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Desantis, Giacomo (2013) Altered differentiation of tumor-associated monocytes and macrophages following genetic ablation of disabled homolog 2 gene. [Tesi di dottorato]

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Abstract (inglese)

Tumor progression is usually associated with abnormal myelopoiesis and recruitment of several myeloid cell subsets into tissues. These cells heavily infiltrate the primary tumor and sustain its growth by providing local immune suppression and promoting angiogenesis. They also assist metastatic spreading by favoring the tumor invasion of adjacent tissues, and by supporting cancer cell seeding into distant sites. Recent advances have partially highlighted the mechanisms through which myeloid cells are recruited into the tumor mass and suppress the immune response against tumor cells, thus laying the basis for new antitumor immunotherapeutic approaches. However, very little is known about the molecular pathways which regulate myeloid cell differentiation and functions within the tumor microenvironment, especially in the context of the metastatic process.
To obtain starting cues about new relevant molecular pathways acting in tumor-infiltrating myeloid cells, we performed gene expression analysis in purified CD11b+ intratumoral myeloid cells isolated from different transplantable murine tumor models. Among the most upregulated genes, we got particularly interested in the disabled homolog 2, mitogen-responsive phosphoprotein (Dab2) gene. The DAB2 protein is a molecular adaptor which participates to endocytosis and signal transduction pathways. Its main function is to link membrane receptors with clathrin assemblies, allowing selective clathrin-mediated endocytosis of transmembrane proteins. The vesicular trafficking has the important function to distribute and organize the protein content of the plasma membrane, allowing the cell to spatially react to external stimuli. We thought that this process is of key-importance within the tumor microenvironment, where complex cell-to-cell interactions occur and oriented stimuli are released.
In this work we show that, once within the tumor, both monocytes and macrophages upregulated the DAB2 protein. Both the cytokines GM-CSF and M-CSF, which regulate the development of mononuclear phagocytes, were able to induce DAB2 expression by myeloid cells in vitro, through a mechanism requiring the transcription factor C/EBPβ. Conditional knockout of the Dab2 gene in the hematopoietic system resulted in a strong reduction of tumor-infiltrating monocytes and macrophages. In vivo tracking experiments showed that Dab2-knockout (Dab2-/-) monocytes were less efficient to generate tumor-associated macrophages than wild type ones, and this was accompanied by reduced recovery of Dab2-/- monocytes within the tumor mass. In vitro differentiation of bone marrow-derived macrophages indicated that Dab2-/- monocytes cannot efficiently carry out the autophagy process, suggesting a molecular mechanism that could explain their macrophage differentiation defects. Moreover, Dab2-/- tumor-associated macrrophages had increased expression of genes and membrane markers associated with the M2 macrophage polarization. Finally, we found that spontaneous generation of metastases was impaired in Dab2-/- mice. These data strongly indicate that DAB2 is required for correct differentiation of tumor-associated macrophages, and suggest that this protein may be an optimal molecular target to obstruct myeloid cell-assisted dissemination of metastases in tumor-bearing hosts

Abstract (italiano)

La progressione della malattia neoplastica è solitamente accompagnata da una mielopoiesi anormale, con il richiamo di diverse sottopopolazioni mieloidi nei tessuti. Queste sottopopolazioni infiltrano fortemente il tumore primario e sostengono la sua crescita fornendo immunosoppressione e stimoli pro-angiogenici. Queste cellule assistono anche il processo metastatico favorendo l’invasione tumorale dei tessuti adiacenti, e sostenendo l’attecchimento delle cellule tumorali nei siti metastatici. Recenti scoperte hanno parzialmente compreso i meccanismi attraverso i quali le cellule mieloidi sono richiamate nella massa tumorale per sopprimere la risposta immunitaria contro le cellule tumorali, ponendo così le basi per nuovi approcci immunoterapeutici. Tuttavia, i meccanismi molecolari che regolano il differenziamento e le funzioni delle cellule mieloidi nel microambiente tumorale sono poco conosciuti, specialmente nel contesto del processo metastatico.
Per ottenere indizi iniziali riguardo nuove vie molecolari che agiscono nelle cellule mieloidi infiltranti il tumore, abbiamo effettuato un’analisi dell’espressione genica in cellule mieloidi CD11b+ intratumorali purificate da diversi modelli murini di tumore trapiantabile. Fra i geni più espressi, abbiamo trovato particolarmente interessante il gene disabled homolog 2, mitogen-responsive phosphoprotein (Dab2). La proteina DAB2 è un adattatore molecolare che partecipa all’endocitosi e a diverse vie di trasduzione del segnale. La sua principale funzione è di collegare i recettori di membrana con i raggruppamenti di clatrina, permettendo l’endocitosi selettiva delle proteine di membrana mediata dalla clatrina. Il traffico vescicolare ha l’importante funzione di distribuire ed organizzare il contenuto proteico della membrana plasmatica, consentendo alla cellula di reagire spazialmente agli stimoli esterni. Riteniamo che questo processo sia di importanza chiave all’interno del microambiente tumorale, dove avvengono complesse interazioni fra cellule e sono rilasciati stimoli orientati.
In questo lavoro mostriamo che, raggiunto il tumore, sia i monociti che i macrofagi esprimono la proteina DAB2. Le citochine GM-CSF ed M-CSF, le quali regolano lo sviluppo dei fagociti mononucleati, inducono l’espressione di DAB2 nelle cellule mieloidi in vitro, attraverso un meccanismo che richiede il fattore di trascrizione C/EBPβ. Il knockout condizionale del gene Dab2 nel sistema ematopoietico porta ad una forte riduzione dei monociti e macrofagi infiltranti il tumore. Esperimenti di tracciamento in vivo dei monociti Dab2-knockout (Dab2-/-) mostrano che questi ultimi, rispetto ai monociti wild type, sono meno efficienti nel generare i macrofagi associati al tumore, e questo effetto si accompagna con un ridotto recupero dei monociti Dab2-/- all’interno della massa tumorale. Il differenziamento in vitro di macrofagi ottenuti dal midollo osseo indica che i monociti Dab2-/- non riescono a sostenere efficientemente il processo autofagico, suggerendo un meccanismo molecolare che può spiegare il loro difetto di differenziamento in macrofagi. Inoltre, i macrofagi Dab2-/- associati al tumore hanno un’aumentata espressione di geni e marcatori di membrana correlati con la polarizzazione macrofagica M2. Infine, abbiamo scoperto che i topi Dab2-/- sono resistenti alla formazione di metastasi. Questi dati indicano fortemente che DAB2 è necessario per il corretto differenziamento dei macrofagi intratumorali, e suggeriscono che questa proteina potrebbe essere un ottimo target molecolare per ostacolare la disseminazione di metastasi assistita dalle cellule mieloidi negli individui con tumore

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Tipo di EPrint:Tesi di dottorato
Relatore:Bronte, Vincenzo
Dottorato (corsi e scuole):Ciclo 25 > Scuole 25 > ONCOLOGIA E ONCOLOGIA CHIRURGICA
Data di deposito della tesi:30 Gennaio 2013
Anno di Pubblicazione:30 Gennaio 2013
Parole chiave (italiano / inglese):cancro, metastasi, macrofagi, gene disabled 2, tumor, metastasis, disabled 2, macrophages
Settori scientifico-disciplinari MIUR:Area 06 - Scienze mediche > MED/06 Oncologia medica
Struttura di riferimento:Dipartimenti > Dipartimento di Scienze Chirurgiche Oncologiche e Gastroenterologiche
Codice ID:5779
Depositato il:07 Nov 2018 12:57
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