................................................................. 1 Resumo ....................................................................................................................................... 5 Abstract ...................................................................................................................................... 7 Chapter 1 - Introduction ............................................................................................................. 9 1.1. Use of natural products as therapeutic agents ..................................................................... 11 1.2. Plants secondary metabolites ............................................................................................... 12 1.2.1. Phenolic compounds and polyphenols ......................................................................... 12 1.2.1.1. Phenolic acids ........................................................................................................ 14 1.2.1.2. Flavonoids.............................................................................................................. 14 1.2.1.3. Tannins .................................................................................................................. 15 1.2.1.3.1. Condensed tannins ............................................................................................. 16 1.2.1.3.2. Complex tannins ................................................................................................. 16 1.2.1.3.3. Hydrolysable tannins .......................................................................................... 16 1.2.1.3.3.1. Gallotannins ................................................................................................ 17 1.2.1.3.3.2. Ellagitannins ................................................................................................ 18 1.3. Ellagitannins and its colonic metabolites .............................................................................. 21 1.3.1. Sources of ellagitannins................................................................................................. 21 1.3.2. Bioavailability and metabolism of ellagitannins............................................................ 22 1.3.2.1. Ellagitannin hydrolysis into ellagic acid ................................................................. 23 1.3.2.2. Ellagic acid metabolization into urolithins ............................................................ 23 1.3.3. Biological and pharmacological properties ..................................................................
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  • Comparative Transcriptome Analysis Uncovers the Regulatory Functions Of

    Comparative Transcriptome Analysis Uncovers the Regulatory Functions Of

    Bai et al. Horticulture Research (2019) 6:42 Horticulture Research https://doi.org/10.1038/s41438-019-0128-4 www.nature.com/hortres ARTICLE Open Access Comparative transcriptome analysis uncovers the regulatory functions of long noncoding RNAs in fruit development and color changes of Fragaria pentaphylla Lijun Bai1,2, Qing Chen 1,LeiyuJiang1,YuanxiuLin1,YuntianYe1,PengLiu2, Xiaorong Wang1 and Haoru Tang1 Abstract To investigate the molecular mechanism underlying fruit development and color change, comparative transcriptome analysis was employed to generate transcriptome profiles of two typical wild varieties of Fragaria pentaphylla at three fruit developmental stages (green fruit stage, turning stage, and ripe fruit stage). We identified 25,699 long noncoding RNAs (lncRNAs) derived from 25,107 loci in the F. pentaphylla fruit transcriptome, which showed distinct stage- and genotype-specific expression patterns. Time course analysis detected a large number of differentially expressed protein-coding genes and lncRNAs associated with fruit development and ripening in both of the F. pentaphylla varieties. The target genes downregulated in the late stages were enriched in terms of photosynthesis and cell wall organization or biogenesis, suggesting that lncRNAs may act as negative regulators to suppress photosynthesis and cell wall organization or biogenesis during fruit development and ripening of F. pentaphylla. Pairwise comparisons of two varieties at three developmental stages identified 365 differentially expressed lncRNAs in total. Functional 1234567890():,; 1234567890():,; 1234567890():,; 1234567890():,; annotation of target genes suggested that lncRNAs in F. pentaphylla may play roles in fruit color formation by regulating the expression of structural genes or regulatory factors. Construction of the regulatory network further revealed that the low expression of Fra a and CHS may be the main cause of colorless fruit in F.