Search bioRxiv⌕ Search

bioRxiv · 10.1101/2024.05.21.595102

Pro-survival roles for p21(Cip1/Waf1) in Non-Small Cell Lung Cancer

Abstract

Quiescence is a reversible state of proliferative arrest, distinct from senescence. While cancer is a disease of dysregulated proliferation, cancer cells can retain the ability to enter quiescence which confers advantages to tumour cells by protecting them from chemotherapy or by allowing metastasis to distant sites. Multiple mechanisms exist to induce and maintain quiescence that are not yet fully understood. Here, we show that high expression of the CDK inhibitor p21Cip1/Waf1 correlates with a poor prognosis in TP53 wild-type, but not TP53 mutant, non-small cell lung cancer (NSCLC) patients. Using quantitative single-cell imaging of genetically-engineered NSCLC reporter cell lines, we show that TP53 wild-type NSCLC cells can enter a p21-dependent spontaneous quiescent state, downstream of replication stress. Furthermore, p21 expression confers survival advantages to TP53 wild-type NSCLC cells, both under normal proliferation and in response to chemotherapy. We also show that p21 can promote tumour relapse by allowing cells to recover from both G1 and G2 arrest states after drug removal. Together, our data suggest that targeting p21 function in TP53 wild-type tumours could lead to better outcomes for chemotherapy treatment in NSCLC patients. Statement of SignificanceWe show that TP53WT Non-Small Cell Lung Cancer cells can enter a p21-dependent spontaneous quiescent state and that p21 maintains the viability of NSCLC cells, is chemoprotective and can promote tumour relapse.

Source connections

Explore related subjects

Keep this discovery

Explore connections, maps & timelines

BibTeXRIS

Cutty, S. J., Hughes, F. A., Ortega-Prieto, P., Desai, S., Thomas, P., Fets, L. V., Secrier, M., Barr, A. R.. 2024-05-21. Pro-survival roles for p21(Cip1/Waf1) in Non-Small Cell Lung Cancer. https://doi.org/10.1101/2024.05.21.595102

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related preprints

mRNA-LNP vaccination induces microenvironment remodeling and generation of tissue-resident memory T cells in glioblastoma

Glioblastoma remains highly refractory to immunotherapy, in part because of a profoundly immunosuppressive tumour microenvironment that limits effective T-cell responses. Although mRNA vaccines can induce anti-tumour immunity, how they reshape the glioblastoma immune ecosystem to support durable tumour control is not well understood. Here we use an immunocompetent EGFRvIII-driven syngeneic glioblastoma model and antigen-specific mRNA lipid nanoparticle (mRNA-LNP) vaccination to define the cellular and spatial mechanisms underlying therapeutic response. In our model, vaccination induced durable EGFRvIII-specific humoral and cellular immunity, resulting in complete tumour eradication and long-term protection against intracranial rechallenge. Integrative analyses incorporating flow cytometry, tumour interstitial fluid profiling, multiplex immunostaining, spatial transcriptomics and ligand-receptor modelling demonstrated extensive remodelling of the tumour microenvironment following vaccination. Early tumour control was associated with expansion of pro-inflammatory and antigen-presenting myeloid populations, increased cytotoxic CD8 T-cell infiltration and activation, enhanced interferon-responsive signalling, and the formation of immune-supportive spatial niches enriched for antigen presentation and chemokine-mediated cellular communication. Vaccination promoted inflammatory chemokine relay networks centred on the CXCL16-CXCR6 axis, a pathway linked to tissue residency programming in the central nervous system. Functional depletion studies identified CD4 and CD8 T cells as essential mediators of therapeutic efficacy, while durable protection was maintained by tumour-specific brain-resident memory CD8 T cells that persisted despite peripheral lymphocyte depletion. Together, these findings identify T-cell-driven microenvironmental remodelling as a critical mechanism linking mRNA vaccination to the establishment of long-term brain-resident anti-tumour immunity in glioblastoma.

cancer biology↗

Regulation of the Epstein-Barr Epigenome by Histone Variant MacroH2A

Histone variants play an important role in regulating chromatin dynamics of Epstein-Barr Virus (EBV). Here, we investigate the role of histone variant macroH2A in EBV chromatin structure, gene expression and copy number control during latent infection. ChIP-seq analysis in EBV+ SNU719 gastric carcinoma and Mutu I Burkitt lymphoma cells revealed that macroH2A was most enriched at repetitive DNA elements, including oriLyt, BHLF1, LF3 and terminal repeat (TR) regions of the EBV genome. MacroH2A depletion in EBV-associated gastric cancer cell line SNU719 led to a small increase in some viral lytic genes and increase in viral DNA copy number. RNAseq transcriptomics after macroH2A depletion identified major perturbations in cellular gene pathways, including beta-catenin/TCF signaling and chromatin remodeling. Depletion of macroH2A during EBV lytic reactivation reduced EBV lytic gene activation, but increased EBV DNA copy number. Previous study demonstrated a colocalization and cooperative binding between histone variant H2A.Z and EBNA1. We now show that depletion of macroH2A causes an increase in both H2A.Z and EBNA1 at oriP and cellular binding sites for EBNA1. We also found that gammaH2AX localizes to oriP and that this depends on macroH2A. Finally, we show that CRISPR/Cas9 knockout of macroH2A increases the replication and episome maintenance of oriP-containing plasmids. Taken together, these findings indicate that macroH2A localizes to the repetitive elements of EBV, including oriLyt, and can function to limit H2A.Z and EBNA1 binding at oriP, which alters DNA damage signaling at oriP and limits episomal replication. These findings provide a novel role for macroH2A in maintaining EBV copy number and genome integrity.

cancer biology↗

Epigenomic circuits shaping cellular heterogeneity in pleural mesothelioma

Pleural mesothelioma (PM) is an aggressive and lethal malignancy with current treatments offering limited clinical benefit. In this study, we utilized single-cell chromatin accessibility and transcriptomic profiling of patient-matched samples to infer the epigenomic regulation underlying cellular heterogeneity in PM. High-resolution epigenomic profiling suggested transcriptional regulators with putative pro-tumoral roles in mesothelioma, whose function was experimentally tested using genetic perturbations across four PM cell lines. Furthermore, we observed several putative associations between epigenomic circuits and macrophage ontogeny, a sarcomatoid-like neoplastic state, and a fetal-like endothelial cell state. Our analysis also showed similarities between the chromatin accessibility landscapes of exhausted CD8 T and KLRC1 natural killer cells and identified NR4A2 as a potential shared regulator of dysfunction in both lymphocyte subsets. We further identified a state-specific distal enhancer near NR4A2 and experimentally validated its regulation of NR4A2 expression in Jurkat cells. Together, we provide an epigenomic map of PM and nominate candidate transcription factors and regulatory elements for future functional investigation, including their potential relevance to epigenetic editing strategies to limit tumor growth and enhance anti-tumor immunity.

cancer biology↗