Project ID CM-HD2026_25

ThemeCM-HD

Co Supervisor 1A Prof Eugene Makeyev Faculty of Life Sciences & Medicine, School of Basic & Medical Biosciences, Department of Medical & Molecular GeneticsEmail

Co Supervisor 1B Prof Claire Wells Faculty of Life Sciences & Medicine, School of Cancer and Pharmaceutical Sciences, Comprehensive Cancer Centre Email

Genomic instability and the assembly of cancer-specific RNA compartments

Cancer cells tend to accumulate mutations, increasing tumour heterogeneity and complicating therapeutic interventions. Such genetic instability is frequently observed for example in breast, ovarian, prostate, and pancreatic cancers. Previously, we identified a long non-coding RNA, PNCTR, which is significantly upregulated in many advanced and metastatic cancers (https://doi.org/10.1016/j.molcel.2018.08.041). We demonstrated that PNCTR promotes cancer cell survival by sequestering the RNA-binding protein PTBP1 within the membraneless perinucleolar compartment (PNC; https://doi.org/10.1080/19491034.2024.2306777).

Building on our preliminary data, this PhD project will test the hypothesis that elevated expression of PNCTR in cancer cells is associated with a genetic rearrangement of its locus. The project includes three major aims:

Aim 1 (Rotation/Years 1-2): Elucidating genetic requirements for PNCTR expression in cancer. To identify mutations associated with increased PNCTR expression, we will mine publicly available cancer genome/exome and RNA sequencing data using bioinformatics and machine learning. We will initially focus on breast cancer datasets, due to the prevalence of genetic instability in this disease. This will be followed by systematic analyses of other tumour types to identify an extended set of PNCTR “driver” genes. Predictions will be validated using quantitative (q)PCR, fluorescence in situ hybridisation (FISH), and immunofluorescence (IF) assays in clinically relevant cancer cell lines.

Aim 2 (Years 2-3): Dissecting DNA repair pathways involved in PNCTR locus rearrangement. Our data suggest that tumours may acquire PNCTR-expressing cells through error-prone resealing of double-strand breaks that often occur in this DNA region. We will use CRISPR/Cas reagents to introduce DNA breaks in PNCTR-negative cells and then analyze expression and locus structure by qPCR, FISH, and deep sequencing. We will further probe the role of different DNA repair pathways by using appropriate inhibitors and knockdown approaches.

Aim 3 (Years 3-4): Understanding the functional role of PNCTR and PNC in metastasis. Using CRISPR/Cas- or Cre/Lox-based genetic tools, we will “turn on” or “turn off” PNCTR expression and assess effects on migration and invasion using 2D assays and organoid models. We will correlate these behaviours with PNC assembly using FISH, IF, and live imaging.

This project offers comprehensive training in bioinformatics, functional genomics, gene editing, molecular imaging, and cancer modelling. The student will gain expertise across computational and experimental approaches, develop critical thinking and interdisciplinary collaboration skills, and be well-prepared for successful careers in both fundamental research and translational biomedical science.

Representative Publications

Yap K, Mukhina S, Zhang G, Tan JSC, Ong HS and Makeyev EV (2018) A Short Tandem Repeat-Enriched RNA Assembles a Nuclear Compartment to Control Alternative Splicing and Promote Cell Survival. Mol Cell 72:525-540.e13. doi: 10.1016/j.molcel.2018.08.041.

Yap K, Chung TH and Makeyev EV. (2022) Hybridization-proximity labeling reveals spatially ordered interactions of nuclear RNA compartments. Mol Cell 82:463-478.e11. doi: 10.1016/j.molcel.2021.10.009.

Makeyev EV and Huang S (2024) The perinucleolar compartment: structure, function, and utility in anti-cancer drug development. Nucleus 15:2306777. doi: 10.1080/19491034.2024.2306777.

Pipili A, Babteen NA, Kuwair L, Jannet MB, Quist J, Ong KKV, Pitaluga R, Grigoriadis AG, Tutt A and Wells CM (2024) PAK6 acts downstream of IQGAP3 to promote contractility in triple negative breast cancer cells. Cell Signal 121:111233. doi: 10.1016/j.cellsig.2024.111233.

Samain R, Maiques O, Monger J, Lam H, Candido J, George S, Ferrari N, KohIhammer L, Lunetto S, Varela A, Orgaz JL, Vilardell F, Olsina JJ, Matias-Guiu X, Sarker D, Biddle A, Balkwill FR, Eyles J, Wilkinson RW, Kocher HM, Calvo F, Wells CM and Sanz-Moreno V (2023) CD73 controls Myosin II-driven invasion, metastasis, and immunosuppression in amoeboid pancreatic cancer cells. Sci Adv 9:eadi0244. doi: 10.1126/sciadv.adi0244.

Best M, Gale ME and Wells CM (2022) PAK-dependent regulation of actin dynamics in breast cancer cells. Int J Biochem Cell Biol 146:106207. doi: 10.1016/j.biocel.2022.106207.