Influência de Quimiotipos, Íons e da Temperatura na ... · ... companhia e valiosas trocas de...

UNIVERSIDADE FEDERAL DE PERNAMBUCO - UFPE

CENTRO DE CIÊNCIAS EXATAS E DA NATUREZA – CCEN

DEPARTAMENTO DE QUÍMICA FUNDAMENTAL – dQF

PROGRAMA DE PÓS-GRADUAÇÃO EM QUÍMICA

Influência de Quimiotipos, Íons e da Temperatura na Estrutura e Dinâmica de Bicamadas de Lipídio A de

Pseudomonas aeruginosa e Escherichia coli.

Aluno: Frederico José de Santana Pontes

Orientador: Roberto D. Lins

Recife, Dezembro 2013

Frederico José de Santana Pontes

Influência de Quimiotipos, Íons e da Temperatura na Estrutura e Dinâmica de Bicamadas de Lipídio A de

Pseudomonas aeruginosa e Escherichia coli.

Tese apresentada como parte dos requisitos para a obtenção do título de Doutor em Química pelo Programa de Pós-Graduação em Química da Universidade Federal de Pernambuco.

Orientador: Roberto Dias Lins Neto

Recife, 2013

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Tese submetida ao Corpo Docente do Programa de Pós-Graduação em

Química do Departamento de Química Fundamental da Universidade Federal de

Pernambuco como parte dos requisitos necessários para a obtenção do Grau de

Doutor em Química.

Aprovada:

Roberto Dias Lins Neto (Orientador) Departamento de Química Fundamental Universidade Federal de Pernambuco

Prof. Ricardo Luiz Longo

Departamento de Química Fundamental Universidade Federal de Pernambuco

Prof. Jorge Luiz Neves Departamento de Química Fundamental Universidade Federal de Pernambuco

Prof. Claudio Gabriel Rodrigues Departamento de Biofísica e Radiobiologia

Universidade Federal de Pernambuco

Prof. Werner Treptow Departamento de Biologia Celular

Universidade de Brasília

“Influência de quimiótipos, íons e temperatura na estrutura e dinâmica de bicamadas de lipídio A de Pseudomonas

aeruginosa e Escherichia coli ”

Frederico José de Santana Pontes

Departamento de Química Fundamental Centro de ciências exatas e da natureza Universidade Federal de Pernambuco

Recife-PE- Brasil 19 de Dezembro de 2013

Agradecimentos

As realizações e conquistas, até as mais íntimas pessoais, não são possíveis, em sua grande maioria sem o apoio e a colaboração de pessoas e/ou instituições. Nessa página, tentarei descrever em palavras a gratidão pelo apoio recebido para a conclusão dessa etapa. Inicialmente gostaria de agradecer ao meu orientador, Prof.° Roberto Lins, pela oportunidade e condições oferecidas a mim de desenvolver esse trabalho de tese e, associado a isso, a um novo horizonte de pesquisas antes não enxergada por mim. Do ponto de vista do fomento intelectual, ainda devo agradecer fortemente aos Professores Thereza Soares, Ricardo Longo e Jorge Neves. In

memoriam o meu agradecimento aos saudosos Professores Benício de Barros Neto e Ricardo Ferreira, ambos de grande legado científico e influência, que me brindaram com orgulhos que posso estampar no currículo.

Difícil seria concluir essa etapa sem agradecer o apoio, companhia e valiosas trocas de informações provenientes das pessoas queridas, poderia repetir os nomes do primeiro parágrafo, mas resolvi citar novas pessoas: Viviane, pelo amor e contemplação das minhas estranhezas, aos amigos e companheiros de grupo BIOMAT (Victor, Gabriel, Roberta Dias, Janilson, Bruna, Agrinaldo, Keila, Vanessa, Denys, Daniela, Rafael, Laércio, Richard, Marcos Paula e Isabelle) pela boa convivência, risos, camaradagem, scripts, artigos e arquivos compartilhados nos últimos anos. Isso pode ser igualmente aplicado aos amigos e companheiros do LQTC, especialmente a Diego, Carol Pacheco, Carlos Henrique, Paulo, Miguel, Júlio, Albano, Renaldo, Eduardo Aguiar, Juliana Angeiras e Carol Roma. Numa esfera de coordenação menos teórica e computacional, devo citar os nomes de bons amigos como: Tiago Rodrigues, Mario Ramos, Kleber Clementino, Juliana, Cândida, Sidney, Lizandra, Rodrigo Cordeiro, Flávia Borba, Vitor Deichmann, Robson Barros e Rafael Queiroz.

Sem financiamento esse trabalho não seria possível de ser desenvolvido, por isso agradeço a INAMI/INAMI pela bolsa concedida durante grande parte do tempo de doutoramento (especialmente ao Prof.° Oscar Malta e ao secretário Gustavo), ao CNPq pela bolsa concedida durante um ano. Agradecer as agências que possibilitaram a infra-estrutura e participação em eventos, como: FACEPE, STINT e EMSL. Agradecer a todos os funcionários do DQF, especialmente a Maurílio Sebastião e a Patrícia Rosa por me tratarem pacientemente durante o doutoramento.

Eu não posso esquecer o agradecimento especial e fraterno ao meu núcleo familiar (Isnar, Ivaldo, Carla, Emerson, Gabriel e Heitor). Além de agradecer ao café pela disposição extra e por me permitir sonhar acordado (já que o mesmo reduziu as minhas horas diárias de sono).

Não importa o que você fez

Há sempre uma próxima vez

Não se perca, não pare

Escolha o menor dos males

Faça o que quer fazer

Aconteça o que acontecer

Tanto faz como se chama

Entregue-se ao que você ama

Titãs (O Fácil é o Certo)

Resumo

Aspectos estruturais, dinâmicos e de mudanças no estado físico e forma de agregação de

bicamadas de Lipídio A foram investigadas utilizando a técnica de simulação computacional por

dinâmica molecular com um campo de força atomístico. Sistematicamente diferentes cátions

(Na+e Mg2+), em diferentes temperaturas (278K, 300 K e 328 K) e variações fenotípicas (lipídios

hexa-, penta- e tetracilados) foram testadas em bicamadas de Lipídio A de duas diferentes

bactérias (Pseudomonas aeruginosa e Escherichia coli). Dessa maneira, conseguimos

caracterizar fases distintas de bicamadas de Lipídio A de P. aeruginosa, além de obter resultados

consistentes com as temperaturas de transição de fase para as membranas das duas espécies de

bactéria Gram-negativas. As simulações apontaram também que íons monovalentes induzem um

rearranjo na membrana da fase lamelar para uma fase não-lamelar. O estado de agregação das

bicamadas de Lipídio A mostrou-se uma combinação importante de dois fatores: a conformação

adotada pelo lipídio (se tem um formato mais cônico ou cilíndrico) e a habilidade do contraíon

presente em realizar pontes entre os grupos fosfatos de unidades lipídicas distintas. A correlação

entre o ângulo de inclinação entre os anéis de glucosamina e o plano da membrana – proposição

experimental utilizada para explicar a endotoxicidade e forma de agregação do Lipídio A – não

foi observada de maneira quantitativa em nossos cálculos.

Palavras-chave: Lipídios. Endotoxicidade. Simulação Computacional. Estrutura

Supramolecular

Abstract

Structure, dynamics, phase transition and general assembly of Lipid A bilayers were

investigated in this work through atomistic molecular dynamics simulations. A range of

temperature (278K, 300K e 328K), cations (mono- and bivalentes: Mg2+ and Na+) and

phenotypes of Lipid A (hexa-, penta- and tetraacilated) of two different Gram-negative bacterias

(Pseudomonas aeruginosa e Escherichia coli) have been tested in order to characterize the

membranes and its properties. Validation for model systems included the appropriate description

of area per lipid, order parameter, spatial chemical group distribution and membrane solvation

and structure as a function of temperature variation. Moreover, our findings show that Lipid A

bilayers undergo from a lamellar to non-lamellar arrangement in the presence of monovalent

ions. This is due to the inability of these ions to crosslink phosphate groups from neighboring

Lipid A units. Our findings support two dominant aspects governing Lipid A bilayer membrane

assembly: the shape of Lipid A units (conical vs cylindrical) and the ability of the counter ion to

crosslink between different phosphate groups. Analysis of simulated trajectories do not support

quantitatively the experimental proposition that correlates the tilt angle between the

glucosamines rings of Lipid A and the membrane plane with acyl chain phenotypical variation.

Keywords: Lipids. Endotoxicity. Computer Simulation. Supramolecular Structure.

Lista de Figuras

Título Página Figura 1.1: Representação de bastões de um Lipídio A com as suas regiões hidrofóbicas (cadeias aciladas), semipolar (grupos alcoóis, amino e ésteres) e polares (açúcares e grupos fosfato) indicadas. Átomos de hidrogênio representados na cor branca, de oxigênio em vermelho; de fósforo em bronze; carbono em verde e nitrogênio em azul, respectivamente.

Figura 1.2: Estrutura geral de um glicerofosfolipídio e seus substituintes mais comuns e carga total em pH = 7 (Nelson e Cox, 2008).

Figura 1.3: Figura ilustrativa do modelo de mosaico fluido demonstrando a complexa composição de uma membrana lipídica [Nelson e Cox, 2008].

Figura 1.4: Movimentos individuais de lipídios em bicamadas. (a) Difusão lateral da ordem de µm2s-1. (b) Movimento de flip-flop em bicamadas com duração de dias (forma não-catalizada) [Nelson e Cox, 2008].

Figura 1.5: Relação entre o formato do lipídio (de comprimento de cadeias alquiladas (L) e área da cabeça (A)) e as diferentes formas de agregação possível: (a) agregado esférico; (b) agregado cilíndrico e (c) agregado planar. A estimativa do valor de parâmetro de empacotamento está indicada na última coluna.

Figura 1.6: Representação de três possíveis formas de agregação de membranas lipídicas em solução aquosa e sua relação com a estrutura primária do lipídio formador da macroestrutura (a) vesículas (b) bicamadas e (c) vesículas. [Nelson e Cox, 2008].

Figura 1.7: Mudança de fase em membranas lipídicas sobre influência da temperatura. No topo da imagem membrana em estado paracristalino e na parte inferior membrana em fase fluida [Nelson e Cox, 2008].

Figura 1.8: Esquema da disposição dos lipídios em membranas em diferentes fases. Da esquerda para a direita: Lβ (fase gel ordenada), Lβ’(fase gel inclinada), Pβ’ (fase ripple) e Lα (fase líquido-cristalina) [Lipowsky e Sackmann, 1995].

Figura 1.9: (Topo) Caracterização da transição de fase em membranas lipídicas através de medidas de absorção de calor. Período de pré-transição fase indicado no gráfico. Estrutura da membrana em estado paracristalino (azul) e conformação trans das ligações carbono - carbono indicadas. Estrutura da membrana em estado fluido (rosa) e conformações gauches adotadas nas ligações carbono – carbono.

Figura 1.10: Esquema geral de uma molécula de LPS. Os grupos básicos da estrutura estão identificados na parte de baixo da figura. As diferentes regiões também estão indicadas na figura: Lipídio A, Núcleo Oligossacarídico (interno e externo) e Antígeno O. Na parte de cima, está a classificação do LPS de acordo com a presença de cada subunidade também está destacada: R (rugoso), SR (semirugoso) e L (liso). (Adaptado de Pupo e Hardy, 2009).

Figura 1.11: Estrutura dos quimiotipos de Lipídios A mais comuns de cada bactéria Gram-negativa. Os números na parte de inferior em cada quadro indicam o

comprimento das cadeias lipídicas. A atividade endotóxica de cada lipídio está indicada, de maneira qualitativa, pelo sinal de positivo [Erridge et al, 2002]. Figura 3.1: a) Condições periódicas de fronteira 2D: as partículas que se movem fora da caixa de simulação são substituídas por uma equivalente proveniente de uma imagem da caixa. b) Estrutura de funcionamento da busca por vizinhos onde as interações não-ligadas são calculadas, se os átomos estão situados num dado raio de corte, dentro da própria caixa ou nas caixas vizinhas [Allen, 2004].

Figura 3.2: Representação dos termos ligados compõem a função de energia potencial em mecânica molecular. Os átomos em amarelo é um exemplo do termo de ligação, os átomos em verde representam o ângulo de ligação e os átomos em vermelho o tempo de ângulo diedro na molécula.

Figura 4.1: Estrutura química da molécula de Lipídio A (a) hexa- (b) penta- e (c) tetraacilado.

Figura 4.2: Representação de uma caixa de simulação de uma bicamada de Lipídio A de Pseudomonas aeruginosa pentaacilado tendo o Mg2+ como contraíon. Os íons estão representados por esferas de cor roxa, as moléculas de água por esferas de van

der Waals e os lipídios por bastões. O instantâneo da imagem é do primeiro nanosegundo de simulação.

Figura 4.3: Representação bidimensional do raio r e Δr para o cálculo de gij(r) para a partícula central i em relação às partículas j (fonte: [http://www.compsoc.man.ac.uk/~lucky/Democritus/Theory/rdf.html]).

Figura 4.4: (b) Relação entre cada esfera de coordenação do gráfico bidimensional com os picos do gráfico para um fluido monoatômico (fonte: [Ziman, 1979]).

Figura 4.5: Principais definições envolvidas no cálculo do parâmetro de ordem SCD em cadeias alifáticas de lipídios (fonte: [Petrache et al, 1999]).

Figura 5.1.1: Energia potencial (kJ/mol) das bicamadas de Lipídio A penta- e hexaaciladas tendo o Na+ e o Mg2+ como contraíons.

Figura 5.1.2: Área por cabeça de Lipídio A (nm2) das membranas hexa- e pentaaciladas tendo Na+ e Mg2+ como contraíons

Figura 5.1.3: Estrutura final das membranas de Lipídio A hexa- e pentaaciladas contendo Mg2+ (superior) e estruturas contendo Na+ como contraíons (inferior). O instante de tempo da simulação correspondente a estrutura está indicada em cada figura. As membranas contendo o íon Na+ (nahex_300 e napent_300) foram representadas por cortes na região da membrana e apenas a região contendo os lipídios foi reproduzida.

Figura 5.1.4: Ângulo de inclinação dos anéis de glucosamina do Lipídio A hexa- e pentacilado tendo o Mg2+ como contraíon em relação ao plano da membrana. O ângulo foi medido durante os últimos 50 ns de trajetória equilibrada.

Figura 5.1.5: Frequência normalizada dos ângulos de inclinação entre as glucosaminas e o plano da membrana nas bicamadas de Lipídio A hexa- e pentaaciladas contendo o íon Mg2+.

Figura 5.1.6: Razão entre o raio de giro dos grupos terminais das cadeias aciladas (CH3) e dos anéis de glucosaminas de Lipídio A hexa- e pentaacilados tendo o Na+ e o Mg2+ como contraíons. As médias foram feitas sobre todos os lipídios da bicamada e nos últimos 50ns de trajetória equilibrada.

Figura 5.1.7: Perfis de densidades parciais de número (nm-3) ao longo do eixo Z de 62

alguns grupos químicos selecionados para as membranas de Lipídio A contendo Na+ e Mg2+. O cálculo foi realizado nos últimos 50 ns simulados de trajetória equilibrada de cada simulação. Figura 5.1.8: Funções de distribuição radial do par Íon – O (H2O) para as bicamadas de Lipídio A hexa- e pentaaciladas contendo os íons Na+ e Mg2+. Os gráficos foram feitos para os últimos 50 ns de trajetória equilibrada.

Figura 5.1.9: Funções de distribuição radial do par P - Íon para as bicamadas de Lipídio A hexa- e pentaaciladas contendo os íons Na+ e Mg2+. Os gráficos foram feitos para os últimos 50 ns de trajetória equilibrada.

Figura 5.1.10: Indicação das cadeias sn-1, sn-2 e sn-3 na molécula de Lipídio A. Entre parênteses o número de átomos de carbono incluídos para análise em cada cadeia.

Figura 5.1.11: Parâmetro de ordem médio para os átomos das cadeias aciladas do Lipídio A em cada simulação. A propriedade foi calculada para os últimos 50 ns de trajetória equilibrada.

Figura 5.1.12: Freqüência não-normalizada dos ângulos de inclinação do Lipídio A hexa- e pentaacilado contendo íons Na+ e Mg2+ em relação ao eixo Z. O ângulo foi medido para os últimos 50 ns de cada simulação

Figura 5.2.1: Conformação do Lipídio A e relação com sua endotoxicidade: (A) altamente endotóxico; (B) endotóxico; (C), (D) e (E) são inativos. [Seydel et al, 2000].

Figura 5.2.2: Energia potencial (kJ/mol) das membranas de Lipídio A hexa-, penta- e tetraaciladas contendo íons Na+ e Mg2+ ao longo de toda a trajetória.

Figura 5.2.3: Área por cabeça (nm2) para das membranas de Lipídio A hexa-, penta- e tetraaciladas contendo íons Na+ e Mg2+ ao longo de toda a trajetória

Figura 5.2.4: Estrutura final das bicamadas de Lipídio A hexa-, penta- e tetraaciladas contendo íons Na+ e Mg2+. A membrana ecoli_namp300 foi representada por um corte no eixo Z onde a maioria dos Lipídios A estavam concentrados. O tempo correspondente a estrutura representada está indicado entre parênteses.

Figura 5.2.5: Perfis de densidades parciais (kg/m3) de massa das membranas Lipídio A hexa-, penta- e tetraaciladas contendo íons Na+ e Mg2+. O perfil foi calculado nos últimos 70 ns de trajetória equilibrada de cada membrana.

Figura 5.2.6: Estrutura final da membrana de Lipídio A tetraacilado contendo íons Mg2+. A linha marrom indica uma posição do eixo Z onde a densidade de moléculas de água (van der Waals) co-existe com a do núcleo hidrofóbico da membrana, sem necessariamente haver uma grande quantidade de moléculas de água dentro desse núcleo como indicado no perfil de densidade da membrana.

Figura 5.2.7: Indicação das cadeias sn-1, sn-2, sn-3 e sn-4 nas variações fenotípicas de Lipídio A. A esquerda temos o hexaacil Lipídio A de E. coli e a direita o tetraacil Lipídio A de P. aeruginosa.

Figura 5.2.8: Parâmetros de ordem dos átomos de deutério para as cadeias aciladas das membranas Lipídio A hexa-, penta- e tetraaciladas contendo íons Na+ e Mg2+. A análise foi realizada nos últimos 70 ns de trajetória equilibrada de cada membrana.

Figura 5.2.9: Transição de fase de membranas de Lipídio A de E. coli [Gutsmann et

al, 2000]. A faixa de temperatura de transição está indicada em vermelho. 81

Figura 5.2.10: Funções de distribuição radial entre o íon e o átomo de oxigênio da água para as membranas Lipídio A hexa-, penta- e tetraaciladas contendo íons Na+ e Mg2+. A análise foi realizada nos últimos 70 ns de simulação.

Figura 5.2.11: Funções de distribuição radial entre o íon e o átomo de fósforo do grupo fosfato para as membranas Lipídio A hexa-, penta- e tetraaciladas contendo íons Na+ e Mg2+. A análise foi realizada nos últimos 70 ns de simulação.

Figura 5.2.12: Razão entre os raios de giro dos grupos metis terminais das cadeias aciladas e dos anéis de glucosamina das unidades de membranas Lipídio A hexa-, penta- e tetraaciladas contendo íons Na+ e Mg2+. As médias foram calculadas sobre todas as moléculas de lipídio da bicamada nos últimos 70 ns de simulação.

Figura 5.2.13: (a) Ângulo de Inclinação entre os anéis de glucosamina do Lipídio A e o plano da membrana. A propriedade foi medida nos últimos 70 ns de cada simulação. (b) Ângulo de inclinação de algumas espécies de Lipídio A medidos por radiação de infravermelho polarizada [Seydel et al, 2003].

Lista de Tabelas

Título Página Tabela 1.1: Valores de coeficiente de difusão lateral de lipídios [µm2 s-1] em membranas lipídicas medidas através de espectroscopia de fluorescência [Máchan e Hof, 2010]. A temperatura (°C) da medida está indicada entre parênteses. O suporte da bicamada lipídica está indicada pelos superescritos (m) mica ou (q) quartzo.

Tabela 4.1 – Relação das simulações computacionais realizadas neste trabalho com especificação do tipo de contra-íon, estrutura química do Lipídio A na bicamada, temperatura (K), tempo de simulação (ns) e sigla para identificação da simulação.

Tabela 5.1.1: Valores médios e desvio-padrão para a razão entre os raios de giro CH3/NAc-Glc para os quimiotipos hexa- e pentacilados contendo íons Mg2+ e Na+ calculados nos últimos 50 ns de simulação.

Tabela 5.1.2: Números de coordenação dos pares Ion – P e Ion – O (H2O) para as membranas de quimiotipos penta- e hexaacilados contendo os íons Mg2+ e Na+.

Tabela 5.2.1: Valor médio com desvio-padrão para a área por cabeça de Lipídio A (nm2) dos sistemas lamelares simulados nessa etapa do estudo. Os valores foram calculados para os últimos 50 ns da trajetória equilibrada.

Tabela 5.2.2: Valores médios com os seus respectivos desvios-padrões para os parâmetros de ordem de deutério das membranas simuladas. Os resultados estão separados por espécie de bactéria.

Tabela 5.2.3: Números de coordenação dos pares Ion – P e Ion – O (H2O) para as membranas de E. coli quimiotipos hexaacilado e mono- e difosforilado, além da membrana de P. aeruginosa tetraacilada.

Tabela 5.2.4: Valores médios e desvio-padrão para a razão entre os raios de giro CH3/NAc-Glc para os quimiotipos de E. coli e P. aeruginosa contendo íons Mg2+ e Na+ calculados nos últimos 50 ns de simulação.

Lista de Siglas e Abreviaturas

Sigla Significado Dlat Difusão Lateral de Lipídios Lα Fase líquido-cristalino Lβ Fase gel ordenada Lβ’ Fase gel inclinada Pβ Fase ripple Tm Transition Melting (Temperatura de Transição de Fase) LPS Lipopolissacarídeo KDO Ácido 3-Deoxi-D-manno-Oct-2-ulosonico DM Dinâmica Molecular NVT Sigla para o ensemble canônico NpT Sigla para o ensemble isotérmico-isobárico PME Particle Mesh Ewald

FT-IR Fourier Transformation – Infrared (Infravermelho com Transformada de Fourier) DLPC 1,2-dilauroil-sn-glicero-3-fosfocolina DOPC 1,2-dioleoil-sn-glicero-3-fosfocolina DSPC 1,2-distearoil-sn-glycero-3-fosfocolina POPC 1-palmitoil-2-oleoil-sn-glicero-3-fosfocolina CMC Concentração Micelar Crítica Apl Área por cabeça de lipídio SCD Parâmetro de ordem de deutério

Sumário

Seção Página Resumo 4 Abstract 5 Lista de Figuras 6 Lista de Tabelas 10 Lista de Abreviaturas 11 1. Introdução 14 1.1 Lipídios e Membranas Biológicas 14 1.1.1 Lipídios 14 1.1.2 Membranas Biológicas 17 1.1.3 Formas de Agregação 20 1.1.4 Fases das Membranas 22 1.1.5 Transições de Fase em Membranas Lipídicas 23 1.2 Lipopolissacarídeos 25 1.2.1 Estrutura e Composição 25 1.2.1.1 Antígeno O 26 1.2.1.2 Núcleo de Oligossacarídeos 26 1.2.1.3 Lipídio A 27 1.3 Lipídio A: Endotoxicidade, Estrutura Química e Importância 27 2. Hipótese e Relevância 30 3. Fundamentos Teóricos 31 3.1 Método de Dinâmica Molecular (DM) 32 3.2 Aspectos Importantes Envolvendo Simulações de Dinâmica Molecular 33 3.3 Campos de Força 37 3.3.1 Termo de Estiramento de Ligação 38 3.3.2 Termo de Flexão de Ângulo de Ligação 39 3.3.3 Termos Torsionais 40 3.3.4 Torsões Impróprias e Movimentos de Flexão Fora do Plano 41 3.3.5 Termo de Lennard-Jones 41 3.3.6 Termo de Interação Eletrostática 42 4. Metodologia 43 4.1. Preparação dos Sistemas 43 4.2 Protocolos de minimização de energia e simulação computacional por dinâmica molecular

4.3 Análises dos Dados das Simulações 48 4.3.1 Área por cabeça de Lipídio A (Apl) 48 4.3.2 Função de Distribuição Radial de Pares 49 4.3.3 Parâmetros de Ordem de Deutério 51 4.3.4 Perfis de Densidade Parcial de Massa 52 4.3.5 Ângulo entre as glucosaminas e o plano da membrana 53

7. Apêndice 92 8. Referências Bibliográficas 97 9. Atividades de pesquisa desenvolvidas durante o Doutorado. 107

4.3.6. Razão entre o raio de giro das glucosaminas e grupos metil (-CH3) terminais. 53 5 Resultados e Discussão 55 5.1 Mudanças na Forma de Agregação 55 5.1.1 Energia Potencial 55 5.1.2 Área por cabeça de Lipídio A 56 5.1.3 Ângulo de Inclinação e Raio de Giro dos Lipídios A na Bicamada. 58 5.1.4 Densidades Parciais 61 5.1.5 Funções de Distribuição Radial 63 5.1.5.1 Função de Distribuição Radial de Pares: Íon – O (H2O). 63 5.1.5.2 Função de Distribuição Radial de Pares: Íon – P. 64 5.1.6 Parâmetros de Ordem do Deutério 66 5.1.7 Orientação das Moléculas de Lipídio A nos Agregados 69 5.2 Efeito do Cátion na Forma de Agregação de Membranas de Lipídio A de P.

aeruginosa e E. coli. 71

5.2.1 Energia Potencial 72 5.2.2 Área por cabeça do Lipídio A 73 5.2.3 Perfil de Densidade 76 5.2.4 Parâmetros de Ordem do Deutério 79 5.2.5 Funções de Distribuição Radial 82 5.2.5.1 Função de Distribuição Radial de Pares: Íon – O (H2O). 82 5.2.5.2 Função de Distribuição Radial de Pares: Íon – P. 84 5.2.6 Ângulo de Inclinação e Raio de Giro dos Lipídios A na Bicamada. 86

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