bims-gerecp Biomed News
on Gene regulatory networks of epithelial cell plasticity
Issue of 2025–04–13
sixteen papers selected by
Xiao Qin, University of Oxford



  1. Nature. 2025 Apr 09.
      In the same way that the mRNA-binding specificities of transfer RNAs define the genetic code, the DNA-binding specificities of transcription factors (TFs) form the molecular basis of the gene regulatory code1,2. The human gene regulatory code is much more complex than the genetic code, in particular because there are more than 1,600 TFs that commonly interact with each other. TF-TF interactions are required for specifying cell fate and executing cell-type-specific transcriptional programs. Despite this, the landscape of interactions between DNA-bound TFs is poorly defined. Here we map the biochemical interactions between DNA-bound TFs using CAP-SELEX, a method that can simultaneously identify individual TF binding preferences, TF-TF interactions and the DNA sequences that are bound by the interacting complexes. A screen of more than 58,000 TF-TF pairs identified 2,198 interacting TF pairs, 1,329 of which preferentially bound to their motifs arranged in a distinct spacing and/or orientation. We also discovered 1,131 TF-TF composite motifs that were markedly different from the motifs of the individual TFs. In total, we estimate that the screen identified between 18% and 47% of all human TF-TF motifs. The novel composite motifs we found were enriched in cell-type-specific elements, active in vivo and more likely to be formed between developmentally co-expressed TFs. Furthermore, TFs that define embryonic axes commonly interacted with different TFs and bound to distinct motifs, explaining how TFs with a similar specificity can define distinct cell types along developmental axes.
    DOI:  https://doi.org/10.1038/s41586-025-08844-z
  2. Cell Stem Cell. 2025 Apr 01. pii: S1934-5909(25)00095-5. [Epub ahead of print]
      Enterocytes and four classic secretory cell types derive from intestinal epithelial stem cells. Based on morphology, location, and canonical markers, goblet and Paneth cells are considered distinct secretory types. Here, we report high overlap in their transcripts and sites of accessible chromatin, in marked contrast to those of their enteroendocrine or tuft cell siblings. Mouse and human goblet and Paneth cells express extraordinary fractions of few antimicrobial genes, which reflect specific responses to local niches. Wnt signaling retains some ATOH1+ secretory cells in crypt bottoms, where the absence of BMP signaling potently induces Paneth features. Cells that migrate away from crypt bottoms encounter BMPs and thereby acquire goblet properties. These phenotypes and underlying accessible cis-elements interconvert in post-mitotic cells. Thus, goblet and Paneth properties represent alternative phenotypic manifestations of a common signal-responsive terminal cell type. These findings reveal exquisite niche-dependent cell plasticity and cis-regulatory dynamics in likely response to antimicrobial needs.
    Keywords:  Paneth cells; epigenetic control of cell properties; goblet cells; intestinal epithelial differentiation; intestinal stem cells; lineage plasticity
    DOI:  https://doi.org/10.1016/j.stem.2025.03.005
  3. Res Sq. 2025 Mar 27. pii: rs.3.rs-6081101. [Epub ahead of print]
      Chronic inflammation is a well-established risk factor for cancer, but the underlying molecular mechanisms remain unclear. Using a mouse model of colitis, we demonstrate that colonic stem cells retain an epigenetic memory of inflammation following disease resolution, characterized by a cumulative gain of activator protein 1 (AP-1) transcription factor activity. Further, we develop SHARE-TRACE, a method that enables simultaneous profiling of gene expression, chromatin accessibility and clonal history in single cells, enabling high resolution tracking of epigenomic memory. This reveals that inflammatory memory is propagated cell-intrinsically and inherited through stem cell lineages, with certain clones demonstrating dramatically stronger memory than others. Finally, we show that colitis primes stem cells for amplified expression of regenerative gene programs following oncogenic mutation that accelerate tumor growth. This includes a subpopulation of tumors that have exceptionally high AP-1 activity and the additional upregulation of pro-oncogenic programs. Together, our findings provide a mechanistic link between chronic inflammation and malignancy, revealing how long-lived epigenetic alterations in regenerative tissues may contribute to disease susceptibility and suggesting potential therapeutic strategies to mitigate cancer risk in patients with chronic inflammatory conditions.
    DOI:  https://doi.org/10.21203/rs.3.rs-6081101/v1
  4. Cancer Res. 2025 Apr 08.
      Epithelial-to-mesenchymal transition (EMT), a complex biological pathway that facilitates cellular plasticity, is used by tumor cells to enable metastasis and drug resistance. Our functional understanding of the impact of EMT on cancer has been limited by the lack of effective tools to ablate tumor cells as they become mesenchymal. In a recent study published in Nature, Perelli and colleagues used elegant genetically engineered lineage tracing and ablation strategies to track and eliminate tumor cells as they undergo EMT in pancreatic cancer. In a two-pronged approach, they queried the functional consequences of ablating EMT tumor cells before pancreatic ductal adenocarcinoma (PDAC) formation or in advanced PDAC tumors. These experiments collectively revealed that epithelial tumor cells only progress to low-grade lesions with minimal proliferative potential, while mesenchymal tumor cells undergo EMT early on to become malignant and metastasize. Profiling of mesenchymal tumor cell lineages revealed an altered chromatin landscape that leads to chromosomal instability (CIN) and disease progression. CIN is facilitated through complex structural rearrangements and chromothripsis, ultimately driving increased tumor heterogeneity and enhanced proliferation in EMT cells. This work reveals that EMT is an important driver of tumor heterogeneity and progression as a downstream consequence of CIN and provides mechanistic insight into how cellular plasticity can lead to genomic changes that drive disease progression.
    DOI:  https://doi.org/10.1158/0008-5472.CAN-25-1443
  5. J Pathol. 2025 Apr 11.
      Colorectal cancer (CRC) is the third most common form of cancer globally, and arises from the hyperproliferation of epithelial cells in the intestine. The architecture and maintenance of these cells is governed by two major signalling pathways working in a counter-gradient: the stem cell WNT signalling pathway, and the prodifferentiation bone morphogenetic protein (BMP) pathway. It has long been known that this WNT-BMP balance is disrupted in CRC, with hyperactive WNT signalling leading to increased proliferation of epithelial cells and tumour progression. BMP signalling, and its prodifferentiation effects, have increasingly become a focus for CRC research. Loss of BMP signalling, and that of its receptors, has been shown to increase WNT signalling and cancer stem cells in CRC. BMP signalling is further modulated through secreted BMP antagonists localised to the intestinal crypts, which create a niche ensuring that sustained WNT signalling can maintain stem-cell self-renewal capacity. A number of studies combine to demonstrate the effects of overexpression of these BMP antagonists, showing that hyperactivity of the stem-cell-supporting WNT signalling pathway ensues, leading to deregulation of the intestinal epithelium. Cellular hyperproliferation, the emergence of ectopic crypts, and an increase in stem cell numbers and characteristics are common themes, contributing to disrupted epithelial homeostasis, an increase in CRC risk and progression, and resistance to therapy. This review aims to compile the current knowledge on BMP antagonists, their role in CRC development, and how we can utilise this information for biomarker research and novel therapeutics. © 2025 The Author(s). The Journal of Pathology published by John Wiley & Sons Ltd on behalf of The Pathological Society of Great Britain and Ireland.
    Keywords:  BMP; BMP antagonists; WNT; cancer stem cells; cellular plasticity; colorectal cancer
    DOI:  https://doi.org/10.1002/path.6428
  6. Bioessays. 2025 Apr 10. e70005
      Cell plasticity enables the dynamic changes in cell identities necessary for normal development and tissue repair. Induced cell reprogramming, which leverages this plasticity, holds great promise for regenerative medicine and personalized therapies. However, the success of cell reprogramming is often impeded by various molecular barriers, such as epigenetic marks, cell senescence, and the activation of alternative or refractory routes. In this review, we examine the cell reprogramming events that occur within or between germ layers and adult stem cell lineages and propose that the overall similarity in the pre-existing chromatin accessibility landscape is a major determinant of reprogramming efficiency from one cell type to another. A better understanding of the regulation and control of chromatin accessibility should facilitate the development of new methods and strategies to improve cell reprogramming efficiency and advance translational research.
    Keywords:  cell reprogramming; chromatin accessibility; epigenetic memory; in vivo reprogramming; molecular barrier; senescence; transcription factor
    DOI:  https://doi.org/10.1002/bies.70005
  7. Genome Res. 2025 Apr 10. pii: gr.279955.124. [Epub ahead of print]
      Reprogramming cell state transitions provides the potential for cell engineering and regenerative therapy for many diseases. Finding the reprogramming transcription factors (TFs) and their combinations that can direct the desired state transition is crucial for the task. Computational methods have been developed to identify such reprogramming TFs. However, most of them can only generate a ranked list of individual TFs and ignore the identification of TF combinations. Even for individual reprogramming TF identification, current methods often fail to put the real effective reprogramming TFs at the top of their rankings. To address these challenges, we developed TFcomb, a computational method that leverages single-cell multiomics data to identify reprogramming TFs and TF combinations that can direct cell state transitions. We modeled the task of finding reprogramming TFs and their combinations as an inverse problem to enable searching for answers in very high dimensional space, and used Tikhonov regularization to guarantee the generalization ability of solutions. For the coefficient matrix of the model, we designed a graph attention network to augment gene regulatory networks built with single-cell RNA-seq and ATAC-seq data. Benchmarking experiments on data of human embryonic stem cells demonstrated superior performance of TFcomb against existing methods for identifying individual TFs. We curated datasets of multiple cell reprogramming cases and demonstrated that TFcomb can efficiently identify reprogramming TF combinations from a vast pool of potential combinations. We applied TFcomb on a dataset of mouse hair follicle development and found key TFs in cell differentiation. All experiments showed that TFcomb is powerful in identifying reprogramming TFs and TF combinations from single-cell datasets to empower future cell engineering.
    DOI:  https://doi.org/10.1101/gr.279955.124
  8. Cells. 2025 Apr 03. pii: 538. [Epub ahead of print]14(7):
      Stem cells have emerged as a pivotal area of research in the field of oncology, offering new insights into the mechanisms of cancer initiation, progression, and resistance to therapy. This review provides a comprehensive overview of the role of stem cells in cancer, focusing on cancer stem cells (CSCs), their characteristics, and their implications for cancer therapy. We discuss the origin and identification of CSCs, their role in tumorigenesis, metastasis, and drug resistance, and the potential therapeutic strategies targeting CSCs. Additionally, we explore the use of normal stem cells in cancer therapy, focusing on their role in tissue regeneration and their use as delivery vehicles for anticancer agents. Finally, we highlight the challenges and future directions in stem cell research in cancer.
    Keywords:  cancer; epigenetics; epithelial–mesenchymal transition (EMT); extracellular matrix (ECM); genetics; metastasis; signaling pathways; stem cells; tumor heterogeneity; tumor microenvironment
    DOI:  https://doi.org/10.3390/cells14070538
  9. NPJ Syst Biol Appl. 2025 Apr 10. 11(1): 31
      Epithelial-mesenchymal transition (EMT) is a cell state transition co-opted by cancer that drives metastasis via stable intermediate states. Here we study EMT dynamics to identify marker genes of highly metastatic intermediate cells via mathematical modeling with single-cell RNA sequencing (scRNA-seq) data. Across multiple tumor types and stimuli, we identified genes consistently upregulated in EMT intermediate states, many previously unrecognized as EMT markers. Bayesian parameter inference of a simple EMT mathematical model revealed tumor-specific transition rates, providing a framework to quantify EMT progression. Consensus analysis of differential expression, RNA velocity, and model-derived dynamics highlighted SFN and NRG1 as key regulators of intermediate EMT. Independent validation confirmed SFN as an intermediate state marker. Our approach integrates modeling and inference to identify genes associated with EMT dynamics, offering biomarkers and therapeutic targets to modulate tumor-promoting cell state transitions driven by EMT.
    DOI:  https://doi.org/10.1038/s41540-025-00512-2
  10. Cancer Cell. 2025 Apr 03. pii: S1535-6108(25)00122-9. [Epub ahead of print]
      Tumor-associated macrophages (TAMs) are key mediators of tumor immune evasion. However, their regulatory circuits and checkpoints are partially understood. Here, we generated a TAM regulatory network by integrating human tumors single-cell RNA sequencing (scRNA-seq) data with a dedicated CRISPR screen. Using a deep generative model, we constructed a gene perturbation network linking individual candidates with prototypical TAM functions. We identified Zeb2 as the master regulator of TAM programs, orchestrating suppression of type-I interferon response and antigen presentation alongside activation of immune suppression programs. Genetic ablation of ZEB2 reprograms TAM function and identity on the chromatin, RNA, and protein levels. In macrophage-rich human tumors, ZEB2 expression is associated with poor prognosis. Selective Zeb2 in vivo targeting reprograms TAMs and mobilizes systemic T cell responses, achieving robust tumor clearance. Overall, our study generates a detailed roadmap of TAM gene circuits and identifies ZEB2 as a master switch with therapeutic potential.
    Keywords:  CRISPR; TAM reprogramming; Zeb2; cancer immunology; cancer immunotherapy; deep generative modeling; regulatory network; single cell genomics; systems immunolgy; tumor-associated macrophage
    DOI:  https://doi.org/10.1016/j.ccell.2025.03.021
  11. Trends Cancer. 2025 Apr 03. pii: S2405-8033(25)00073-1. [Epub ahead of print]
      Tumoroids are cultures of patient-derived tumor cells, which are grown in 3D in the presence of an extracellular matrix extract and specific growth factors. Tumoroids can be generated from adult as well as pediatric cancers, including epithelial cancers, sarcomas, and brain cancers. Tumoroids retain multi-omic characteristics of their corresponding tumor and recapitulate interpatient and intratumor heterogeneity. Retrospective and prospective studies have demonstrated that tumoroids predict patient responses to anticancer therapies, making them a promising tool for precision oncology. However, several challenges remain before tumoroids can be fully integrated into clinical decision-making, including success rates of tumoroid establishment and turnaround times. This review discusses the current advances, challenges, and future directions of tumoroid-based models in cancer research and precision therapy.
    Keywords:  cancer organoid; personalized cancer treatment; tumoroid
    DOI:  https://doi.org/10.1016/j.trecan.2025.03.005
  12. Lab Invest. 2025 Apr 08. pii: S0023-6837(25)00082-0. [Epub ahead of print] 104172
      Ulcerative colitis (UC) is characterized by chronic relapsing inflammation starting from the rectum and distal colon, which in severe disease cases may affect the entire colon. Intestinal stem cells (ISCs) directly isolated from inflamed UC colonic tissue specimens have been found to present an inflammatory gene expression profile. However, a critical issue is whether these cells retain memory of exposure to inflammation and/or therapeutics. Here, we aimed to investigate whether human intestinal epithelial cells retain the inflammatory state observed in vivo when expanded in vitro as 3D cultured organoids to assess their suitability for therapeutic transplantation. ISCs were isolated from non-inflammatory bowel disease controls (non-inflamed; n = 18), as well as from colonoscopy-obtained biopsies of the sigmoid colon from individuals diagnosed with UC (inflamed), who were glucocorticoid-naïve (n = 19). Moreover, ISCs were collected from all patients with inflammatory bowel disease following prednisolone treatment. Epithelial cells were cultured as 3D intestinal organoids in media to support stem cell maintenance and differentiation. Subsequently, the 3D intestinal organoids were harvested at the end of passage two for bulk RNA sequencing. The data revealed that the cellular phenotype of in vitro-cultured epithelial cells isolated from inflamed tissue did not maintain the hallmarks of inflammation observed in the ulcerated environment from which the cells were initially obtained. Our findings indicate that the autologous reinsertion of in vitro-expanded ISCs in active stages of UC may aid in intestinal healing, which calls for future clinical studies. Additionally, a link between organoid morphology and the inflammatory state of the tissue of origin was identified, as organoids derived from inflamed colon exhibited a lower degree of circularity.
    Keywords:  Cellular memory; RNA sequencing; in vitro organoid cultures; inflammatory bowel disease; intestinal stem cells; organoid morphology; prednisolone; ulcerative colitis
    DOI:  https://doi.org/10.1016/j.labinv.2025.104172
  13. Tissue Eng Part B Rev. 2025 Apr 08.
      Colorectal cancer (CRC) recurs at a striking rate, specifically in patients with liver metastasis. Dormant CRC cells disseminated following initial primary tumor resection or treatment often resurface years later to form aggressive, therapy-resistant tumors that result in high patient mortality. Routine imaging-based screenings often fail to detect dormant cancer cell clusters, and there are no overt symptomatic presentations, making dormant CRC a major clinical challenge to diagnose and treat. Tissue engineering approaches are ideally suited to model dormant cancer cells and enable the discovery of therapeutic vulnerabilities or unique mechanistic dependencies of dormant CRC. Emerging evidence suggests that tissue-engineered approaches have been successfully used to model dormant breast and lung cancer. With CRC responsible for the second most cancer-related deaths worldwide and CRC patients commonly experiencing recurrence, it is essential to expand dormancy models to understand this phenomenon in the context of CRC. Most published in vitro models of CRC dormancy simplify the complex tumor microenvironment with two-dimensional culture systems to elucidate dormancy-driving mechanisms. Building on this foundation, future research should apply tissue engineering methods to this growing field to generate competent three-dimensional models and increase mechanistic knowledge. This review summarizes the current state of in vitro CRC dormancy models, highlighting the techniques utilized to give rise to dormant CRC cells: nutrient depletion, anticancer drugs, physical extracellular matrix interactions, and genetic manipulation. The metrics used to validate dormancy within each model are also consolidated to demonstrate the lack of established standards and the ambiguity around comparing studies that have been validated differently. The methods of these studies are organized in this review to increase comprehensibility and identify needs and opportunities for future bioengineered in vitro models to address dormancy-driven mortality in patients with CRC liver metastasis. Impact Statement Dormant cancer drives high patient mortality, especially in metastatic colorectal cancer, owing to the clinical inability to identify dormant cells prior to their overt recurrence. Lacking clinical insights, in vitro modeling for mechanistic and therapeutic discovery is hindered. Here, we review models and methods of inducing colorectal cancer dormancy with the goal of consolidating findings for reference. We also highlight the need for advanced, tissue-engineered models to better mimic the organ-specific 3D microenvironment of metastatic colorectal cancer. New models would enable breakthroughs in understanding mechanisms driving dormancy progression and reversal, thereby providing context for therapeutic advances to improve patient survival.
    Keywords:  colorectal cancer; dormancy; in vitro; models; tissue engineering
    DOI:  https://doi.org/10.1089/ten.teb.2025.0009
  14. Front Pharmacol. 2025 ;16 1563198
      The persistently high mortality rates associated with cancer underscore the imperative need for innovative, efficacious, and safer therapeutic agents, as well as a more nuanced understanding of tumor biology. Patient-derived organoids (PDOs) have emerged as innovative preclinical models with significant translational potential, capable of accurately recapitulating the structural, functional, and heterogeneous characteristics of primary tumors. When integrated with cutting-edge genomic tools such as CRISPR, PDOs provide a powerful platform for identifying cancer driver genes and novel therapeutic targets. This comprehensive review delves into recent advancements in CRISPR-mediated functional screens leveraging PDOs across diverse cancer types, highlighting their pivotal role in high-throughput functional genomics and tumor microenvironment (TME) modeling. Furthermore, this review highlights the synergistic potential of integrating PDOs with CRISPR screens in cancer immunotherapy, focusing on uncovering immune evasion mechanisms and improving the efficacy of immunotherapeutic approaches. Together, these cutting-edge technologies offer significant promise for advancing precision oncology.
    Keywords:  CRISPR screening; cancer treatment; immunotherapy; patient-derived organoids; precision medicine
    DOI:  https://doi.org/10.3389/fphar.2025.1563198
  15. Front Immunol. 2025 ;16 1526668
      Colorectal cancer (CRC) is one of the most common malignant tumors of the digestive tract, with increasing incidence and mortality rates, posing a significant burden on human health. Its progression relies on various mechanisms, among which the tumor microenvironment and tumor-associated macrophages (TAMs) have garnered increasing attention. Macrophage infiltration in various solid tumors is associated with poor prognosis and is linked to chemotherapy resistance in many cancers. These significant biological behaviors depend on the heterogeneity of macrophages. Tumor-promoting TAMs comprise subpopulations characterized by distinct markers and unique transcriptional profiles, rendering them potential targets for anticancer therapies through either depletion or reprogramming from a pro-tumoral to an anti-tumoral state. Single-cell RNA sequencing technology has significantly enhanced our research resolution, breaking the traditional simplistic definitions of macrophage subtypes and deepening our understanding of the diversity within TAMs. However, a unified elucidation of the nomenclature and molecular characteristics associated with this diversity remains lacking. In this review, we assess the application of conventional macrophage polarization subtypes in colorectal malignancies and explore several unique subtypes defined from a single-cell omics perspective in recent years, categorizing them based on their potential functions.
    Keywords:  M2-macrophage; colorectal cancer; single-cell RNA sequencing; tumor microenvironment; tumor-associated macrophages
    DOI:  https://doi.org/10.3389/fimmu.2025.1526668
  16. Nature. 2025 Apr;640(8058): 555-557
      
    Keywords:  Careers; Information technology; Institutions; Machine learning; Research management
    DOI:  https://doi.org/10.1038/d41586-025-01069-0