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Profiling Vaccinium Macrocarpon Components and Metabolites in Human Urine and the Urine Ex-Vivo Effect on Candida Albicans Adhesion and Biofilm

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Profiling Vaccinium Macrocarpon Components and Metabolites in Human Urine and the Urine Ex-Vivo Effect on Candida Albicans Adhesion and Biofilm DOTTORATO DI MEDICINA MOLECOLARE E TRASLAZIONALE CICLO XXXIII Anno Accademico 2019/2020 TESI DI DOTTORATO DI RICERCA MED/07 Tackling biofilm-related opportunistic fungal infections Dottorando: Emerenziana OTTAVIANO Matricola N°: R11871 TUTORE: Prof.ssa Elisa BORGHI COORDINATORE DEL DOTTORATO: Prof. Michele SAMAJA 1 2 RIASSUNTO 3 Ogni anno, oltre di 1 milione di persone muore a causa di infezioni fungine correlate alla produzione di biofilm. I biofilm sono comunità di microrganismi che si sviluppano adesi ad una superficie, biotica o abiotica, immerse in una matrice polimerica extracellulare autoprodotta. La capacità di organizzarsi in comunità microbiche è molto comune tra i microrganismi responsabili di infezione nell’uomo, tra questi vi sono anche i funghi. Tale organizzazione, rispetto alle forme planctoniche, è responsabile di una più difficile eliminazione del patogeno e predispone a frequenti fallimenti terapeutici legati alla maggiore refrattarietà alle terapie antimicrobiche. Alcune caratteristiche dell’ospite, quali alterazioni immunitarie o condizioni infiammatorie croniche, possono esacerbare la patogenesi dell’infezione e ritardarne la risoluzione. Candida albicans, tra i lieviti, e Aspergillus fumigatus tra le muffe, sono i patobionti più comuni tra gli agenti eziologici di infezioni nell’uomo. Nel nostro studio abbiamo valutato diverse strategie per inibire la formazione di biofilm fungini e per contrastare le infezioni ad essi correlate, considerano sia i fattori di virulenza microbici sia la risposta immunitaria dell'ospite. Abbiamo studiato l'efficacia delle frazioni urinarie, raccolte da volontari sani dopo l'assunzione di un integratore a base di mirtillo rosso, nell’inibire il biofilm di C. albicans. Mediante analisi di spettrometria di massa, abbiamo identificato due metaboliti più concentrati nelle frazioni urinarie risultate più attive, il 5-(3 ′, 4′-diidrossi fenil)-γ-valerolattone e l’acido 4-idrossibenzoico, che hanno mostrato avere un forte effetto 4 inibitorio sull'adesione di C. albicans e la sua filamentazione. Entrambi i composti sono stati anche in grado di ridurre l'espressione dei geni chiave delle prime fasi della formazione del biofilm. A causa dell’alta diffusione dell'uso di cateteri o protesi in campo medico, lo sviluppo di biomateriali con attività inibitoria nei confronti della formazione di biofilm microbici potrebbe rappresentare una buona strategia per controllare le infezioni nosocomiali. Abbiamo quindi testato matrici idro-gel di nuova sintesi e dimostrato la loro capacità di prevenire efficacemente la crescita di C. albicans. Al fine di valutare strategie che mirassero sia alla virulenza del patogeno sia alla risposta immunitaria dell'ospite, abbiamo condotto due diversi studi, il primo sulla candidosi sistemica da C. albicans e il secondo sull'infezione da A. fumigatus nei pazienti con CF. Abbiamo studiato l'attività, in vitro e in vivo nel modello di invertebrato Galleria mellonella, della pilocarpina, un agonista dei recettori muscarinici. La pilocarpina ha mostrato un effetto diretto nell'inibire la produzione di biomassa e l'attività metabolica del biofilm di C. albicans e la sua somministrazione alle larve precedentemente infettate ha aumentato la loro sopravvivenza. A causa del diverso comportamento della pilocarpina rispetto all'acetilcolina nella modulazione della risposta immunitaria della larva, abbiamo concluso che l'attività antifungina della pilocarpina potrebbe essere il risultato dell’attivazione in C. albicans di un recettore muscarinico-simile, mentre il forte effetto immunomodulante dell'acetilcolina (ma non di pilocarpina) potrebbe 5 derivare dal coinvolgimento dei recettori nicotinici, non ingaggiati da pilocarpina. Un approccio simile, mirato pertanto a combattere simultaneamente infezione e infiammazione, è stato utilizzato per studiare la persistenza di A. fumigatus nei polmoni dei pazienti con CF. Infatti, i monociti CF sono caratterizzati da un anomalo accumulo di lipidi intracellulari, che promuove uno stato infiammatorio, a sua volta responsabile di una ridotta capacità di eliminare i patogeni e, di conseguenza, una tardiva risoluzione dell'infezione. Abbiamo dimostrato che il trattamento con miriocina dei monociti isolati da pazienti CF, inibendo la sintesi degli sfingolipidi e riducendo l'infiammazione intracellulare, migliora la fagocitosi e l’eliminazione dei conidi di A. fumigatus. Inoltre, la miriocina è risultata in grado di ridurre l’espressione dei geni che codificano per le citochine pro- infiammatorie e allo stesso tempo di aumentare l'espressione dei geni che codificano per i recettori coinvolti nel riconoscimento dei patogeni, cruciali per una corretta eliminazione di questi ultimi. I nostri risultati indicano che, nonostante siamo ancora lontani dalla pratica clinica, esplorare strategie alternative anti-biofilm potrebbe aprire la strada alla scoperta di nuovi target e ad approcci integrati in grado di promuovere la risoluzione dell'infezione. 6 7 ABSTRACT 8 More than 1.5 million people/year die for a biofilm-related fungal infection. The ability to develop biofilms is widespread among human opportunistic pathogens, among them fungi. Biofilms are a community of microorganisms with the ability to attach to surfaces biotic or abiotic, surrounded by a self-produced extracellular polymeric matrix. The pathogen clearance and the general overcoming of the infection are complicated by biofilm presence as it confers tolerance to antimicrobial treatments. Compromised or altered immune response and an inflammatory milieu can exacerbate the pathogenesis and prolong the resolution of the infection. Candida albicans, between yeasts, and Aspergillus fumigatus between molds, are pathobionts considered the most common agents of opportunistic fungi mediated. In our study we assessed different strategies to eradicate biofilms and counteract biofilm-related infections, targeting both pathogens and host immune response. We investigated the efficacy of urinary fractions after cranberry extract intake by healthy volunteers against C. albicans biofilm. By mass spectrometry analyses, we identified two metabolites picking in the most active urine fractions, 5-(3′,4′- dihydroxy phenyl)-γ-valerolactone and 4-hydroxybenzoic acid, which revealed a strong inhibitory effect on C. albicans adhesion and biofilm formation. Both compounds were also able to downregulate the expression of key genes involved in early phases of biofilm formation. Due to the spread of the use of catheters or prostheses in the medical field, the possibility to develop biomaterials with biofilm inhibitory activity could represent a good 9 strategy to control nosocomial infections. We thus investigated newly synthesized hydrogels and demonstrated their ability to prevent C. albicans growth. To target both pathogen virulence and host immune response, we conducted two different studies, the first on C. albicans systemic candidiasis and the second on A. fumigatus infection in cystic fibrosis patients. We investigated the possible dual action of pilocarpine, a muscarinic receptor agonist, in vitro and in vivo using the model host Galleria mellonella. Pilocarpine showed a direct effect in inhibiting C. albicans biofilm biomass and metabolic activity, and its administration to infected larvae increased larval survival. Because of the different behavior of pilocarpine compared to acetylcholine in the modulation of larva immune response, we concluded that the antifungal activity of pilocarpine might rely on muscarinic-like receptor activation on C. albicans, whereas the strong immunomodulatory effect of acetylcholine (but not of pilocarpine) might imply the engagement of nicotinic receptors. A similar approach, aimed at targeting both infection and inflammation, was used to investigate A. fumigatus persistence in CF patient lungs. Indeed, CF monocytes are characterized by altered intracellular lipid accumulation, that compromise pathogen clearance, and the infection resolution. We demonstrated that the treatment of patient monocytes with Myriocin, by inhibiting the synthesis of sphingolipids and hampering CF inflammation, ameliorate the A. fumigatus conidia internalization and clearance. On the host side, Myriocin 10 was able to reduce the over expression of genes encoding for pro- inflammatory cytokines and at the same time to increase the expression of gene encoding for pathogen recognizing receptors, crucial for its clearance. Our results indicate that, despite we are still far from clinical practice, exploring alternative anti-biofilm strategies could pave the way to new target discovery and to integrated approaches able to promote the infection resolution. 11 12 TABLE OF CONTENTS ABSTRACT I RIASSUNTO II TABLE OF CONTENTS III RESEARCH INTEGRITY IV LIST OF ABBREVIATIONS V 1.INTRODUCTION 1.1 Clinical burden of fungal infections 1.1.1. Candida spp. 1.1.1.1. Candida virulence factors 1.1.1.2 Mucosal infections 1.1.1.3 Bloodstream infections 1.1.1.4 Galleria mellonella: an in vivo model of systemic infection 1.1.2. Aspergillus spp. 1.1.3. Antifungal resi stance 1.2 Biofilm-related tolerance to antifungal and strategies to overcome it 1.2.1 Candida albicans biofilms 13 1.2.2 Aspergillus fumigatus biofilms 1.2.3 Biofilm-related antifungal tollerance 1.2.4 Alternative strategies for fungal infection management 1.3 The vicious cycle: infection-inflammation 1.3.1 Candida albicans: its role in Inflammation 1.3.2 Aspergillus fumigatus: its role in cystic Fibrosis 2.AIM 3 MATERIALS AND METHODS 3.1 Culture
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