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SEARCH for BIOACTIVE COMPOUNDS from MEDICINAL PLANTS USED AS ANTIMALARIALS the Study of Momordica Balsamina L

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SEARCH for BIOACTIVE COMPOUNDS from MEDICINAL PLANTS USED AS ANTIMALARIALS the Study of Momordica Balsamina L UNIVERSIDADE DE LISBOA, FACULDADE DE FARMÁCIA SEARCH FOR BIOACTIVE COMPOUNDS FROM MEDICINAL PLANTS USED AS ANTIMALARIALS The study of Momordica balsamina L. Cátia Beatriz Almeida Ramalhete DOUTORAMENTO EM FARMÁCIA (QUÍMICA FARMACÊUTICA E TERAPÊUTICA) 2010 Universidade de Lisboa, Faculdade de Farmácia SEARCH FOR BIOACTIVE COMPOUNDS FROM MEDICINAL PLANTS USED AS ANTIMALARIALS The study of Momordica balsamina L. Cátia Beatriz Almeida Ramalhete Tese orientada por: Orientador: Professora Doutora Maria José Umbelino Ferreira Co-orientador: Professor Doutor Virgílio Estólio do Rosário Dissertação apresentada à Faculdade de Farmácia, Universidade de Lisboa, com vista à obtenção do grau de Doutor em Farmácia (Química Farmacêutica e Terapêutica) 2010 This thesis was conducted at the Medicinal Chemistry Group of the Research Institute for Medicines and Pharmaceutical Sciences (iMed.UL), Faculdade de Farmácia, Universidade de Lisboa. The financial support was provided by Fundação para a Ciência e a Tecnologia (SFH/BD/22321/2005). Dedicated to my Parents Francisco and Otelinda ABSTRACT The main goal of this dissertation was to search for new antimalarial compounds from plants used in traditional medicine. For the purpose, the claimed antimalarial properties of fifty eight extracts from fifteen plants, used in traditional medicine against malaria and/or fever, mainly in Mozambique, were evaluated against the 3D7 Plasmodium falciparum strain. The highest activity was shown by Momordica balsamina L. (Cucurbitaceae), which was selected for further studies. Bioassay-guided fractionation of the methanol extract of M. balsamina led to the isolation of fourteen new cucurbitane-type triterpenoids, along with five known cucurbitacins and one megastigmane-type nor-isoprenoid. In order to obtain a higher homologous series of compounds required for structure-activity relationships, karavilagenin C and balsaminol F were esterified using several acylating agents, yielding twenty new derivatives, named karavoates A - R, triacetylbalsaminol F and tribenzoylbalsaminol F, respectively. The chemical structures of compounds were deduced from their physical and spectroscopic data (IR, UV, MS, HRMS, 1H and 13C NMR and 2D NMR experiments - COSY, HMQC, HMBC and NOESY experiments). Some of the new compounds feature unusual oxidation patterns, reported for the first time in cucurbitane triterpenoids from plant sources, such as at C-29 (balsaminagenins A, B, balsaminols A - D, and balsaminapentaol) and C-12 (cucurbalsaminols A, B, and C). Moreover, balsaminapentaol has a 23,24-diol system coupled with an exocyclic double bond in the side chain, never found before in cucurbitane-type triterpenoids. Compounds were evaluated for their antimalarial activity against the chloroquine-sensitive (3D7) and chloroquine-resistant (Dd2) P. falciparum strains. Most of them displayed antimalarial activity. Among the natural compounds, the glycoside derivatives and karavilagenin E revealed the highest activity against both strains of P. falciparum tested, displaying IC50 < 9 μM. A strong increase in the activity was found for the majority of alkanoyl ester derivatives of karavilagenin C and balsaminol F. Triacetylbalsaminol F, and karavoates B, D, and E displayed IC50 values similar to those obtained with chloroquine, particularly against the resistant strain (IC50 ≤ 0.6 μM). However, a significant decrease of activity was observed when both positions, C-3 and C-23 of the parent compounds, were esterified with aroyl or cinnamoyl chlorides, highlighting the influence of molecular esteric effects on the antimalarial activity. Moreover, the substitution pattern of ring B seems also to play an important role in the antiplasmodial activity of compounds. The preliminary toxicity toward human cells of compounds was also investigated on breast cancer cell line, and the selectivity index was calculated. Compounds were also evaluated for their ability as MDR reversers in both cancer cells and resistant bacteria strains. In cancer cells, the anti-MDR activity was carried out in human MDR1 gene-transfected mouse lymphoma cells, by flow cytometry. Most of the compounds exhibited a strong activity when compared with the one of the positive control, verapamil, in a non-toxic concentration. Karavilagenin C showed the strongest activity, at a low concentration. Structure- activity relationships will be discussed. The presence of free hydroxyl groups at C-3 and C-23 seems to be crucial for the reversing activity. Moreover, in the checkerboard model of combination chemotherapy, the interaction between doxorubicin and most of the compounds synergistically enhanced the effect of the anticancer drug. Some of the results obtained by flow cytometry were corroborated by using a real-time fluorometric method that employs ethidium bromide. Some of the compounds were also able to inhibit, significantly, the efflux of ethidium bromide by methicillin- resistant Staphylococcus aureus highly resistant to oxacillin (MRSA COLoxa), and Enterococcus faecalis ATCC29212 strains. A good correlation between MRSA COLoxa reversal activity and the topological polar surface area of compounds was found. Keywords: Momordica balsamina; Cucurbitane-type triterpenoids; Antimalarial activity; Plasmodium falciparum; Multidrug resistance; P-glycoprotein; MDR modulators. i RESUMO Esta dissertação teve como principal objectivo o isolamento de compostos com actividade antimalárica a partir de plantas usadas na medicina tradicional. Nesse sentido, foram avaliadas as propriedades antimaláricas de cinquenta e oito extractos provenientes de quinze plantas, usadas na sua maioria em Moçambique para o tratamento da malaria e/ou febres associadas, usando a estirpe sensível 3D7 de Plasmodium falciparum. A espécie Africana Momordica balsamina L. (Cucurbitaceae) demonstrou a melhor actividade, sendo escolhida para estudos posteriores. Do fraccionamento bio-guiado do extracto metanólico da espécie M. balsamina resultaram catorze novos compostos com o esqueleto do cucurbitano, juntamente com cinco compostos conhecidos com o mesmo esqueleto e um nor-isoprenóide com o esqueleto do megastigmano. De modo a obter um número de compostos que possibilitasse a realização de estudos de relação estrutura-actividade, os compostos karavilagenina C e balsaminol F, isolados em maiores quantidades da planta, foram esterificados. Do balsaminol F, por acilação em C-3/C-7/C-23 com anidrido acético ou cloreto de benzoílo, obtiveram-se os derivados triacilados, designados por triacetilbalsaminol F e tribenzoilbalsaminol F, respectivamente. Do mesmo modo, a karavilagenina C foi esterificada com vários anidridos/cloretos de ácido, originando dezoito novos compostos (monoésteres em C-23 e diésteres em C-3/C-23) designados de karavoatos A - R. Os compostos foram isolados utilizando técnicas cromatográficas (cromatografia em coluna, cromatografia preparativa em camada fina e cromatografia líquida de alta resolução). A caracterização estrutural foi estabelecida com base nas suas características físicas e dados espectroscópicos (IV, UV, MS, HRMS e RMN unidimensional- 1H, 13C, DEPT e bidimensional- COSY, HMQC, HMBC e NOESY). Alguns dos compostos apresentaram particularidades estruturais identificadas pela primeira vez em compostos com o esqueleto do cucurbitano, isolados a partir de plantas, nomeadamente no padrão de oxidação em C-29 (balsaminageninas A, B; balsaminois A - D e balsaminapentaol) e em C-12 (cucurbalsaminois A - C). O composto balsaminapentaol apresentou igualmente, na cadeia lateral, um sistema 23,24-diol vicinal a uma dupla ligação exocíclica, identificado pela primeira vez em compostos com o esqueleto do cucurbitano. A actividade antimalárica dos compostos obtidos foi avaliada, in vitro, em dois clones de P. falciparum, um sensível 3D7 e um resistente Dd2. A maioria dos compostos demonstrou actividade antimalárica. Dos compostos isolados, as melhores actividades foram observadas para os derivados glicosilados e karavilagenina E (IC50 < 9 μM). No que diz respeito aos ésteres, verificou-se um aumento pronunciado da actividade antimalárica para a maioria dos ésteres alifáticos da karavilagenina C e triacetilbalsaminol F. Com efeito, os derivados triacetilbalsaminol F e karavoatos B, D e E demonstraram uma actividade antimalárica (IC50 ≤ 0.6 μM) comparável à obtida com a iii cloroquina, principalmente na estirpe resistente de P. falciparum. Contudo, verificou-se que, quando ambas as posições C-3 e C-23 da karavilagenina C são substituídas por grupos aroílo ou cinamoílo, é observada uma diminuição significativa da actividade antimalárica. O mesmo sucedeu no caso do derivado tribenzoílado do balsaminol F. Estes resultados evidenciam a importância de efeitos estéreos na actividade antimalárica deste grupo de compostos. É também de salientar que o padrão de substituição no anel B parece influenciar a actividade. Foi realizado um ensaio preliminar de citotoxicidade em células humanas tumorais de mama (MCF-7). Os valores de IC50 obtidos neste ensaio permitiram o cálculo do índice de selectividade (razão entre a citotoxicidade e a actividade antimalárica) para todos os compostos. Os compostos foram também avaliados no que diz respeito à sua capacidade como reversores de multirresistência em células cancerígenas. Alguns compostos foram também testados em estirpes bacterianas resistentes. Deste modo, estudou-se a actividade anti-MDR em células de linfoma de rato transfectadas com o gene humano MDR1. Neste ensaio avaliou-se, por citometria de fluxo, a acumulação intracelular
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