Abstract

Melanoma, a neural crest-derived cancer, exemplifies the complex interplay of genetic and non-genetic factors driving tumor progression, therapeutic resistance, and phenotypic plasticity. Central to this adaptability is SOX10, a master regulator of neural crest development and melanocyte differentiation, whose expression is controlled by enhancer elements that are reactivated in melanoma. This work provides a comprehensive investigation into the regulatory landscape of SOX10, integrating insights from zebrafish models, human melanoma cell lines, and comparative genomics to uncover the mechanisms underlying SOX10 enhancer activity during development and cancer progression. Using zebrafish as a model system, we identified and validated multiple SOX10 enhancer elements through ATAC-seq, CRISPR-mediated deletions, and enhancer-reporter assays. These studies revealed the spatiotemporal roles of individual enhancers in neural crest development and their reactivation in melanoma. Functional characterization of these enhancers highlighted their critical contributions to SOX10 expression, melanoma cell identity, and the dynamic process of phenotype switching, where melanoma cells transition between drug-sensitive and drug-resistant states. In human melanoma cell lines, deletion of conserved SOX10 enhancer elements led to significant transcriptional and phenotypic shifts, driving cells toward a more invasive, mesenchymal-like state associated with increased drug resistance. RNA-seq and gene set enrichment analyses identified key regulatory networks and candidate genes, that mediate these transitions. Notably, NTRK1 emerged as a promising therapeutic target, with its inhibition restoring drug sensitivity in phenotype-switched, resistant cells. This study further demonstrated the translational potential of cross-species genomic approaches by identifying human SOX10 enhancer elements with conserved functionality in zebrafish. Leveraging CRISPR-based tools, we established a workflow for dissecting enhancer activity and modulating gene expression with precision, offering a scalable method to uncover regulatory mechanisms in development and disease. By elucidating the role of SOX10 enhancers in melanoma plasticity and phenotype switching, this work advances our understanding of the epigenetic regulation of melanoma progression. It provides a foundation for developing novel therapeutic strategies that target enhancer elements to modulate melanoma cell states, combat drug resistance, and improve patient outcomes. This integrative approach underscores the critical importance of regulatory elements in shaping cellular identity, offering new avenues for intervention in melanoma and other neural crest-derived cancers.

Committee Chair

Charles Kaufman

Committee Members

Kristen Kroll; Lavinia Sheets; Michael Meers; Thor Theunnissen

Degree

Doctor of Philosophy (PhD)

Author's Department

Biology & Biomedical Sciences (Molecular Cell Biology)

Author's School

Graduate School of Arts and Sciences

Document Type

Dissertation

Date of Award

5-8-2025

Language

English (en)

Author's ORCID

https://orcid.org/0000-0002-2558-4829

Available for download on Wednesday, May 05, 2027

Included in

Biology Commons

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