Recent studies have provided evidence of interactions among the gut microbiota (GM), local host immune cells, and intestinal tissues in colon carcinogenesis. However, little is known regarding the functions exerted by the GM in colon cancer (CC), particularly with respect to tumor clinical classification and lymphocyte infiltration. In addition, stool, usually employed as a proxy of the GM, cannot fully represent the original complexity of CC microenvironment. Here, we present a pilot study aimed at characterizing the metaproteome of CC-associated colonic luminal contents and identifying its possible associations with CC clinicopathological features. Colonic luminal contents were collected from 24 CC tissue specimens immediately after surgery. Samples were analyzed by shotgun metaproteomics. Almost 30,000 microbial peptides were quantified in the samples, enabling the achievement of the taxonomic and functional profile of the tumor-associated colonic luminal metaproteome. Upon sample aggregation based on tumor stage, grade, or tumor-infiltrating lymphocytes (TILs), peptide sets enabling discrimination of sample groups were identified through discriminant analysis (DA). As a result, Bifidobacterium and Bacteroides fragilis were significantly enriched in high-stage and high-grade CC, respectively. Among metabolic functions, formate–tetrahydrofolate ligase was significantly associated with high-stage CC. Finally, based on the results of this pilot study, we assessed the optimal sample size for differential metaproteomic studies analyzing colonic luminal contents. In conclusion, we provide a detailed picture of the microbial and host components of the colonic luminal proteome and propose promising associations between GM taxonomic/functional features and CC clinicopathological features. Future studies will be needed to verify the prognostic value of these data and to fully exploit the potential of metaproteomics in enhancing our knowledge concerning CC progression.

Metaproteomic profile of the colonic luminal microbiota from patients with colon cancer / Tanca, Alessandro; Abbondio, Marcello; Fiorito, Giovanni; Pira, Giovanna; Sau, Rosangela; Manca, Alessandra; Muroni, Maria Rosaria; Porcu, Alberto; Scanu, Antonio Mario; Paolo, Cossu-Rocca; DE MIGLIO, Maria Rosaria; Uzzau, Sergio. - In: FRONTIERS IN MICROBIOLOGY. - ISSN 1664-302X. - 13:(2022), pp. 1-15. [10.3389/fmicb.2022.869523]

Metaproteomic profile of the colonic luminal microbiota from patients with colon cancer

Alessandro Tanca
Membro del Collaboration Group
;
Marcello Abbondio
Membro del Collaboration Group
;
Giovanni Fiorito
Membro del Collaboration Group
;
Giovanna Pira
Membro del Collaboration Group
;
Rosangela Sau
Membro del Collaboration Group
;
Alessandra Manca
Membro del Collaboration Group
;
Maria Rosaria Muroni
Membro del Collaboration Group
;
Alberto Porcu
Membro del Collaboration Group
;
Antonio Mario Scanu
Membro del Collaboration Group
;
Paolo Cossu-Rocca
Membro del Collaboration Group
;
Maria Rosaria De Miglio
Membro del Collaboration Group
;
Sergio Uzzau
Membro del Collaboration Group
2022-01-01

Abstract

Recent studies have provided evidence of interactions among the gut microbiota (GM), local host immune cells, and intestinal tissues in colon carcinogenesis. However, little is known regarding the functions exerted by the GM in colon cancer (CC), particularly with respect to tumor clinical classification and lymphocyte infiltration. In addition, stool, usually employed as a proxy of the GM, cannot fully represent the original complexity of CC microenvironment. Here, we present a pilot study aimed at characterizing the metaproteome of CC-associated colonic luminal contents and identifying its possible associations with CC clinicopathological features. Colonic luminal contents were collected from 24 CC tissue specimens immediately after surgery. Samples were analyzed by shotgun metaproteomics. Almost 30,000 microbial peptides were quantified in the samples, enabling the achievement of the taxonomic and functional profile of the tumor-associated colonic luminal metaproteome. Upon sample aggregation based on tumor stage, grade, or tumor-infiltrating lymphocytes (TILs), peptide sets enabling discrimination of sample groups were identified through discriminant analysis (DA). As a result, Bifidobacterium and Bacteroides fragilis were significantly enriched in high-stage and high-grade CC, respectively. Among metabolic functions, formate–tetrahydrofolate ligase was significantly associated with high-stage CC. Finally, based on the results of this pilot study, we assessed the optimal sample size for differential metaproteomic studies analyzing colonic luminal contents. In conclusion, we provide a detailed picture of the microbial and host components of the colonic luminal proteome and propose promising associations between GM taxonomic/functional features and CC clinicopathological features. Future studies will be needed to verify the prognostic value of these data and to fully exploit the potential of metaproteomics in enhancing our knowledge concerning CC progression.
2022
Metaproteomic profile of the colonic luminal microbiota from patients with colon cancer / Tanca, Alessandro; Abbondio, Marcello; Fiorito, Giovanni; Pira, Giovanna; Sau, Rosangela; Manca, Alessandra; Muroni, Maria Rosaria; Porcu, Alberto; Scanu, Antonio Mario; Paolo, Cossu-Rocca; DE MIGLIO, Maria Rosaria; Uzzau, Sergio. - In: FRONTIERS IN MICROBIOLOGY. - ISSN 1664-302X. - 13:(2022), pp. 1-15. [10.3389/fmicb.2022.869523]
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Utilizza questo identificativo per citare o creare un link a questo documento: https://hdl.handle.net/11388/275905
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