bims-unfpre Biomed News
on Unfolded protein response
Issue of 2025–02–09
nine papers selected by
Susan Logue, University of Manitoba



  1. Cell Commun Signal. 2025 Feb 07. 23(1): 66
       BACKGROUND: Fibrosis remains a major complication in several chronic diseases, including systemic sclerosis (SSc). Plasmacytoid dendritic cells (pDCs) are innate immune cells that play a key role in the development of fibrosis in SSc patients, through still poorly defined mechanisms. Interestingly, endoplasmic reticulum (ER) stress signaling pathways are dysregulated in pDCs from patients with SSc, but their contribution to fibrosis remains unclear. Thus, this study aimed to unravel the mechanisms behind the involvement of pDCs and ER stress in fibrosis.
    METHODS: To address this question, we established an in vitro model designed to study the interactions between pDCs and fibroblasts. More specifically, IMR-90 fibroblasts were co-cultured with CAL-1, a pDC cell line. ER stress was then induced by the bacterial toxin SubAB. Extracellular matrix (ECM) production was assessed using immunoblotting, qPCR and confocal microscopy. The importance of cell-to-cell contact was investigated using conditioned media (CM) and transwell assays.
    RESULTS: Direct contact of CAL-1 and IMR-90 cells under ER stress conditions led to increased expression of fibronectin and alpha-smooth muscle actin (α-SMA). This effect required expression of the ER stress signaling sensor protein kinase R-like ER kinase (PERK) in pDCs and was observed only upon direct contact between both cell types.
    CONCLUSIONS: Overall, our data suggest that ER stress induction in pDCs promotes fibroblast activation, which may contribute to the development of fibrosis in SSc.
    Keywords:  Cell-cell communication; ER stress; Fibroblasts; Fibrosis; Interstitial lung disease; PERK; Plasmacytoid dendritic cells; Scleroderma; UPR
    DOI:  https://doi.org/10.1186/s12964-025-02057-7
  2. RSC Med Chem. 2025 Jan 23.
      The endoplasmic reticulum (ER) is a vital subcellular organelle that orchestrates numerous essential biological processes, including protein synthesis and processing. Disruption of ER function can lead to ER stress, a condition closely associated with the progression and development of cancer. Consequently, inducing ER stress in cancer cells has emerged as an unconventional yet promising therapeutic approach. However, selectively targeting the ER within cancer cells remains a significant challenge. To address this, we have designed and synthesized a novel small-molecule library composed of non-steroidal anti-inflammatory drugs (NSAIDs), fluorescent probes, and ER-targeting moieties. Through screening the library in cancer cells, we identified a promising compound: an ibuprofen derivative conjugated with a dansyl group as a dual fluorescence tag and ER-targeting moiety. This ibuprofen derivative successfully localized into the ER of HCT-116 colon cancer cells within 3 h, induced ER stress by upregulating key stress markers such as CHOP, GRP94, IRE-1α, PERK, and Cas-12, while simultaneously inhibiting Cox-2. The resulting ER stress triggered autophagy by upregulating Beclin and LC3-II/LC3-I as autophagy markers, followed by apoptosis, culminating in significant cancer cell death, particularly when combined with bafilomycin A, 10-hydroxycamptothecin and obatoclax. This NSAID-based ER stress inducer provides a powerful tool for exploring the chemical biology of NSAIDs in the ER and holds great potential for advancing ER-targeted cancer therapies in combination with other anti-cancer drugs.
    DOI:  https://doi.org/10.1039/d4md00936c
  3. J Invest Dermatol. 2025 Feb 03. pii: S0022-202X(25)00085-5. [Epub ahead of print]
      Desmosomes are intercellular junctions that mediate cell-cell adhesion and are essential for maintaining tissue integrity. Pemphigus vulgaris (PV) is an autoimmune epidermal blistering disease caused by autoantibodies (IgG) targeting desmoglein 3 (Dsg3), a desmosomal cadherin. PV autoantibodies cause desmosome disassembly and loss of cell-cell adhesion, but the molecular signaling pathways that regulate these processes are not fully understood. Using high-resolution time-lapse imaging of live keratinocytes, we found that ER tubules make frequent and persistent contacts with internalizing Dsg3 puncta in keratinocytes treated with PV patient IgG. Biochemical experiments demonstrated that PV IgG activated ER stress signaling pathways, including both IRE1⍺ and PERK pathways, in cultured keratinocytes. Further, ER stress transcripts were upregulated in PV patient skin. Pharmacological inhibition of ER stress protected against PV IgG-induced desmosome disruption and loss of keratinocyte cell-cell adhesion, suggesting that ER stress may be an important pathomechanism and a therapeutically targetable pathway for PV treatment. These data support a model in which desmosome adhesion is integrated with ER function to serve as a cell adhesion stress sensor that is activated in blistering skin disease.
    Keywords:  ER stress; cadherins; desmosomes; endoplasmic reticulum; pemphigus
    DOI:  https://doi.org/10.1016/j.jid.2024.12.028
  4. J Neurosci. 2025 Feb 07. pii: e1406242025. [Epub ahead of print]
      Endoplasmic reticulum (ER) stress is crucial in cerebral ischemia/reperfusion injury by triggering cellular apoptosis and exacerbating neuronal damage. This study elucidates the dynamics of TP53-induced glycolysis and apoptosis regulator (TIGAR) translocation and its role in regulating neural fate during cerebral ischemia-induced ER stress, specifically in male mice. We found enhanced nuclear localization of TIGAR in neurons after transient middle cerebral artery occlusion/reperfusion (tMCAO/R) in male mice, as well as oxygen glucose deprivation/reperfusion (OGD/R) and treatment with ER stress inducer (tunicamycin and thapsigargin) in neuronal cells. Conditional neuronal knockdown of Tigar aggravated the injury following ischemia-reperfusion, whereas overexpression of Tigar attenuated cerebral ischemic injury and ameliorated intra-neuronal ER stress. Additionally, TIGAR overexpression reduced the elevation of ATF4 target genes and attenuated ER stress-induced cell death. Notably, TIGAR co-localized and interacted with ATF4 in the nucleus, inhibiting its downstream pro-apoptotic gene transcription, consequently protecting against ischemic injury. In vitro and in vivo experiments revealed that ATF4 overexpression reversed the protective effects of TIGAR against cerebral ischemic injury. Intriguingly, our study identified the Q141/K145 residues of TIGAR, crucial for its nuclear translocation and interaction with ATF4, highlighting a novel aspect of TIGAR's function distinct from its known phosphatase activity or mitochondrial localization domains. These findings reveal a novel neuroprotective mechanism of TIGAR in regulating ER stress through ATF4-mediated signaling pathways. These insights may guide targeted therapeutic strategies to protect neuronal function and alleviate the deleterious effects of cerebral ischemic injury.Significance statement TIGAR (TP53-induced glycolysis and apoptosis regulator) is one of the downstream target genes of p53, and its encoded protein exerts Fru-2, 6-BPase activity to promote glucose metabolic flux to pentose phosphate pathway. However, the non-enzymatic function of TIGAR has been gradually discovered. Here, we demonstrate that TIGAR translocates to the nucleus to interact with ATF4 in neurons after cerebral ischemia/reperfusion induced ER stress via its Q141/K145 residues. Then TIGAR inhibits ATF4's downstream pro-apoptotic genes expression, reduces ER stress-dependent apoptosis, consequently alleviating neuronal damage. This study uncovered a novel neuroprotective mechanism of TIGAR by regulating ER stress via ATF4-mediated signaling pathway. The Q141/K145 residues of TIGAR are critical for its interaction with ATF4 and inhibition of ATF4 target genes.
    DOI:  https://doi.org/10.1523/JNEUROSCI.1406-24.2025
  5. Cell Death Discov. 2025 Feb 04. 11(1): 42
      In tumors, cancer cells are frequently exposed to adverse environmental conditions that result in endoplasmic reticulum (ER) stress. Mechanical signals emerging from extracellular matrix (ECM) rigidity and cell shape regulate the activity of transcriptional co-activators Yes-associated protein (YAP) and its paralog Transcriptional Coactivator with PDZ-binding motif (TAZ). However, the role of ECM rigidity and YAP/TAZ in tumor cell fate decisions under ER stress remains relatively unexplored. Our results suggest that the YAP/TAZ system plays an important role in the control of ER stress-induced cell death by mechanical signaling arising from ECM stiffness in tumor cells. Mechanistically, YAP/TAZ regulates apoptosis induced by ER stress in tumor cells by controlling the activation of the TRAIL-R2/DR5-mediated extrinsic apoptotic pathway through a dual mechanism. On the one hand, the YAP/TAZ system prevents intracellular TRAIL-R2/DR5 clustering in tumor cells. On the other hand, it inhibits cFLIP down-regulation in tumor cells experiencing ER stress. In addition, YAP/TAZ controls the expression of pro-inflammatory interleukin-8 (IL-8/CXCL8) in tumor cells undergoing ER stress by a TRAIL-R2/DR5/caspase-8-dependent mechanism. Although other mechanisms may also be involved in controlling cell death and inflammation in tumor cells facing environmental stress, our results support a model in which regulation of the subcellular localization and activity of the YAP/TAZ transcriptional co-activators could contribute to the microenvironmental control of cell fate decisions in tumor cells undergoing ER stress.
    DOI:  https://doi.org/10.1038/s41420-025-02335-w
  6. J Clin Invest. 2025 Feb 03. pii: e188708. [Epub ahead of print]135(3):
      Sensorineural hearing loss (SNHL) is the most prevalent form of permanent hearing impairment, arising from factors such as aging, exposure to loud noise, disease, ototoxic medications, and genetic mutations. Despite extensive research, effective treatments or cures for SNHL remain elusive. In this issue of the JCI, Lee et al. reveal a link between mutations in ATF6 and SNHL in patients with achromatopsia. The study also shows that Atf6-deficient (Atf6-/-) mice exhibit disorganized stereocilia and age-related loss of outer hair cells. Additionally, the researchers show that Atf6 is critical for cochlear hair cell function. Mice lacking Atf6 expression experienced ER stress, which ultimately led to SNHL. Collectively, these findings enhance our understanding of the emerging role of protein homeostasis and ER stress in the pathogenesis of SNHL.
    DOI:  https://doi.org/10.1172/JCI188708
  7. Apoptosis. 2025 Feb 04.
       BACKGROUND: Colorectal cancer (CRC) represents a significant global health burden, with chemotherapy resistance representing a significant challenge to effective treatment. SEC23A, a core component of the COPII vesicle trafficking system, is of critical importance with regard to protein transport and cellular homeostasis. Nevertheless, its function in CRC progression and chemoresistance remains uncertain. The present study investigates the correlation between SEC23A expression and sensitivity to 5-fluorouracil (5-FU), a widely used chemotherapeutic agent, with particular emphasis on ER stress-induced apoptosis.
    METHODS: A bioinformatic analysis was conducted to evaluate SEC23A expression in CRC and its association with patient prognosis. Chemotherapy sensitivity was predicted using GDSC data and validated experimentally using CRC cell lines with manipulated SEC23A expression. In order to explore the role of SEC23A in acquired drug resistance, patient-derived xenograft (PDX) models and 5-FU-resistant cell lines were employed. Apoptosis assays, cell cycle analysis, and ER stress modulation experiments were performed to elucidate the underlying mechanisms.
    RESULTS: SEC23A expression was significantly reduced in CRC samples compared to normal tissues. This reduction was linked to a poorer prognosis, including both overall and disease-specific survival. A correlation was observed between low SEC23A expression and increased resistance to 5-FU, as evidenced by both bioinformatic predictions and in vitro experiments. In PDX models, metastatic lesions exhibited decreased SEC23A expression following 5-FU treatment in comparison to primary tumors. Overexpression of SEC23A in 5-FU-resistant cell lines restored sensitivity to the drug and increased apoptosis. Bioinformatic and experimental analyses revealed a robust correlation between SEC23A and ER stress-related apoptotic pathways. Elevated expression of SEC23A was observed to facilitate the accumulation of misfolded proteins in response to 5-FU treatment, which in turn resulted in increased ER stress and apoptosis.
    CONCLUSIONS: SEC23A plays a crucial role in modulating the sensitivity of CRC cells to 5-FU by regulating ER stress-induced apoptosis. Its downregulation contributes to chemoresistance, indicating that SEC23A may serve as a prognostic marker and therapeutic target in CRC. Strategies aimed at upregulating SEC23A or enhancing ER stress may provide new avenues for overcoming chemoresistance and improving treatment outcomes for CRC patients.
    Keywords:  5-Fluorouracil; Apoptosis; CRC; Drug Resistance; Endoplasmic reticulum stress; Misfolded protein; SEC23A
    DOI:  https://doi.org/10.1007/s10495-025-02084-2
  8. J Biol Chem. 2025 Feb 03. pii: S0021-9258(25)00104-8. [Epub ahead of print] 108257
      Insulin, a critical metabolic hormone to maintain blood glucose homeostasis, is synthesized and folded in the endoplasmic reticulum (ER) of pancreatic β-cells as the insulin precursor proinsulin. Proinsulin misfolding and aggregation detected in diabetic β-cells induces ER stress and obstructs normal trafficking, processing, and secretion of insulin, which eventually can result in pancreatic β-cell dedifferentiation and death. We have developed quantitative methods to measure misfolded and aggregated proinsulin in β-cells by utilizing proinsulin oligomer specific ELISA and Proximity Ligation Assay (PLA) assays. Under conditions of induced ER stress, both assays detected significant accumulation of aggregated proinsulin in β-cells. Proinsulin aggregation was also observed in isolated pancreatic islets cultured at high glucose levels. Moreover, high glucose in β-cells downregulated expression of genes mediating clearance of misfolded proteins from the secretory pathway through ER autophagy and ER-associated degradation (ERAD). Inhibition of autophagy in β-cells induced strong induction of misfolded proinsulin accumulation, whereas ERAD inhibition was not effective in generating proinsulin aggregates. Finally, we observed subcellular colocalization of aggregated proinsulin with protein markers of autophagosomes. Our results indicate that autophagy controls degradation of aggregated misfolded proinsulin under conditions of hyperglycemia and diabetes.
    Keywords:  ER-associated degradation; autophagy; pancreatic islets; proinsulin; protein aggregation
    DOI:  https://doi.org/10.1016/j.jbc.2025.108257
  9. Dev Cell. 2025 Feb 04. pii: S1534-5807(25)00031-0. [Epub ahead of print]
      Cellular stresses, particularly endoplasmic reticulum (ER) stress induced by ER-to-Golgi transport blockade, trigger Golgi-independent secretion of cytosolic and transmembrane proteins. However, the molecular mechanisms underlying this unconventional protein secretion (UPS) remain largely elusive. Here, we report that an ER tubulovesicular structure (ER tubular body [ER-TB]), shaped by the tubular ER-phagy receptors ATL3 and RTN3L, plays an important role in stress-induced UPS of transmembrane proteins such as cystic fibrosis transmembrane conductance regulator (CFTR) and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) spike protein. Correlative light-electron microscopy analyses demonstrate the formation of ER-TB under UPS-inducing conditions in HEK293 and HeLa cells. Individual gene knockdowns of ATL3 and RTN3 inhibit ER-TB formation and the UPS of trafficking-deficient ΔF508-CFTR. Combined supplementation of ATL3 and RTN3L induces ER-TB formation and UPS. ATL3 also participates in the SARS-CoV-2-associated convoluted membrane formation and Golgi-independent trafficking of SARS-CoV-2 spike protein. These findings suggest that ER-TB serves a common function in mediating stress-induced UPS, which participates in various physiological and pathophysiological processes.
    Keywords:  ATL3; ER stress; ER tubular body; RTN3; unconventional protein secretion
    DOI:  https://doi.org/10.1016/j.devcel.2025.01.011