Graduation Date

Spring 5-9-2026

Document Type

Dissertation

Degree Name

Doctor of Philosophy (PhD)

Programs

Molecular Genetics & Cell Biology

First Advisor

Kishor K. Bhakat

Second Advisor

Vimla Band

Third Advisor

Kyle Hewitt

Fourth Advisor

M. Jordan Rowley

Abstract

G-quadruplexes (G4s) are non-canonical secondary DNA structures and are prevalently present on oncogene promoters and enhancers, suggesting a crucial role in regulating oncogene expression and tumorigenesis. Genome-wide bioinformatic studies revealed that G4s positively correlated with elevated gene expression, while G4-ligand- based studies showed that G4 stabilization inhibited transcription. The controversial observations raise our interest in straightening G4’s regulatory role on native chromatin context, which will help clear the ambiguity of G4’s effect on gene expression. Our lab has long focused on G4 biology and identified a G4 binding partner, APE1, a multifunctional protein with DNA damage repair activity and reduction-oxidation (redox) activity. Both G4 and APE1 were found to be elevated in aggressive triple-negative breast cancer (TNBC), while whether G4 and APE1 coordinate to regulate oncogene expression and affect tumor malignancy is not known.

Herein, we provide direct genetic evidence that endogenous promoter G4 structures are favorable to drive oncogene expression through a novel regulatory mechanism. Using endogenous CXCL1 as a model gene, a key oncogene for breast cancer progression and metastasis, we demonstrated that CRISPR-Cas9-mediated G4 loss at the CXCL1 promoter led to remarkable downregulation of CXCL1 expression as well as inhibition of cellular functions such as cell migration and invasion. Mechanistically, we revealed that G4 and APE1 colocalized in certain oncogene promoters, and G4 recruited APE1 to gene promoters through interaction with APE1’s unstructured N-terminal domain. Subsequently, APE1’s redox activity drives a pro-metastatic gene expression program. Many G4 ligands, such as TMPyP4, PDS, and PhenDC3, blocked G4-APE1 interaction both in vitro and in the cell context. G4 mutation, APE1 deletion, or disruption of the G4-APE1 interaction by TMPyP4 suppressed gene expression, cellular functions, and in vivo metastatic dissemination. Altogether, our study provided compelling evidence that a single G4 motif in the CXCL1 promoter was essential for CXCL1 expression, and that the G4-APE1 axis was a promising therapeutic target to constrain certain oncogene activation and inhibit tumor malignancy in TNBC.

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Available for download on Sunday, April 23, 2028

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