Immortalized mesenchymal stromal cells overexpressing alpha-1 antitrypsin protect acinar cells from apoptotic and ferroptotic cell death.

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    • Source:
      Publisher: Wiley-Blackwell Country of Publication: England NLM ID: 101083777 Publication Model: Print Cited Medium: Internet ISSN: 1582-4934 (Electronic) Linking ISSN: 15821838 NLM ISO Abbreviation: J Cell Mol Med Subsets: MEDLINE
    • Publication Information:
      Publication: Oxford, England : Wiley-Blackwell
      Original Publication: Bucharest : "Carol Davila" University Press, 2000-
    • Subject Terms:
    • Abstract:
      Chronic pancreatitis (CP) is a progressive inflammatory disorder that impairs endocrine and exocrine function. Our previous work showed that mesenchymal stem/stromal cells (MSCs) and MSCs overexpressing alpha-1 antitrypsin (AAT-MSCs) could be therapeutic tools for CP. However, primary MSCs are predisposed to undergo senescence during culture expansion, which limits their therapeutic applications. We generated and characterized immortalized human MSCs (iMSCs) and AAT-MSCs (iAAT-MSCs) and tested their protective effect on 2,4,6-Trinitrobenzenesulfonic acid (TNBS)-induced acinar cell death in an in vitro cell culture system. Primary MSCs were immortalized by transduction with simian virus 40 large T antigen (SV40LT), and the resulting iMSC and iAAT-MSC lines were analysed for proliferation, senescence, phenotype and multi-differentiation potential. Subsequently, apoptosis and ferroptosis pathways were investigated by assessing changes before and after TNBS treatment. Coculture of iMSCs and iAAT-MSCs with acinar cell lines inhibited early cell death induced by TNBS, reduced ER stress and reversed TNBS-induced protein reduction at tight junctions. Additionally, iMSCs and iAAT-MSCs exerted such protection by regulating mitochondrial respiration, ATP content and ROS production in TNBS-induced acinar cells. Furthermore, iMSCs and iAAT-MSCs ameliorated TNBS-induced ferroptosis by modulating iron generation and ROS production and regulating the ferritin heavy chain 1 (FTH1)/protein disulfide isomerase (PDI)/glutathione peroxide 4 (GPX4) signalling pathways in acinar cells. These findings identify ferroptosis as an unrecognized mechanism that leads to TNBS-induced cell death and offer mechanistic insights relevant to using stem cell therapy to treat acinar cell death associated with CP.
      (© 2024 The Author(s). Journal of Cellular and Molecular Medicine published by Foundation for Cellular and Molecular Medicine and John Wiley & Sons Ltd.)
    • Comments:
      Update of: Res Sq. 2023 Aug 09:rs.3.rs-2961444. doi: 10.21203/rs.3.rs-2961444/v1. (PMID: 37609340)
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    • Grant Information:
      R01DK125454 United States DK NIDDK NIH HHS; I01 BX004536 United States BX BLRD VA; VA-ORD BLR&D Merit I01BX004536) United States VA VA; R01DK120394 United States DK NIDDK NIH HHS; R01DK118529 United States DK NIDDK NIH HHS; R01DK105183 United States DK NIDDK NIH HHS; UG3DK136705 United States DK NIDDK NIH HHS
    • Contributed Indexing:
      Keywords: acinar cell death; chronic pancreatitis; ferroptosis; immortalized human MSCs
    • Accession Number:
      0 (alpha 1-Antitrypsin)
      8T3HQG2ZC4 (Trinitrobenzenesulfonic Acid)
    • Publication Date:
      Date Created: 20241029 Date Completed: 20241029 Latest Revision: 20241105
    • Publication Date:
      20241105
    • Accession Number:
      PMC11518823
    • Accession Number:
      10.1111/jcmm.70093
    • Accession Number:
      39468387