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Atividades Antibacteriana E Antibiofilme De Dois Peptídeos Helicoidais: Pa-Map 1.9 E Ecdbs1r5

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Atividades Antibacteriana E Antibiofilme De Dois Peptídeos Helicoidais: Pa-Map 1.9 E Ecdbs1r5 UNIVERSIDADE DE BRASÍLIA PROGRAMA DE PÓS-GRADUAÇÃO EM PATOLOGIA MOLECULAR ATIVIDADES ANTIBACTERIANA E ANTIBIOFILME DE DOIS PEPTÍDEOS HELICOIDAIS: PA-MAP 1.9 E ECDBS1R5 Autor: Marlon Henrique e Silva Cardoso Orientador: Prof. Dr. Octávio Luiz Franco Brasília – DF Março de 2019 UNIVERSIDADE DE BRASÍLIA PROGRAMA DE PÓS-GRADUAÇÃO EM PATOLOGIA MOLECULAR ATIVIDADES ANTIBACTERIANA E ANTIBIOFILME DE DOIS PEPTÍDEOS HELICOIDAIS: PA-MAP 1.9 E ECDBS1R5 Autor: Marlon Henrique e Silva Cardoso Orientador: Prof. Dr. Octávio Luiz Franco Tese apresentada como requisito para a obtenção do Título de Doutor em Patologia Molecular pelo Programa de Pós-Graduação em Patologia Molecular - Universidade de Brasília. Área de Concentração: Bioquímica/Biofísica Brasília – DF Março de 2019 2 “Que as palavras que falo não sejam ouvidas como prece nem repetidas com fervor. Apenas respeitadas.” Oswaldo Montenegro 3 Dedico este trabalho ao(a) meu(minha) filho(a), Dan/Hinata, por representar o que há de mais importante em minha vida, sendo meu motivo diário de motivação pessoal e profissional. 4 AGRADECIMENTOS À minha companheira que escolhi para a vida, Dra. Elizabete Cândido, por todo o amor prestado, pela imensa compreensão mesmo nos momentos mais difíceis e, acima de tudo, por estar carregando o fruto do nosso relacionamento, nosso(a) filho(a) Dan/Hinata; Ao meu orientador, Prof. Dr. Octávio Luiz Franco, por ser meu maior exemplo de pesquisador, por seu dinamismo e oportunidades que tem me oferecido ao longo dos anos. Conte sempre comigo; Aos meus orientadores do Institute for Molecular Bioscience (IMB) na Austrália, Dra. Lai (Angeline) Chan e Dr. David J. Craik, por terem me acolhido em seu laboratório, pelos ensinamentos e, principalmente, por terem comprado minhas ideias de forma prestativa e humilde; Às minhas filhas de quatro patas, Luna, Frida, Amora e Sunny, por serem parte essencial de nossas vidas e por tornarem mais leve a rotina diária; À meu pai, Paulo Henrique, por todo o suporte emocional e financeiro, sempre compreendendo minhas escolhas e sendo meu porto seguro; Aos meus avós, Dora e José, por serem, sem dúvidas, aqueles que mais estiveram presentes em todas as fases da minha vida e por quem tenho imenso afeto; As minhas tias, Magda e Adriana, as quais foram minhas mães de criação, sempre me dando suporte no que fosse necessário; Aos meus primos, Gabriel e Júlia, com os quais cresci e espero poder continuar acompanhando seu desenvolvimento; À pessoa mais guerreira que já conheci até então, minha irmã, Laís Marina, meu exemplo de conquista e perseverança; À minha mãe, Edna Maria, e minha vó, Nina, por todo o carinho maternal; À meu amigo e colaborador, Dr. Nelson Gomes, por ter sido aquele que inicialmente apostou no meu potencial, me oferecendo oportunidades enquanto pesquisador, e a quem devo grande parte de meu conhecimento; Às alunas de iniciação científica, mestrado e doutorado que tenho o orgulho de coorientar, MSc. Karen Oshiro, BSc. Samilla Rezende, MSc. Beatriz Meneguetti, MSc. Gislaine de Oliveira e BSc. Raquel Orozco, por todo o esforço e, principalmente, por depositarem sua confiança em mim enquanto pesquisador; 5 Às amizades que, felizmente, surgiram em minha vida, MSc. Karen Oshiro, MSc. Esther Carvalho, MSc. Sílvia Gomes, BSc. Elizangela Barros e BSc. Samilla Rezende; À banca avaliadora, a qual é composta por pesquisadores que fizeram grande diferença na minha vida profissional ao longo da minha iniciação científica e doutorado; À todos os integrantes do S-Inova Biotech, CAPB e IMB; Aos meus colaboradores, Dr. César de la Fuente-Núñez, Dr. Marcelo Torres, Dr. Nuno Santos, MSc. Mário Felício, Dra. Sónia Gonçalves e Dr. Luciano Lião por todo o auxilio para que eu pudesse finalizar meus projetos; À CAPES, CNPq, UnB, UCDB, UCB e FAP-DF por todo o suporte financeiro. 6 RESUMO Os peptídeos antimicrobianos (PAMs) vêm sendo amplamente investigados, representando uma estratégia promissora no combate a células planctônicas e biofilmes bacterianos multirresistentes. Assim, o presente trabalho teve como objetivo a caracterização funcional e estrutural de dois PAMs helicoidais com potencial antibacteriano, antibiofilme e anti- infeccioso, denominados Pa-MAP 1.9 e EcDBS1R5. Inicialmente, foi observado que ambos os peptídeos de estudo apresentam atividades contra cepas Gram-negativas e Gram-positivas, susceptíveis e resistentes, sem causar hemólise ou comprometer a viabilidade de linhagens celulares saudáveis proveniente de mamíferos. Em adição, o peptídeo Pa-MAP 1.9 demonstrou atividade deletéria contra biofilmes a baixas concentrações (1,1-3,0 µM), resultando não somente na inibição da formação de biofilmes, como também na erradicação de biofilmes pré-formados por E. coli e Klebsiella pneumoniae KpC+. A atividade antibiofilme para EcDBS1R5 foi também confirmada, uma vez que este peptídeo reduziu o volume e altura de biofilmes de P. aeruginosa pré-formados, comprometendo também a viabilidade de células bacterianas nos biofilmes. Ademais, o potencial anti-infeccioso de EcDBS1R5 foi avaliado, resultando em uma redução de 100 vezes na carga de P. aeruginosa em infecções cutâneas. Ensaios in vivo com o peptídeo Pa-MAP 1.9 ainda estão em andamento. Em contrapartida, o mecanismo de ação de Pa-MAP 1.9 frente a cepas de E. coli foi aqui investigado, sugerindo sua atuação em alvos intracelulares. Além disso, estudos biofísicos mostram que Pa-MAP 1.9 foi mais eficiente na interação com vesículas e membranas aniônicas (bactérias Gram-negativas), em comparação àquelas enriquecidas com colesterol (células de mamíferos). Estruturalmente, ambos os peptídeos foram submetidos a experimentos de dicroísmo circular (DC), revelando a presença de altos conteúdos de α-hélice em ambientes hidrofóbicos e aniônicos, contrário à conformações em random coil observadas em ambientes aquosos. As estruturas tridimensionais desses peptídeos foram detalhadamente estudadas e corroboram os dados de DC, reforçando a preferência conformacional em α- hélice anfipática com regiões terminais flexíveis tanto para Pa-MAP 1.9 quanto para EcDBS1R5 em ambientes que mimetizam membranas bacterianas. Dessa forma, os PAMs helicoidais aqui estudados se mostram promissores candidatos no desenvolvimento de novas ferramentas biotecnológicas contra infecções causadas por células platônicas e biofilmes bacterianos. Palavras chave: Peptídeos antimicrobianos; Desenho racional; Biofilmes; Biofísica estrutural. 7 ABSTRACT Antimicrobial peptides (AMPs) have been largely investigated, representing a promising strategy in the combat of multidrug resistant planktonic bacteria and biofilms. Thus, the present study focused on the functional and structural characterization of two helical AMPs with antibacterial, antibiofilm and anti-infective potential, denominated Pa-MAP 1.9 and EcDBS1R5. Initially, it was observed that both peptides present activities against Gram- negative and Gram-positive, susceptible and resistant strains, without causing hemolysis or compromising healthy mammalian cell lines viability. Moreover, the peptide Pa-MAP 1.9 demonstrated deleterious activities against biofilms at low concentrations (1.1-3.0 µM), resulting not only in the inhibition of biofilm formation, but also in the eradication of E. coli and K. pneumoniae KpC+ pre-formed biofilms. The antibiofilm activity for EcDBS1R5 was also confirmed, as this peptide decreased both the volume and height of pre-formed P. aeruginosa biofilms, also compromising the viability of bacterial cells within biofilms. Moreover, the anti-infective potential of EcDBS1R5 was evaluated, reducing 100-times P. aeruginosa counts in cutaneous infections. In vivo assays for Pa-MAP 1.9 are in progress. In contrast, the mechanism of action of Pa-MAP 1.9 toward E. coli was here investigated, suggesting its action on intracellular targets. Moreover, biophysical studies showed that Pa- MAP 1.9 was more efficient in interacting with anionic vesicles and membranes (Gram- negative bacteria), in comparison to those enriched with cholesterol (mammalian cells). Structurally, both peptides were submitted to circular dichroism (CD) experiments, revealing the presence of high α-helical contents in hydrophobic and anionic environments, in contrary to random coil conformations observed in hydrophilic environment. The tridimensional structures of these peptides were studied in detail and corroborate the CD data, reinforcing the conformational preference in amphipathic α-helix with flexible termini for both Pa-MAP 1.9 and EcDBS1R5 in environments that mimic bacterial membranes. Thus, the helical AMPs here studied appear as promising candidates in the development of biotechnological tools against infections caused by bacterial planktonic cells and biofilms. Keywords: Antimicrobial peptides; Rational design; Biofilms; Structural biophysics. 8 LISTA DE ILUSTRAÇÕES Figura 1. Esquema demonstrando alguns dos mecanismos de resistência bacteriana a antibióticos mais comumente relatados em cepas Gram-negativas, incluindo a atuação de β- lactamases na hidrólise do anel β-lactâmico de antibióticos, superexpressão de bombas de efluxo, redução na expressão de porinas, modificação do alvo por meio de mutações em genes específicos, bem como modificações nas propriedades físico-químicas da superfície celular. Figura do autor. ......................................................................................................................... 15 Figura 2. Desenvolvimento de biofilmes bacterianos destacando os estágios de adesão, crescimento séssil, maturação e dispersão. Figura
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