Search bioRxiv⌕ Search

bioRxiv · 10.1101/2024.10.10.617550

Loss of PKCtheta-GADD45a axis drives triple-negative breast cancer cells into p53-independent senescence

Abstract

BackgroundPKC{theta} is a serine/threonine kinase that is well known for its role in the immune system. However, increasing evidence implicates PKC{theta} in the pathology of breast cancer. PKC{theta} is highly expressed in triple negative breast cancer (TNBC) cells in which it controls cell migration and invasion, while its implication in cell proliferation remains poorly understood. MethodsTo determine the function of PKC{theta} in cell proliferation, siRNAs were used to modulate the expression of PKC{theta} in TNBC cells (MDA-MB-231, MDA-MB-436, HCC1937) and cell growth was examined by clonogenic and EdU assays. {beta}-galactosidase assay, RT-qPCR and western blot were used to characterize the senescence features. PCR microarrays and rescue experiments were conducted to investigate the underlying mechanism. ResultsWe show that PKC{theta} inhibition leads to a growth arrest in TNBC cells harboring a p53 loss-of-function mutation. This p53-independent growth arrest is accompanied by an increased activity of senescence-associated {beta}-galactosidase, the presence of a senescence-associated secretory phenotype, and the striking expression change of various genes implicated in cell proliferation and senescence. Thus, our data show that PKC{theta} silencing drives TNBC cells into a senescence-like phenotype. Mechanistically, we demonstrate that p27 is the main CDK inhibitor controlling the PKC{theta} loss-induced senescence. The accumulation of p27 is due to a surprising strong reduction in GADD45a expression. Indeed, similar to PKC{theta} silencing phenotype, GADD45a knockdown drives TNBC cells into a senescence-like phenotype. ConclusionsAltogether, our study highlights that the loss of PKC{theta}-GADD45a axis triggers a p27-dependent senescence response in TNBC cells and further supports strategies targeting PKC{theta} as treatment for this type of aggressive breast cancer.

Explore related subjects

Keep this discovery

Explore connections, maps & timelines

BibTeXRIS

Nicolle, A., Zhang, Y., Choesmel-Cadamuro, V., Wang, X., Belguise, K.. 2024-10-11. Loss of PKCtheta-GADD45a axis drives triple-negative breast cancer cells into p53-independent senescence. https://doi.org/10.1101/2024.10.10.617550

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

KEEP EXPLORING

Related preprints

Epigenetic progression of pancreatic cancer to aggressive subtypes involves alternate routes of lineage reprogramming in subtype-intermediate progenitor cells

Pancreatic ductal adenocarcinoma (PDAC) progression involves malignant cell state plasticity. Epigenetic changes underlie this plasticity, yet the PDAC cis-regulatory landscape remains understudied. To address this, we profiled 33 primary tumors and 7 metastases from 39 patients with single-cell ATAC-seq, paired with 10 single-cell RNA-seq profiles. We found that epigenetic GATA6+/KRT17+ co-accessibility identifies a classical-basal subtype-intermediate progenitor state (SIP) associated with better clinical outcomes. SIP cells display limited epigenetic reprogramming from premalignant epithelium and retain gastric-intestinal differentiation reminiscent of neoplastic precursors. Lineages without GATA6+/KRT17+ co-accessibility exhibit greater lineage and epithelial-mesenchymal plasticity. Classical PDACs that repress basal gene accessibility activate neural-like progenitor (NRP) and tuft lineage enhancers, whereas basal committed tumors display esophageal transdifferentiation. Compared to SIP, classical-NRP and basal committed tumors have poorer outcomes, and show distinct PD-1/PD-L1 immune proteomic phenotypes and prognostic myofibroblast epigenetic states, respectively. Our work reveals links between lineage reprogramming, EMT, and epigenetic progression in human PDAC.

cancer biology↗

Tissue resident CD4+ memory T-cells mark response to immune checkpoint inhibition in high-grade glioma

Background: Immune checkpoint inhibitors (ICI) are efficacious in many solid tumors, but response in glioma is restricted to a small subgroup. The determinants of response and resistance to ICI remain poorly understood. Methods: Here we exploit a syngeneic hypermutated high-grade glioma model with dichotomous response to combined PD-1 and CTLA-4 inhibition to unravel determinants of tumor-infiltrating T-cells driving response. Tumor-infiltrating T-cells from ICI-responsive and non-responsive tumors were analyzed by single-cell RNA and T-cell receptor sequencing and tumor-reactive T-cell receptor clonotypes were functionally validated to characterize their transcriptional phenotypes. We verify our findings in IDH1 wildtype glioblastoma patients treated with neoadjuvant pembrolizumab. Results: ICI response was associated with intratumoral clonal expansion of tumor-reactive cytotoxic T-cells and increased infiltration of CXCR6+ CD4+ tissue resident memory T-cells (Trm). CD4 stem-like memory T-cells in responding tumors demonstrated elevated interferon responses, following trajectories toward clonally expanded Trm, versus trajectories toward exhaustion in non-responsive tumors. In responsive tumors, CD4+ Trm interacted with infiltrating CXCR3+ tumor-reactive and clonally expanded, yet transcriptionally versatile cytotoxic T-cells. Probing the post neoadjuvant ICI high-grade glioma patient tissue dataset, we confirmed increased CXCR6 expression in CD4+ T cells and the association of CD4+ Trm with prolonged overall survival. Conclusion: These findings identify CD4 tissue-resident memory T-cells as determinants of ICI response in IDH1 wildtype high-grade glioma and warrant their further investigation to improve immunotherapy outcomes.

cancer biology↗

Low-dose doxorubicin drives caveolin-1 depended re-epithelialization of breast cancer cells as a mechanism of cancer plasticity

Breast cancer progression is driven by dynamic changes in epithelial plasticity, membrane organization, and intracellular signaling, yet the effects of sustained low-dose chemotherapy on these processes remain poorly understood. Here, we investigated the impact of prolonged low-dose doxorubicin on membrane remodeling, epithelial phenotype, membrane-associated Ras lipid-anchor localization, and autophagy in mesenchymal-like MDA-MB-231 breast cancer cells. Low-dose doxorubicin significantly increased Caveolin-1 expression and enhanced E-cadherin protein levels, accompanied by a transition toward a more compact epithelial-like morphology with increased cell-cell contacts. Live-cell imaging demonstrated a significant reduction in the membrane-to-cytoplasm fluorescence ratio of the lipid-anchored GFP-tH probe, indicating redistribution from the plasma membrane to the cytoplasm following treatment. Analysis of autophagy-related proteins revealed decreased LC3-I together with increased LC3-II, ATG5, and p62 expression, consistent with autophagosome accumulation and impaired autophagic flux. Collectively, our findings demonstrate that low-dose doxorubicin promotes extensive remodeling of plasma membrane organization, epithelial plasticity, membrane-associated lipid-anchor localization, and autophagy. This integrated response reveals previously unrecognized links between membrane architecture, Ras membrane association, and autophagy during phenotypic reprogramming of breast cancer cells, providing mechanistic insight into cellular adaptations elicited by sub-cytotoxic doxorubicin exposure.

cancer biology↗