bims-unfpre Biomed News
on Unfolded protein response
Issue of 2023‒12‒31
six papers selected by
Susan Logue, University of Manitoba



  1. Neuro Oncol. 2023 Dec 28. pii: noad256. [Epub ahead of print]
      BACKGROUND: Intrinsic or environmental stresses trigger the accumulation of improperly folded proteins in the endoplasmic reticulum (ER), leading to ER stress. To cope with this, cells have evolved an adaptive mechanism named the unfolded protein response (UPR) which is hijacked by tumor cells to develop malignant features. Glioblastoma (GB), the most aggressive and lethal primary brain tumor, relies on UPR to sustain growth. We recently showed that IRE1 alpha (referred to IRE1 hereafter), one of the UPR transducers, promotes GB invasion, angiogenesis and infiltration by macrophage. Hence, high tumor IRE1 activity in tumor cells predicts worse outcome. Herein, we characterized the IRE1-dependent signaling that shapes the immune microenvironment towards monocytes/macrophages and neutrophils.METHODS: We used human and mouse cellular models in which IRE1 was genetically or pharmacologically invalidated and which were tested in vivo. Publicly available datasets from GB patients were also analyzed to confirm our findings.
    RESULTS: We showed that IRE1 signaling, through both the transcription factor XBP1s and the regulated IRE1-dependent decay (RIDD) controls the expression of the ubiquitin-conjugating E2 enzyme UBE2D3. In turn, UBE2D3 activates the NFκB pathway, ensuing chemokine production and myeloid infiltration in tumors.
    CONCLUSION: Our work identifies a novel IRE1/UBE2D3 pro-inflammatory axis that plays an instrumental role in GB immune regulation.
    Keywords:  ER stress; IRE1; chemokines; glioblastoma; inflammation
    DOI:  https://doi.org/10.1093/neuonc/noad256
  2. J Mol Biol. 2023 Dec 22. pii: S0022-2836(23)00535-1. [Epub ahead of print] 168418
      It has been estimated that up to one-third of the proteins encoded by the human genome enter the endoplasmic reticulum (ER) as extended polypeptide chains where they undergo covalent modifications, fold into their native structures, and assemble into oligomeric protein complexes. The fidelity of these processes is critical to support organellar, cellular, and organismal health, and is perhaps best underscored by the growing number of disease-causing mutations that reduce the fidelity of protein biogenesis in the ER. To meet demands encountered by the diverse protein clientele that mature in the ER, this organelle is populated with a cadre of molecular chaperones that prevent protein aggregation, facilitate protein disulfide isomerization, and lower the activation energy barrier of cis-trans prolyl isomerization. Components of the lectin (glycan-binding) chaperone system also reside within the ER and play numerous roles during protein biogenesis. In addition, the ER houses multiple homologs of select chaperones that can recognize and act upon diverse peptide signatures. Moreover, redundancy helps ensure that folding-compromised substrates are unable to overwhelm essential ER-resident chaperones and enzymes. In contrast, the ER in higher eukaryotic cells possesses a single member of the Hsp70, Hsp90, and Hsp110 chaperone families, even though multiple homologs of these molecules reside in the cytoplasm. In this review, we discuss specific functions of the many factors that maintain ER quality control, highlight some of their interactions, and describe the vulnerabilities that arise from the absence of multiple members of some chaperone families.
    Keywords:  Endoplasmic Reticulum Associated Degradation (ERAD); Unfolded Protein Response (UPR); chaperones; co-chaperones; protein folding; proteostasis
    DOI:  https://doi.org/10.1016/j.jmb.2023.168418
  3. Dev Biol. 2023 Dec 23. pii: S0012-1606(23)00209-9. [Epub ahead of print]507 11-19
      Notch signaling controls numerous key cellular processes including cell fate determination and cell proliferation. Its malfunction has been linked to many developmental abnormalities and human disorders. Overactivation of Notch signaling is shown to be oncogenic. Retention of excess Notch protein in the endoplasmic reticulum (ER) can lead to altered Notch signaling and cell fate, but the mechanism is not well understood. In this study, we show that V5-tagged or untagged exogenous Notch is retained in the ER when overexpressed in fly tissues. Furthermore, we show that Notch retention in the ER leads to robust ER enlargement and elicits a rough eye phenotype. Gain-of-function of unfolded protein response (UPR) factors IRE1 or spliced Xbp1 (Xbp1-s) alleviates Notch accumulation in the ER, restores ER morphology and ameliorates the rough eye phenotype. Our results uncover a pivotal role of the IRE1/Xbp1 axis in regulating the detrimental effect of ER-localized excess Notch protein during development and tissue homeostasis.
    Keywords:  Drosophila melanogaster; Endoplasmic reticulum (ER); IRE1; Notch; Unfolded protein response (UPR)
    DOI:  https://doi.org/10.1016/j.ydbio.2023.12.007
  4. Autophagy. 2023 Dec 28.
      The endoplasmic reticulum (ER) extends to the outer (ONM) and the inner (INM) nuclear membrane forming the nuclear envelope (NE) that delimits the nucleoplasm containing the cell genome. Unfolded protein responses (UPRs) and reticulophagy responses increase or reduce ER size and activities, respectively. If dynamic changes of the ER are transmitted to the contiguous NE was not known. In our recent publication, we report on the transmission of stress-induced ER expansion to the NE, which requires disassembly of the Linker of Nucleoskeleton and Cytoskeleton (LINC) complexes deputed to ensure a physical connection between the cytoplasmic cytoskeleton and the nuclear lamina and to maintain the width between INM and ONM within 50 nm. LINC complexes disassembly relies on reduction of the disulfide bond that covalently links SUN proteins in the INM and KASH proteins (SYNE/NESPRIN proteins in mammals) in the ONM by the ONM-resident reductase TMX4. Upon stress resolution, the physiological shape of the NE is re-established by SEC62-driven ONM-phagy, where ONM-derived vesicles are directly captured by RAB7- and LAMP1-positive endolysosomes in processes that proceed via asymmetric microautophagy of the NE.
    Keywords:  ER-phagy; ONM-phagy
    DOI:  https://doi.org/10.1080/15548627.2023.2299123
  5. Genes Immun. 2023 Dec 25.
      The utilization of host-cell machinery during SARS-CoV-2 infection can overwhelm the protein-folding capacity of the endoplasmic reticulum and activate the unfolded protein response (UPR). The IRE1α-XBP1 arm of the UPR could also be activated by viral RNA via Toll-like receptors. Based on these premises, a study to gain insight into the pathogenesis of COVID-19 disease was conducted using nasopharyngeal exudates and bronchioloalveolar aspirates. The presence of the mRNA of spliced XBP1 and a high expression of cytokine mRNAs were observed during active infection. TLR8 mRNA showed an overwhelming expression in comparison with TLR7 mRNA in bronchioloalveolar aspirates of COVID-19 patients, thus suggesting the presence of monocytes and monocyte-derived dendritic cells (MDDCs). In vitro experiments in MDDCs activated with ssRNA40, a synthetic mimic of SARS-CoV-2 RNA, showed induction of XBP1 splicing and the expression of proinflammatory cytokines. These responses were blunted by the IRE1α inhibitor MKC8866, the TLR8 antagonist CU-CPT9a, and knockdown of TLR8 receptor. In contrast, the IRE1α-XBP1 activator IXA4 enhanced these responses. Based on these findings, the TLR8/IRE1α system seems to play a significant role in the induction of the proinflammatory cytokines associated with severe COVID-19 disease and might be a druggable target to control cytokine storm.
    DOI:  https://doi.org/10.1038/s41435-023-00243-6
  6. Mol Metab. 2023 Dec 21. pii: S2212-8778(23)00192-8. [Epub ahead of print] 101858
      OBJECTIVE: Non-alcoholic fatty liver disease (NAFLD) affects 1 in 3 adults and contributes to advanced liver injury and cardiometabolic disease. While recent evidence points to involvement of the brain in NAFLD, the downstream neural circuits and neuronal molecular mechanisms involved in this response, remain unclear. Here, we investigated the role of a unique forebrain-hypothalamic circuit in NAFLD.METHODS: Chemogenetic activation and inhibition of circumventricular subfornical organ (SFO) neurons that project to the paraventricular nucleus of the hypothalamus (PVN; SFO→PVN) in mice were used to study the role of SFO→PVN signaling in NAFLD. Novel scanning electron microscopy techniques, histological approaches, molecular biology techniques, and viral methodologies were further used to delineate the role of endoplasmic reticulum (ER) stress within this circuit in driving NAFLD.
    RESULTS: In lean animals, acute chemogenetic activation of SFO→PVN neurons was sufficient to cause hepatic steatosis in a liver sympathetic nerve dependent manner. Conversely, inhibition of this forebrain-hypothalamic circuit rescued obesity-associated NAFLD. Furthermore, dietary NAFLD is associated with marked ER ultrastructural alterations and ER stress in the PVN, which was blunted following reductions in excitatory signaling from the SFO. Finally, selective inhibition of PVN ER stress reduced hepatic steatosis during obesity.
    CONCLUSIONS: Collectively, these findings characterize a previously unrecognized forebrain-hypothalamic-ER stress circuit that is involved in hepatic steatosis, which may point to future therapeutic strategies for NAFLD.
    Keywords:  Non-alcoholic fatty liver disease; endoplasmic reticulum; paraventricular nucleus of the hypothalamus; subfornical organ; sympathetic nervous system; unfolded protein response
    DOI:  https://doi.org/10.1016/j.molmet.2023.101858