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Multimodal Actions of Brown Seaweed (Ochrophyta)

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Multimodal Actions of Brown Seaweed (Ochrophyta) Mariana Nunes Barbosa MULTIMODAL ACTIONS OF BROWN SEAWEED (OCHROPHYTA) BIOACTIVE COMPOUNDS IN INFLAMMATION AND ALLERGY NETWORK Thesis for Doctor Degree in Pharmaceutical Sciences Phytochemistry and Pharmacognosy Specialty Work performed under the supervision of Professor Doctor Paula Cristina Branquinho de Andrade and co-supervision of Professor Doctor Patrícia Carla Ribeiro Valentão May 2018 Study nature, love nature, stay close to nature. It will never fail you. – Frank Lloyd Wright To my beloved family and my dear friends Work financially supported through the attribution of a Doctoral Grant (SFRH/BD/95861/2013) by the Fundação para a Ciência e a Tecnologia (FCT) under the framework of POPH – QREN – Type 4.1 – Advanced Training, funded by the Fundo Social Europeu (FSE) and by National funds of Ministério da Educação e Ciência (MEC), and by Programa de Cooperación Interreg V-A España–Portugal (POCTEP) 2014–2020 (project 0377_IBERPHENOL_6_E). VII IT IS AUTHORIZED THE REPRODUCTION OF THIS THESIS ONLY FOR RESEARCH PURPOSES, UNDER THE WRITTEN STATEMENT OF THE INTERESTED PARTY, COMMITTING ITSELF TO DO IT. VIII PUBLICATIONS PUBLICATIONS The data contained in the following works make part of this thesis. PUBLICATIONS IN INTERNATIONAL PEER-REVIEWED JOURNALS INDEXED AT THE JOURNAL CITATION REPORTS (JCR) OF THE ISI WEB OF KNOWLEDGE: 1. Barbosa M, Valentão P, Andrade PB. Bioactive compounds from macroalgae in the new millennium: Implications for neurodegenerative diseases. Mar Drugs. 2014 Sep; 12 (9): 4934–4972. 2. Barbosa M, Collado-González J, Andrade PB, Ferreres F, Valentão P, Galano JM, Durand T, Gil-Izquierdo Á. Nonenzymatic α-linolenic acid derivatives from the sea: Macroalgae as novel sources of phytoprostanes. J Agric Food Chem. 2015 Jul ;63 (28): 6466–6474. 3. Barbosa M, Valentão P, Andrade PB. Biologically active oxylipins from enzymatic and nonenzymatic routes in macroalgae. Mar Drugs. 2016 Jan; 14 (1): 23. 4. Fernandes F, Barbosa M, Oliveira AP, Azevedo IC, Sousa-Pinto I, Valentão P, Andrade PB. The pigments of kelps (Ochrophyta) as part of the flexible response to highly variable marine environments. J Appl Phycol 2016 Dec; 28 (6): 3689–3696. 5. Barbosa M, Fernandes F, Pereira DM, Azevedo IC, Sousa-Pinto I, Andrade PB, Valentão P. Fatty acid patterns of the kelps Saccharina latissima, Saccorhiza polyschides and Laminaria ochroleuca: Influence of changing environmental conditions. Arab J Chem 2017 (in press). DOI: 10.1016/j.arabjc.2017.01.015. 6. Barbosa M, Lopes G, Ferreres F, Andrade PB, Pereira DM, Gil-Izquierdo Á, Valentão P. Phlorotannin extracts from Fucales: Marine polyphenols as bioregulators engaged in inflammation-related mediators and enzymes. Algal Res 2017 Dec; 28: 1–8. 7. Lopes G, Barbosa M, Vallejo F, Gil-Izquierdo Á, Andrade PB, Valentão P, Pereira DM, Ferreres F. Profiling phlorotannins from Fucus spp. of the Northern Portuguese coastline: Chemical approach by HPLC-DAD- ESI/MSn and UPLC-ESI-QTOF/MS. Algal Res 2018 Jan; 29: 113–120. IX PUBLICATIONS 8. Barbosa M, Lopes G, Valentão P, Ferreres F, Gil-Izquierdo Á, Pereira DM, Andrade PB. Edible seaweeds’ phlorotannins in allergy: a natural multi- target approach. (Under review) 9. Barbosa M, Lopes G, Andrade PB, Valentão P. Inflammation and allergy network: The multimodal actions of brown seaweed phlorotannins. (Manuscript in preparation) BOOK CHAPTER: 1. Barbosa M, Valentão P, Andrade PB. Astaxanthin and fucoxanthin: Promising marine xanthophylls with therapeutic potential. Accepted for publication in Encyclopedia of Marine Biotechnology, Kim SK (Ed.). Wiley- Blackwell, New Jersey, USA. ORAL COMMUNICATION: 1. Barbosa M, Fernandes F, Pereira DM, Valentão P, Ferreres F, Gil- Izquierdo Á, Andrade PB. UHPLC-QqQ-MS/MS method for phytoprostane profiling in macroalgae. 11th National Meeting of Organic Chemistry and 4th Meeting of Therapeutic Chemistry. December 1–3, 2015. Porto, Portugal. POSTER COMMUNICATIONS: 1. Andrade PB, Lopes G, Barbosa M, Weber GM, Pinto E, Valentão P. Exploring seaweeds: the potential of phlorotannins. 8th ISANH Congress on Polyphenols Applications. June 5–6, 2014. Lisboa, Portugal. 2. Barbosa M, Collado-González J, Ferreres F, Valentão P, Fernandes F, Pereira DM, Gil-Izquierdo Á, Andrade PB. Non-enzymatic α-linolenic acid derivatives in macroalgae: Phytoprostane profiling. 2nd EuCheMS Congress on Green and Sustainable Chemistry (EuGSC). October 4–7, 2015. Lisboa, Portugal. X PUBLICATIONS 3. Andrade PB, Barbosa M, Lopes G, Ferreres F, Gil-Izquierdo Á, Pereira DM, Valentão P. Marine algal polyphenols: Phlorotannin-targeted extracts from Fucus spp. and their anti-inflammatory potential. XXIX International Conference on Polyphenols and 9th Tannin Conference. July 16–20, 2018. Madison, USA. XI AUTHOR STATEMENT The author declares to have afforded a major contribution to the technical execution, interpretation of the results and manuscript preparation of all works included in this thesis, with the collaboration of other coauthors. XII ACKNOWLEDGMENTS ACKNOWLEDGMENTS Accomplishing this PhD thesis would not have been possible without the contribution of several people and institutions to whom I would like to thank: To “Fundação para a Ciência e a Tecnologia” (FCT) for granting me a Doctoral scholarship (SFRH/BD/95861/2013) under the POPH – QREN – Type 4.1 – Advanced Training, funded by the European Social Fund (FSE) and by National funds from the “Ministério da Educação e Ciência”, and by Programa de Cooperación Interreg V-A España–Portugal (POCTEP) 2014–2020 (project 0377_IBERPHENOL_6_E). To Prof. Doctor Paula Cristina Branquinho de Andrade, my supervisor, for the continuous support of my PhD. I am gratefully indebted to her for accepting me in the Laboratory of Pharmacognosy of the Faculty of Pharmacy of the University of Porto and for all the years of guidance and encouragement. With her, I began my humble path in research, always as her dedicated student. I have always admired her professional journey and her charisma, which incented me to pursue the PhD. Prof. Paula consistently allowed this thesis to be my own work but steered me in the right direction whenever she thought I needed. In fact, without her valuable inputs this thesis could not have been successfully conducted. I could not have imagined having a better supervisor and mentor for my PhD. Thank you. To Prof. Doctor Patrícia Carla Ribeiro Valentão, co-supervisor of this thesis, for her uninterrupted patience and insightful recommendations. Whenever I ran into a trouble spot or had a question about my research or writing, her door was always open. Prof. Patrícia’s attention to detail drove me to be better and her hard questions incented me to widen my research from various perspectives. For all this, I would like to express my very great appreciation. To Prof. Doctor Federico Ferreres, from Centro de Edafología y Biología Aplicada del Segura (CEBAS), of Consejo Superior de Investigaciones Científicas (CSIC), Murcia, Spain, for his availability and essential contribution for the identification of phlorotannins by HPLC-DAD-ESI/MSn and UPLC-ESI-QTOF/MS. His willingness to give his time so generously has been very much appreciated. To Prof. Doctor Ángel Gil-Izquierdo, also from CEBAS-CSIC, for his assistance in conducting the UHPLC-QqQ-MS/MS analysis of phytoprostanes. XIII ACKNOWLEDGMENTS To my PhD colleagues and to all the staff of the Laboratory of Pharmacognosy of the Faculty of Pharmacy of the University of Porto, for their companionship, for the stimulating discussions and for contributing to the normal functioning of the lab and the development of this thesis. To my dear friends that even under the toughest circumstances always made me laugh. I sincerely appreciate your support. To Lara Reis, my friend of a lifetime, for her precious encouragement and unceasing support. To my family, particularly my grandmother Belmira, my uncle Serafim, my cousin Ana, my brother, and my nephew Francisco, for their care and support. To Hugo Santos, for all his dedication, understanding and care. Thank you for always being there. To my parents, for their never-ending support and unconditional love. None of this would have been possible without them. XIV ABSTRACT ABSTRACT ABSTRACT Among the wealth of biodiversity characterizing the marine environment, macroalgae, commonly addressed as seaweeds, have proved their auspicious ecological roles, as well as their chemical and biological potential. Seaweeds are an abundant and heterogenous group of photosynthetic organisms, distributed worldwide and endowed of unique molecules with high impact in food science, pharmaceutical industry, and public health. Within seaweed groups, the brown ones (Ochrophyta) stand out, as one of the most prolific producers of functional compounds. To harness the biotechnological potential of the Portuguese marine flora, several seaweed species were analyzed and explored for their chemical composition and biological activities. Moreover, as seaweed cultivation has become more widespread, there is a need to expand the knowledge on this material. Therefore, seaweeds grown in integrated multi-trophic aquaculture (IMTA) systems were also studied. A complex fatty acid profile, characterized mainly by the presence of medium and long fatty acyl chains (14–22 carbon atoms), with different degrees of unsaturation, was observed in Saccharina latissima (Linnaeus) C.E. Lane, C. Mayes, Druehl & G.W. Saunders, Saccorhiza polyschides (Lightfoot) Batters, and Laminaria ochroleuca Bachelot de la Pylaie tissues subjected to seasonal variations,
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