Bone Marrow Mesenchymal Stem Cell Exosome Attenuates Inflammasome-Related Pyroptosis via Delivering circ_003564 to Improve the Recovery of Spinal Cord Injury

Mol Neurobiol. 2022 Nov;59(11):6771-6789. doi: 10.1007/s12035-022-03006-y. Epub 2022 Aug 30.

Abstract

Bone marrow mesenchymal stem cell (BMSC) is previously reported to present a certain effect on treating spinal cord injury (SCI), while the underlying mechanism is largely uncovered. Therefore, the current study aimed to investigate the involvement of exosome-delivered circRNA profile in the BMSC's effect on pyroptosis for SCI treatment. H2O2 treated rat primary neurons were cultured with normal medium, BMSC, BMSC plus GW4869, and BMSC-derived exosome, respectively, then inflammasome-related pyroptosis markers, and circRNA profiles were detected. Subsequently, circ_003564-knockdown BMSC exosome was transfected into H2O2 treated rat primary neurons and NGF-stimulated PC-12 cells. Furthermore, in vivo validation was conducted. BMSC and BMSC-derived exosome both decreased inflammasome-related pyroptosis markers including cleaved caspase-1, GSDMD, NLRP3, IL-1β, and IL-18 in H2O2-treated neurons, while exosome-free BMSC (BMSC plus GW4869) did not obviously reduce these factors. Microarray assay revealed that BMSC (vs. exosome-free BMSC) and BMSC-derived exosome (vs. normal medium) greatly regulated circRNA profiles, which were enriched in neuroinflammation pathways (such as neurotrophin, apoptosis, and TNF). Among three functional candidate circRNAs (circ_015525, circ_008876, and circ_003564), circ_003564 was most effective to regulate inflammasome-related pyroptosis. Interestingly, circ_003564-knockdown BMSC exosome showed higher expression of inflammasome-related pyroptosis markers compared to negative-control-knockdown BMSC exosome in H2O2 treated primary neurons/NGF-stimulated PC-12 cells. In vivo, BMSC exosome improved the function recovery and decreased tissue injury and inflammasome-related pyroptosis in SCI rats, whose effect was attenuated by circ_003564 knockdown transfection. BMSC exosome attenuates inflammasome-related pyroptosis via delivering circ_003564, contributing to its treatment efficacy for SCI.

Keywords: Bone marrow mesenchymal stem cell; Circular RNA; Exosome; Pyroptosis; Spinal cord injury.

MeSH terms

  • Aniline Compounds
  • Animals
  • Benzylidene Compounds
  • Caspase 1 / metabolism
  • Hydrogen Peroxide / metabolism
  • Inflammasomes / metabolism
  • Interleukin-18 / metabolism
  • Mesenchymal Stem Cell Transplantation*
  • Mesenchymal Stem Cells* / metabolism
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism
  • Nerve Growth Factor / metabolism
  • Pyroptosis
  • RNA, Circular / genetics
  • Rats
  • Spinal Cord / metabolism
  • Spinal Cord Injuries*

Substances

  • Aniline Compounds
  • Benzylidene Compounds
  • GW 4869
  • Inflammasomes
  • Interleukin-18
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • RNA, Circular
  • Nerve Growth Factor
  • Hydrogen Peroxide
  • Caspase 1