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Differential transcriptional invasion signatures from patient derived organoid models define a functional prognostic tool for head and neck cancer

ABSTRACT: Differential transcriptional invasion signatures from patient derived organoid models define a functional prognostic tool for head and neck cancer

PROVIDER: PRJNA1026511 | ENA |

REPOSITORIES: ENA

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			Action	DRS
	SRR26333200_1.fastq.gz	Fastqsanger.gz
	SRR26333200_2.fastq.gz	Fastqsanger.gz
	SRR26333201_1.fastq.gz	Fastqsanger.gz
	SRR26333201_2.fastq.gz	Fastqsanger.gz
	SRR26333202_1.fastq.gz	Fastqsanger.gz

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Differential transcriptional invasion signatures from patient derived organoid models define a functional prognostic tool for head and neck cancer

Project description:Clinical outcome for patients suffering from head and neck squamous cell carcinoma (HNSCC) remains poor. This is mostly due to highly invasive tumors that cause loco-regional relapses after initial therapeutic intervention. The molecular pathways governing the detrimental invasive growth modes in HNSCC remain however understudied. Here, we have established HNSCC patient derived organoid (PDO) models that recapitulate 3-dimensional invasion in vitro. Single cell mRNA sequencing was applied to study the differences between non-invasive and invasive conditions, and in a collective versus single cell invading PDO model. Differential expression analysis under invasive conditions in Collagen gels reveals an overall upregulation of a YAP-centered transcriptional program, irrespective of the invasion mode. However, we find that collectively invading HNSCC PDO cells show elevated levels of YAP transcription targets when compared to single cell invasion. Also, collectively invading cells are characterized by increased nuclear translocation of YAP within the invasive strands, which coincides with Collagen-I matrix alignment at the invasive front. Using gene set enrichment analysis, we identify immune cell-like migratory pathways in the single cell invading HNSCC PDO, while collective invasion is characterized by overt upregulation of adhesion and migratory pathways. Lastly, based on a clinical head and neck cancer cohort, we demonstrate that the identified collective invasion signature provides a candidate prognostic platform for survival in HNSCC. By uncoupling collective and single cell invasive programs, we have established invasion signatures that may guide new therapeutic options.

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Differential transcriptional invasion signatures from patient derived organoid models define a functional prognostic tool for head and neck cancer.

Project description:Clinical outcome for patients suffering from HPV-negative head and neck squamous cell carcinoma (HNSCC) remains poor. This is mostly due to highly invasive tumors that cause loco-regional relapses after initial therapeutic intervention and metastatic outgrowth. The molecular pathways governing the detrimental invasive growth modes in HNSCC remain however understudied. Here, we have established HNSCC patient derived organoid (PDO) models that recapitulate 3-dimensional invasion in vitro. Single cell mRNA sequencing was applied to study the differences between non-invasive and invasive conditions, and in a collective versus single cell invading PDO model. Differential expression analysis under invasive conditions in Collagen gels reveals an overall upregulation of a YAP-centered transcriptional program, irrespective of the invasion mode. However, we find that collectively invading HNSCC PDO cells show elevated levels of YAP transcription targets when compared to single cell invasion. Also, collectively invading cells are characterized by increased nuclear translocation of YAP within the invasive strands, which coincides with Collagen-I matrix alignment at the invasive front. Using gene set enrichment analysis, we identify immune cell-like migratory pathways in the single cell invading HNSCC PDO, while collective invasion is characterized by overt upregulation of adhesion and migratory pathways. Lastly, based on clinical head and neck cancer cohorts, we demonstrate that the identified collective invasion signature provides a candidate prognostic platform for survival in HNSCC. By uncoupling collective and single cell invasive programs, we have established invasion signatures that may guide new therapeutic options.

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Project description:Recurrent/metastatic head and neck squamous cell carcinoma (R/M-HNSCC) is a severe, frequently lethal condition. Targeted therapy includes epidermal growth factor receptor (EGFR) blockade, but overall response rates are low and predictive biomarkers amiss. Deepened understanding of molecular networks governing EGFR-driven progression are required to explore predictive markers and therapeutic targets. We have mapped EGFR-mediated local invasion in a 3D-model using photoconvertible cell-tracers and uncovered invasion-associated, differentially expressed genes (DEGs) correlated with EGFR/MAPK activity and epithelial-to-mesenchymal transition (EMT) in primary malignant cells. A gene regulatory network (GRN) of local invasion was defined, composed of the central hubs inhibin subunit beta alpha (INHBA) and SLUG, and druggable effectors integrin subunit beta 4 (ITGβ4), its ligand laminin 5 (LAMB3/LAMC2), sphingosine kinase 1 (SPHK1), and EGFR ligand amphiregulin (AREG). Blockade of INHBA repressed local invasion, which was rescued by Activin A, Laminin 5, and sphingosine-1-phosphate, proving functional interconnection of the GRN. Functional DEGs (fDEGs) and, most prominently, central hub IHNBA, were associated with tumor buds in TCGA-HNSCC. Newly defined EGFR-activity subtypes, primarily dictated by AREG and epiregulin (EREG), show enhanced fDEGs expression, EMT correlation, and prognostic value. Cell-communication revealed strong interactions of AREG/EREG-governed EGFR-activities with non-malignant cells, potentially impacting on tumor progression. High expression of fDEGs enriched in EGFR-activities (INHBA, ITGA3, ITGΒ4, LAMA3, LAMC2, MT2A, EREG) was associated with response to Cetuximab in PDX models and R/M-HNSCC patients. Thus, we describe a novel GRN of EGFR-mediated local invasion and define druggable effectors with predictive potential regarding the response to Cetuximab.

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