Decoding chromosomal instability insights in CRC by integrating omics and patient-derived organoids

BackgroundChromosomal instability (CIN) is involved in about 70% of colorectal cancers (CRCs) and is associated with poor prognosis and drug resistance. From a clinical perspective, a better knowledge of these tumour's biology will help to guide therapeutic strategies more effectively.MethodsWe...

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Detalles Bibliográficos
Autores: Papaccio, F, Cabeza-Segura, M, García-Micó, B, Gimeno-Valiente, F, Zúñiga-Trejos, S, Gambardella, V, Gutiérrez-Bravo, MF, Martinez-Ciarpaglini, C, Rentero-Garrido, P, Fleitas, T, Roselló, S, Carbonell-Asins, JA, Huerta, M, Moro-Valdezate, D, Roda, D, Tarazona, N, del Pino, MMS, Cervantes, A, Castillo, J
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2025
País:España
Institución:INCLIVA
Repositorio:r-INCLIVA. Repositorio Institucional de Producción Científica de INCLIVA
OAI Identifier:oai:incliva.fundanetsuite.com:p19925
Acceso en línea:https://incliva.portalinvestigacion.com/publicaciones/19925
Access Level:acceso abierto
Palabra clave:Chromosomal instability
Colorectal cancer
Multi-omics
Mass spectrometry-based proteomics
Patient-derived organoids
Descripción
Sumario:BackgroundChromosomal instability (CIN) is involved in about 70% of colorectal cancers (CRCs) and is associated with poor prognosis and drug resistance. From a clinical perspective, a better knowledge of these tumour's biology will help to guide therapeutic strategies more effectively.MethodsWe used high-density chromosomal microarray analysis to evaluate CIN level of patient-derived organoids (PDOs) and their original mCRC tissues. We integrated the RNA-seq and mass spectrometry-based proteomics data from PDOs in a functional interaction network to identify the significantly dysregulated processes in CIN. This was followed by a proteome-wGII Pearson correlation analysis and an in silico validation of main findings using functional genomic databases and patient-tissues datasets to prioritize the high-confidence CIN features.ResultsBy applying the weighted Genome Instability Index (wGII) to identify CIN, we classified PDOs and demonstrated a good correlation with tissues. Multi-omics analysis showed that our organoids recapitulated genomic, transcriptomic and proteomic CIN features of independent tissues cohorts. Thanks to proteotranscriptomics, we uncovered significant associations between mitochondrial metabolism and epithelial-mesenchymal transition in CIN CRC PDOs. Correlating PDOs wGII with protein abundance, we identified a subset of proteins significantly correlated with CIN. Co-localisation analysis in PDOs strengthened the putative role of IPO7 and YAP, and, through in silico analysis, we found that some of the targets give significant dependencies in cell lines with CIN compatible status.ConclusionsWe first demonstrated that PDO models are a faithful reflection of CIN tissues at the genetic and phenotypic level. Our new findings prioritize a subset of genes and molecular processes putatively required to cope with the burden on cellular fitness imposed by CIN and associated with disease aggressiveness.