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Alvarez Fallas, Mario Enrique (2016) Diaphragm derived acellular matrix as multistep study: from development to characterization using in vitro and in vivo strategies. [Tesi di dottorato]

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Abstract (inglese)

Abstract

Introduction

The demand for organ transplantation has rapidly increased during the past decades, thus requiring the development of a new interdisciplinary field, aimed at supplying this demand. Branching from regenerative medicine, the combination of elements usually applied separately for same or other purposes, was named Tissue Engineering (TE). Precisely, the components combined in TE constitute the so-called TE triad, are i) cells (derived from cell therapy), ii) scaffolding material (derived from material science) and iii) molecular signals (mainly derived from molecular biology and drug research). Among the organs and tissue that experience damages such that requiring implantation/transplantation, skeletal muscle represents no exception. As result of this, several approaches developed to efficiently repair the most common defects requiring surgery: Volumetric muscle loss (VML), abdominal wall defects (AWD) and defects of the diaphragm, namely traumatic diaphragmatic hernias or congenital diaphragmatic hernias (CDHs). While the first necessitates a substitute large in volume, the other two need a thinner but, according to defect size, wider surface. Thus far, between the materials chosen for repair of such defects, mostly synthetic materials were used, but decellularized tissue are rapidly covering the gap, likely to surpass them in the next future. Reason of this potential is the close resemblance to the organ or tissue of origin, while possessing features able to endpoint to constructive and functional remodeling. While decellularization-derivates of several organs and tissue were already attained, some were even tested in clinic and further moved to large-scale production (i.e. Surgisis®). However, only recently the proposal of developing a decellularized scaffold from diaphragm muscle for autologous repair purposes was reprised, and in general, was never considered in mouse.

Methods

Diaphragms (mouse and rabbit) were decellularized by a cyclical exposure to the sequence deionised water, sodium deoxycholate, DNase. Scaffolds were characterized in order to evaluate decellularization protocol efficiency, by the means of cell removal (mouse and rabbit), maintenance of microarchitecture (mouse and rabbit), ECM components (mouse), mechanical properties (mouse). Next, the interaction host-scaffold was tested in vivo, both in healthy and atrophic mice. Subsequent, a further characterization by disclosing the angiogenetic properties, both potential, taking advantage of the well-known CAM assay and subcutaneous transplant, as well as revealing angiogenesis-related protein content whithin the scaffold, and actual, by performing an orthotropic transplant in comparison with a synthetic material. To draw nearer the clinical validation, the characterized decellularized diaphragm (DD) were thus transplanted in the first surgically created model of CDH, again compared to the most commonly used material for the repair of this defect, polytetrafluoroethylene (PTFE), with the introduction recently of an allotransplant control. Lastly, as completion of a TE approach, it was developed a method to combine the cellular component, which was then applied to both mouse and rabbit derived scaffold.

Results
The adaption of a previously published detergent-enzymatic protocol aiming at obtaining a decellularized scaffold from diaphragm, resulted successful in with both mouse and rabbit sources, as cell removal while preserving microarchitecture and ECM components was attained. Moreover, it was confirmed that mechanical properties and growth factors were preserved in the mouse-derived scaffold. Upon implantation of the latter, angiogenesis and myogenic activation, while modulating the immune response were observed. In the healthy environment, the effect was transient, whereas implantation in a mouse model of atrophy led to long-term beneficial effects. The testing of mouse scaffold in a surgical model of CDH proved the previously seen results, as, compared to PTFE, yielded better outcomes, such as no recurrence, amelioration of diaphragm excursion and, differently from before, to a sustained myogenic response through time points analysed. The method used to re-populate both mouse and acellular muscles , after being developed, thus far resulted in a successful cell delivery, while the scaffold supported cell proliferation, survival and differentiation.
Conclusions

Muscle scaffold from mice and rabbit can be successfully obtained by decellularizing the diaphragm muscle via detergent enzymatic protocol. These scaffolds were proven to have several attractive properties both in vitro and in vivo, derived from their close resemblance to the tissue of origin. Precisely, it was demonstrated that while in vitro can sustain cell survival, proliferation and differentiation, in vivo positively interact with the recipient environment, driving a constructive response. Hence, scaling up of this type of construct is likely to be happening in the next future.

Abstract (italiano)

Riassunto

Introduzione

Negli ultimi decenni, la lista di attesa dei pazienti che necessitano trapianto di organi o un intervento chirurgico mirato alla sostituzione di grandi porzioni di tessuto, è andata aumentando. Al contrario però, la disponibilità di donatori, sia vivi che cadaverici, non ha seguito lo stesso andamento. Come conseguenza, nonostante i tentativi di supplire a queste necessità, molti ancora muoiono in attesa di essere curati. La medicina rigenerativa, ovvero la combinazione di diversi elementi dell’ingegneria tissutale, nasce proprio per rispondere alla ancora pressante domanda di organi e tessuti trapiantabili. Precisamente, un approccio di medicina rigenerativa si avvale di tre componenti principali: i) le cellule (dalla terapia cellulare), ii) il supporto o impalcatura per favorirne la crescita (derivato dalla scienza dei materiali, ad esempio prostetici, comunemente chiamato scaffold o mesh) e iii) segnali molecolari (principalmente dalla biologia molecolare e della farmaceutica). Tra gli organi e tessuti che sperimentano danni tali da richiedere l'impianto/trapianto, vi è anche il muscolo scheletrico. Di conseguenza, anche per questo sono stati sviluppati diversi approcci mirati a riparare efficacemente i più comuni difetti sia pediatrici sia adulti che richiedono un intervento chirurgico: A) la perdita muscolare di un grande volume di muscolo (causato da incidenti o dalla necessità di rimuovere tumori muscolari), B) difetti della parete addominale e C) difetti del diaframma, soprattutto congeniti. A seconda del tipo di difetto, il sostituto da sviluppare dovrà avere peculiari proprietà, oltre a quelle basilari necessarie per essere considerato un approccio di ingegneria tissutale completo. Infatti, mentre A necessita di un sostituto in grado di ripristinare un grande volume, B e C richiedono un costrutto sottile ma, a seconda delle dimensioni del difetto, di una più o meno ampia superficie. Finora, per la riparazione di tali difetti per lo più sono stati utilizzati più frequentemente scaffold/mesh sintetici, ma quelli di derivazione naturale, ed in particolare ottenuti dalla decellularizzazione di un tessuto nella sua completezza, stanno rapidamente recuperando strada, ed è probabile che diverranno il metodo di elezione nel prossimo futuro. La ragione di questo potenziale è la stretta somiglianza con l'organo o il tessuto di origine, pur possedendo caratteristiche in grado di culminare in un rimodellamento costruttivo e funzionale. Inoltre, mentre la decellularizzazione è stata ottenuta anche in organi più complessi, i prodotti derivati da tessuti più semplici sono stati anche già testati in clinica e per alcuni si è persino giunti alla commercializzazione su larga scala (ad esempio il Surgisis®).
In questo lavoro si è partiti dal considerare la patologia dell’ernia diaframmatica, ad oggi riparata chirurgicamente tramite chiusura primaria con tessuto autologo, se il difetto lo permette, oppure ancora con mesh prostetici di natura sintetica. Tuttavia, gli svantaggi di questi tipi di materiali in termini di rigidità ed inerzia, rendono conto dell’attuale ricerca di una valida alternativa.
Si è proposto quindi di derivare un costrutto muscolare partendo dalla decellularizzazione del muscolo diaframmatico utilizzabile come toppa tissutale per riparare il danno dell’ernia sia senza cellule sia con nuove cellule donatrici. Il modello studiato è stato, per la prima volta, quello murino.

Metodi

Diaframmi (topo e coniglio) sono stati decellularizati tramite esposizione ciclica alla sequenza: acqua deionizzata, sodio desossicolato, DNasi. Gli scaffold ottenuti sono stati caratterizzati per valutare l'efficienza del protocollo in termini di rimozione delle cellule (topo e coniglio), preservazione della micro architettura (topo e coniglio), componenti della matrice extracellulare (topo), proprietà meccaniche (topo). Successivamente, l'interazione ospite-scaffold (in topo) è stata testata in vivo, sia in topi sani che atrofici. Un ulteriore caratterizzazione è stata attuata approfondendo le proprietà angiogeniche, sia potenziali, sfruttando il noto test CAM, il trapianto sottocutaneo e rivelando il contenuto di proteine coinvolte nella angiogenesi ancora presenti dopo la decellularizzazione, sia effettive, eseguendo un impianto ortotopico, utilizzando come confronto un materiale sintetico. Per avvicinare la validazione alla pratica clinica, il diaframma decellularizato di topo precedentemente caratterizzato è stato quindi utilizzato per il riparo nel primo modello di ernia diaframmatica chirurgicamente indotta in topo. Il paragone è stato fatto anche in questo caso con il materiale più comunemente usato per la riparazione di questo difetto in clinica. Inoltre, più recentemente è stato introdotto un controllo rappresentato dall’allotrapianto. Infine, a completamento di un approccio di ingegneria tissuatle, è stato sviluppato un metodo per combinare la componente cellulare, poi applicato a entrambi gli scaffold derivati da topo e coniglio.

Risultati

L'adattamento di un protocollo detergente enzimatico precedentemente pubblicato, al fine di ottenere uno scaffold decellularizato da diaframma, si è rivelato efficiente sia utilizzando il topo che il coniglio come fonti, ottenendo così da entrami la rimozione delle cellule preservando la somiglianza della struttura con il tessuto di origine. Inoltre, è stato confermato, solo in topo, che le proprietà meccaniche e i fattori di crescita sono stati conservati dopo la decellularizzazione. L'impianto dello scaffold di topo, ha provocato sia angiogenesi che l'attivazione dei precursori muscolari, modulando al contempo la risposta immunitaria. Nell'ambiente sano, l'effetto è stato transitorio, mentre l'impianto in un modello murino di atrofia ha portato ad effetti benefici a lungo termine. La sperimentazione nel modello chirurgico di ernia ha confermato i risultati precedentemente osservati ed in aggiunta, rispetto al materiale sintetico, ha mostrato migliori risultati, come l'assenza di erniazione recidiva, il miglioramento dell’escursione diaframmatica e, diversamente da prima, una più sostenuta risposta miogenica nel tempo. Il metodo utilizzato per ripopolare entrambi i diaframmi acellulari di topo e muscoli, dopo essere stato sviluppato, ha finora portato a risulstati positivi, mentre lo scaffold ha dimostrato di poter supportare la proliferazione, la sopravvivenza e la differenziazione delle cellule.

Conclusioni

Scaffold derivati dal muscolo di diaframma possono essere conseguiti con successo sia da topi che conigli, utilizzando un protocollo di tipo detergente-enzimatico. Tali, hanno dimostrato di possedere diverse proprietà interessanti sia in vitro che in vivo, derivate dalla loro stretta somiglianza con il tessuto di origine. Precisamente, è stato dimostrato che, mentre in vitro possono sostenere la sopravvivenza, la proliferazione e la differenziazione cellulare, in vivo sono in grado di interagire positivamente con l'ambiente ricevente, guidando una risposta costruttiva. Quindi, è molto probabile che ulteriori passi vengano fatti nel prossimo futuro, fino a raggiungere infine l’applicazione in clinica.

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Tipo di EPrint:Tesi di dottorato
Relatore:Pozzobon, Michela
Dottorato (corsi e scuole):Ciclo 28 > Scuole 28 > MEDICINA DELLO SVILUPPO E SCIENZE DELLA PROGRAMMAZIONE SANITARIA > EMATO-ONCOLOGIA, GENETICA, MALATTIE RARE E MEDICINA PREDITTIVA
Data di deposito della tesi:29 Gennaio 2016
Anno di Pubblicazione:29 Gennaio 2016
Parole chiave (italiano / inglese):Tissue engineering; Acellular scaffold; Skeletal muscle; Congenital diaphragmatic hernia; Translational medicine; Regenerative medicine
Settori scientifico-disciplinari MIUR:Area 05 - Scienze biologiche > BIO/13 Biologia applicata
Struttura di riferimento:Dipartimenti > Dipartimento di Salute della Donna e del Bambino
Codice ID:9336
Depositato il:21 Ott 2016 10:20
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