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Health Sciences Research Centre

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Natural Products: Therapeutic Properties and Beyond II
Publication . Duarte, Ana Paula; Luís, Ângelo; Gallardo, Eugenia
Historically, natural products have contributed to drug discovery as a source of active molecules due to their great diversity and structural complexity. Thus, they have contributed to the development of drugs for applications in different therapeutic areas. In recent decades, there has been a paradigm shift in drug discovery strategies that has allowed for identifying new natural products that exhibit activities on therapeutic targets. Newman and Cragg studied the origin of 1330 new drugs that had been approved between 1981 and 2010 and found that 64% of them were somewhat related to natural compounds [1]. In a recent review by these same authors, it was noted that, within all of the drugs newly approved by the Food and Drug Administration between January 1981 and September 2019, compounds derived from natural products ranked second [2]. Besides the importance of the discovery of new molecules based on natural compounds, the concern today is focused on the therapeutic potential of secondary metabolites classified as drugs of abuse, such as derivatives of cannabis [3] and psilocybin [4], or even on the use of plants used ancestrally in medicine as well [5,6]. On the other hand, with the development of computational techniques, a decision has been made to study the possibilities of analyzing the pharmacological potential of natural products or their derivatives and converting these molecules into low toxicity active products. However, apart from the use of naturally occurring compounds in the field of health, they have been studied and are increasingly used in solutions, for instance in the agrochemical and food industries. After the success of the Special Issue “Natural Products: Therapeutic Properties and Beyond I”, this second edition aims to categorize the state of the art concerning scientific research on natural products, including their applications as compounds with added value to human health. This issue intends to be used as a text for academia or as a reference tool for researchers, particularly for those working in the fields of medicinal chemistry, toxicology, phytochemistry, and natural product chemistry, and for health and industry professionals.
Thyroid modulating activity of UV-B filter octylmethoxycinnamate on vascular system
Publication . Lorigo, Margarida Ferreira; Oliveira, Maria Elisa Cairrão Rodrigues; Granadeiro, Luiza Augusta Tereza Gil Breitenfeld; Antunes, Carla Patrícia Quintaneiro
Every day, an extensive and varied range of emerging contaminants encounter humans. Exposure to these endocrine-disrupting chemicals (EDCs) is not without risks and has even been associated with adverse effects on multiple human systems, including the cardiovascular system. Due to the fundamental role of thyroid hormones (TH) in vascular homeostasis, EDCs capable of disturbing thyroid homeostasis (thyroid disruptive chemicals, TDCs) may increase the risk of cardiovascular disease (CVD). However, the mechanisms underlying thyroid disruption associated with the progression or development of CVD are not fully understood. Endocrine disruption is one of the biggest concerns and, therefore, one of the most extensive research forces. Endocrine disruption comprises a diverse set of target organs, processes, and modes of action (MoA), with multiple interactions and complex actions. Periods of development, such as pregnancy, are susceptible to endocrine disruption and constitute a priority area of research. Pregnant women often use various personal care products containing UV filters. The UV-B filters are designed to protect humans against the biological effects of UV radiation. However, their use has been questioned, and some concerns of toxicity to human health have emerged, demonstrating an EDC role for some UV filters. Octylmethoxycinnamate (OMC) is one of the most used UV-B filters worldwide. However, the OMC is also an EDC that affects human health and the environment, and its use remains under intense controversy. The scientific community has given special importance to the environmental and severe effects on coral reefs and aquatic species, which led to OMC being withdrawn from the market in different countries since 2018. On the contrary, the endocrine-disrupting effects in humans have been neglected despite in vitro studies having proven effects at the estrogenic level and non-consensual effects concerning (anti)thyroid and (anti)androgenic activities. Based on the above, it is worrying that the effects of a UV filter widely used worldwide are practically unknown on human health. Within the scope of my MSc dissertation, we demonstrated that OMC acts as a rapid vasodilator of the human umbilical artery (HUA). Although this vasorelaxation has a short-term beneficial effect on the vascular system, also observed with other EDCs, in the long term, all EDCs studied impaired the main vasorelaxation mechanisms of HUA through different MoA. In the case of OMC, only one study evaluated its short-term effects on human vasculature, and the effects of its long-term exposure on human health were not known until this research. Therefore, the main objective of this doctoral thesis was to understand whether exposure to the OMC UV filter impairs human vascular function in the presence of thyroid disorders. We hypothesize that exposure to OMC has adverse effects on the human vasculature, altering the expression of different receptors involved in thyroid functions. To achieve our objective and answer our research hypothesis, various in silico (molecular docking), ex vivo, in vitro (HUA and human umbilical artery smooth muscle cells, HUASMC), and in vivo (zebrafish) approaches were outlined. The first research work analysed the effects of long-term exposure to OMC on HUA vascular homeostasis. Potential changes in the vascular responses of proteins and channels involved in contractile processes were the focus of the research. The effects of 24- hour exposure to OMC (1, 10, and 50 μmol/L) were evaluated on HUA contractile responses to serotonin (5-HT) and potassium chloride (KCl). The data showed that exposure to OMC altered HUA vascular homeostasis; therefore, its MoA was explored in more detail by studying the activity of cyclic guanosine 3’,5’–monophosphate (cGMP) and Ca2+ channels (two pathways involved in its relaxation and contraction, respectively). Prolonged exposure to OMC impaired the main vasorelaxant mechanism of HUA. Interference in the nitric oxide (NO)/soluble guanyl cyclase (sGC)/cGMP/protein kinase G (PKG) signaling pathway and modulation of L-Type voltage-operated Ca2+ channels, BKCa1.1 potassium channels (α subunit), and PKG were the MoA implicated in the decrease in the contractile response. This work demonstrated that OMC could compromise vascular homeostasis in pregnant women and may have a role in the induction of hypertensive diseases of pregnancy. The HUA is regulated mainly by local mediators (5-HT and histamine, His). Membrane receptors, such as G protein-coupled receptors, GPCR induce the effects of these mediators which, when altered, compromises maternal-foetal health. Elevated levels of 5-HT and His increased HUA reactivity/sensitivity to these vasoactive agents, increasing vascular resistance and inducing preeclampsia (PE) and gestational hypertension. On the other hand, it has been demonstrated that EDCs can activate membrane receptors and alter signal transduction. Based on the above and considering the results obtained in the first study, our second research work deepened knowledge about the effects of prolonged exposure to OMC on vascular homeostasis, evaluating the modulation of receptors involved in the contractile processes of HUA. In this work, the research focused on the activity and expression of different 5-HT and His receptors. Thus, the effects of 24-hour exposure to OMC (1, 10 and 50 μmol/L) were evaluated on the contractile responses of HUA to 5-HT and His, using different specific agonists and antagonists, namely 5-HT2A receptor agonist (AMHT), 5-HT7 receptor agonist (AS19), 5- HT1B/1D receptor agonist (L69), H1 receptor agonist (BHI), H2 receptor agonist (dimaprit) and H2 receptor antagonist (cimetidine). Our results demonstrated that exposure to OMC increased HUA reactivity to the vasoactive agents under study. Consequently, and in line with previous research, our results denote a potential role for OMC in the development of hypertensive diseases of pregnancy, such as PE or gestational hypertension. In the third research work, the effects of short- and long-term exposure to OMC were evaluated on the vasculature of pregnant women with hypothyroidism. Although it has been suggested that OMC is a TDC due to its action on thyroid hormone receptor (TR), its disruptive effects on thyroid pathologies during pregnancy have never been evaluated. Therefore, in this study, we assessed the disruptive vascular effects of OMC in hypothyroidism conditions. Computational simulations using molecular docking allowed the correlation of vascular changes with the action of OMC on TRα. Our results indicated that OMC alters the contractility patterns of HUA contracted with 5-HT, His, and KCl, possibly due to interference with 5-HT and His receptors and/or involvement of Ca2+ channels (as shown in two previous investigations, in the absence of thyroid pathologies). Molecular docking analysis confirmed OMC competition with the endogenous hormone T3 for binding to the active centre of TRα, supporting the observed vascular changes. Taken together, our data demonstrate that exposure to OMC alters the vascular reactivity of pregnant women with thyroid pathologies and, thus, may be related to an increased risk and development of cardiovascular diseases. In the fourth research work, developing zebrafish embryos were used as a model to study the effects of OMC exposure in conditions of thyroid pathologies. This work aimed to unravel whether and how the response to OMC exposure is altered by developmental hypothyroidism and hyperthyroidism simulated conditions in zebrafish developing embryos and impair their normal development. For this purpose, developmental hypothyroidism and hyperthyroidism were induced through exogenous exposure to PTU (propylthiouracil, an anti-thyroid drug) or T3 (triiodothyronine endogenous hormone), respectively. Then, embryos were exposed during 120h to OMC isolated and in binary mixture with PTU or T3. In hypo- or hyperthyroidism developmental conditions, exposure to OMC impaired the embryonic development of zebrafish through the induction of several malformations. Pericardial and yolk sac oedema, yolk sac delayed absorption, noninflation of the swim bladder, notochord curvature, and lack of pigmentation were the most prevalent malformations. Furthermore, exposure to OMC under these conditions impairs the behaviour of larvae. Altered transcription of genes related with the HPT axis found proves the TDC action of the OMC. Our findings highlight a modified OMC response in the presence of thyroid pathologies, with harmful effects in development period more sensitive to endocrine disruption, which is in line with research work III. Lastly, the fifth research work was based on the study of the molecular interactions of the OMC in the HPT axis and their implications for humans and zebrafish. This in silico research aimed to reveal the different modes of interaction of the OMC at different levels of the HPT axis, comparing it to the PTU and T3. Our results demonstrated an action of OMC at different levels on the HPT axis, with different actions depending on the target. Molecular docking analysis revealed favourable binding to the corticotrophin-releasing hormone (CRH) receptor and the TH transporter protein, transthyretin (TTR). Furthermore, competition with T3 (inverse agonist activity) was observed for TRα and TRβ. Overall, the action of OMC appears to lead to a decrease in TH, which may promote hypothyroidism. This investigation proves that the OMC acts as a TDC and offers new insights about its disruptive action on the HPT axis, capable of supporting previous investigations. In summary, this doctoral thesis analysed the effects of prolonged exposure to OMC on human vasculature for the first time. Our mechanistic and integrative in silico, ex vivo, in vitro and in vivo approaches demonstrate that OMC impairs vascular homeostasis in pregnant women with and without thyroid pathologies, acting through different molecular initiating events (MIEs) and key events (Kes). Consequently, exposure to OMC can induce the development of cardiovascular diseases. Complementation with in vivo studies made it possible to prove the action of OMC on the HPT axis since the response to OMC was altered in the presence of both thyroid pathologies. In silico studies compared its thyroid modulatory activity to that of the endogenous hormone T3 and the antithyroid drug PTU, which revealed interference at different levels in the HPT axis. Considering the agonist and antagonist actions as an endocrine disruptor, we conclude that prolonged exposure to OMC triggers pathophysiological mechanisms capable of inducing vascular changes with implications for human thyroid health.
Sulfobetaine methacrylate-coated reduced graphene oxide-IR780 hybrid nanosystems for effective cancer photothermal-photodynamic therapy
Publication . Melo, Bruna L.; Lima-Sousa, Rita; Alves, Cátia; Correia, I.J.; de Melo-Diogo, Duarte
Nanomaterials with near infrared light absorption can mediate an antitumoral photothermal-photodynamic response that is weakly affected by cancer cells’ resistance mechanisms. Such nanosystems are commonly prepared by loading photosensitizers into nanomaterials displaying photothermal capacity, followed by functionalization to achieve biological compatibility. However, the translation of these multifunctional nanomaterials has been limited by the fact that many of the photosensitizers are not responsive to near infrared light. Furthermore, the reliance on poly(ethylene glycol) for functionalizing the nanomaterials is also not ideal due to some immunogenicity reports. Herein, a novel photoeffective near infrared light-responsive nanosystem for cancer photothermal-photodynamic therapy was assembled. For such, dopamine-reduced graphene oxide was, for the first time, functionalized with sulfobetaine methacrylate-brushes, and then loaded with IR780 (IR780/SB/DOPA-rGO). This hybrid system revealed a nanometric size distribution, optimal surface charge and colloidal stability. The interaction of IR780/SB/DOPA-rGO with near infrared light prompted a temperature increase (photothermal effect) and production of singlet oxygen (photodynamic effect). In in vitro studies, the IR780/SB/DOPA-rGO per se did not elicit cytotoxicity (viability > 78 %). In contrast, the combination of IR780/SB/DOPA-rGO with near infrared light decreased breast cancer cells’ viability to just 21 %, at a very low nanomaterial dose, highlighting its potential for cancer photothermal-photodynamic therapy.
RalGPS2 na proliferação e sobrevivência de células tumorais humanas de cancro da próstata
Publication . Roque, Ana Catarina Santos; Santos, Adriana Oliveira dos; Vaz, Cátia Alexandra Vicente; Rocha, Sandra Catarina Moreira
A ativação das GTPases Ral (RalA e RalB), pertencentes a uma subfamília de proteínas Ras, é efetuada por 6 fatores de troca de nucleótidos de guanina específicos de Ral (RalGEFs). RalGPS2 (Ral GEF with PH domain and SH3 binding motif 2) é um dos membros da família de RalGEFs cuja ativação é independente da sinalização por Ras. Resultados anteriores obtidos em linhas de cancro do pulmão e um ensaio de duplohíbrido em leveduras (Santos A.O. e Camonis J., não publicado) sugeriram a hipótese de que RalGPS2 teria um papel na regulação dos co-ativadores transcricionais da via Hippo YAP/TAZ. No presente trabalho, essa hipótese foi testada silenciando RalGPS2 em células de cancro da próstata e avaliando o crescimento, a sobrevivência e a expressão de genes induzidos pela ativação de YAP/TAZ. O silenciamento de RalGPS2 por siRNA foi otimizado em células de cancro da próstata PC-3, sendo o efeito na viabilidade/proliferação celular avaliado pelo ensaio de redução de resazurina aos 5 dias após a transfeção. A percentagem de indução espontânea de apoptose e a distribuição do ciclo celular foram obtidos por citometria de fluxo após marcação das células com iodeto de propídio. A expressão de mRNA dos genes regulados por YAP/TAZ, CTGF e CYR61, assim como de RalGPS2, foi obtida por PCR quantitativo em tempo real. Adicionalmente, foi explorado o efeito do silenciamento de RalGPS2 na expressão de CTGF e CYR61 em condições de estimulação com soro fetal bovino. O silenciamento de RalGPS2 inibiu o crescimento de PC-3 (˜ 59%) e aumentou a taxa de apoptose espontânea das células. A expressão de mRNA de RalGPS2 diminuiu significativamente tanto aos 3 quanto aos 5 dias após o silenciamento, no entanto, não se detetou a diminuição da expressão dos genes CTGF e CYR61. Em conclusão, o papel de RalGPS2 no controlo da proliferação e sobrevivência de células PC-3 não parece estar associado à ativação de YAP/TAZ induzida pelo soro nesta linha celular.
Avaliação do Potencial Protetor do Acetato de Segesterona e da Sinvastatina em um Modelo In Vitro de Isquemia Cerebral
Publication . Chiangalala, Anabela; Baltazar, Graça Maria Fernandes; Santos, Adriana Oliveira dos; Ferreira, Susana Maria Alves
O Acidente Vascular Cerebral Isquémico (AVCI) ocorre quando o fluxo sanguíneo cerebral é interrompido ou diminuído devido à obstrução de uma artéria, levando consequentemente a danos no tecido cerebral. Quando não revertido rapidamente, o AVCI leva a sequelas duradouras que podem comprometer as funções motoras, cognitivas e emocionais do doente. Em lesões graves, os tratamentos existentes não são eficazes na reversão dos danos causados pelo evento isquémico, sendo crucial o desenvolvimento de novas estratégias terapêuticas. Com o presente trabalho, pretendemos avaliar o potencial efeito neuroprotetor dos fármacos acetato de segesterona, um potente agonista do recetor da progesterona, e a sinvastatina, uma estatina com ação antioxidante, num modelo in vitro de AVCI, e testar a segurança de duas novas formulações (nanoemulsão e microemulsão) para o acetato de segesterona. Para o efeito, foram usadas como modelo de AVCI culturas de córtex de rato submetidas a privação de oxigénio e de glucose. Numa primeira fase, otimizámos o modelo celular de forma a obter uma percentagem de morte celular que permitisse detetar possíveis efeitos protetores dos fármacos em estudo. A citotoxicidade foi avaliada pelo ensaio de redução do sal de tetrazólio. Posteriormente, otimizámos as condições de cultura de forma a eliminar possíveis ações protetoras endógenas, que pudessem camuflar a ação protetora dos compostos em estudo. Com este objetivo, procedemos à remoção do soro da cultura e testámos a lesão isquémica em culturas enriquecidas em neurónios, para eliminar a ação protetora dos astrócitos. Apesar destas estratégias conduzirem ao aumento da morte celular, a análise da viabilidade celular com o ensaio MTT (do inglês, Thiazolyl Blue Tetrazolium Bromide) não demonstrou efeito protetor do acetato de segesterona ou da sinvastatina em nenhuma das concentrações testadas (0,001 mM a 10000 mM para o acetato de segesterona e 0,1 mM a 10000 mM para a sinvastatina), sugerindo que o efeito protetor destes compostos, observado em estudos in vivo, pode depender da ação destes em outros alvos. A segunda parte do trabalho consistiu na análise da segurança de uma nanoemulsão e de uma microemulsão para o acetato de segesterona, tendo-se verificado que nenhuma das formulações apresentou citoxicidade nas concentrações estudadas. Concluindo, as formulações de acetato de segesterona são promissoras para uso in vivo, de modo a aumentar a biodisponibilidade do fármaco na administração intranasal. Embora não tenhamos conseguido obter os efeitos neuroprotetores pretendidos, ainda existe necessidade de efetuar mais estudos, para compreender os efeitos protetores descritos pela literatura tanto para o acetato de segesterona como da sinvastatina em AVCI, bem como o impacto da interação com outros alvos na neuroprotecção exercida por esses fármacos.

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Funding agency

Fundação para a Ciência e a Tecnologia

Funding programme

6817 - DCRRNI ID

Funding Award Number

UIDP/00709/2020

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