Transcriptional rewiring and diversity underpin the intratumoural heterogeneity in melanoma evolution, and has been linked to cancer metastasis and resistance to therapy1,2. The dysregulated RNA splicing in melanoma facilitates tumour-associated splicing patterns that can drive cancer cell phenotypic plasticity, independent of gene expression alteration3,4. Furthermore, aberrant splicing often produces cancer-specific novel isoforms with unknown molecular functions that are promising anticancer therapeutic targets5,6.
We aim to extensively study the full-length mRNA transcript isoform repertoire in primary and early-metastatic melanomas, and their functional consequences in driving cancer metastasis. By using Nanopore long-read RNA sequencing, we have deeply profiled the transcriptomic landscape of 57 treatment-naïve melanoma tumours collected from 48 patients, representing both primary and lymph node-metastatic disease. We have sequenced 1.7 billion high-quality long reads with 2 trillion nucleotide bases to facilitate novel isoform discovery and transcript abundance estimation.
Transcriptomic analysis reveals approximately 88,000 distinct transcript isoforms in the melanoma tumour microenvironment (TME). While most isoforms are structurally matched to the Ensembl human transcriptome annotation (ver. 112), we have identified 14,821 (20%) novel isoforms that have not been curated before. The majority of novel isoforms (∼10k) are unannotated splice variants of previously characterized genes, suggesting the understudied complexity of alternative splicing in the human transcriptome. Intriguingly, the analysis also reveals nearly 3,500 uncharacterized gene loci that are supported by 5,000 unannotated novel isoform variants, with their molecular functions completely undescribed. Transcript abundance estimation reveals that some novel isoforms are aberrantly expressed in melanoma but almost negligible in benign or healthy states, highlighting that they could be melanoma TME-specific. Bioinformatics analyses also suggest that these novel isoforms could be prognostic to melanoma recurrence and metastasis. Future experimental validation will further investigate whether these novel isoforms are potential immunogenic tumour-specific antigens (TSAs) that may improve immune targeting of melanoma through immunotherapy.
To our knowledge, this work is the first to leverage long-read RNA-seq to transcriptionally profile a large cohort of melanoma patients. These results highlight the ability to uncover completely new biology by investigating transcript diversity, while emphasizing the necessity of further investigating alternative splicing in driving melanoma progression and metastasis.