Gene-Silencing Therapeutic Approaches Targeting PI3K/Akt/mTOR Signaling in Degenerative Intervertebral Disk Cells: An In Vitro Comparative Study Between RNA Interference and CRISPR-Cas9

Cells. 2024 Dec 9;13(23):2030. doi: 10.3390/cells13232030.

Abstract

The mammalian target of rapamycin (mTOR), a serine/threonine kinase, promotes cell growth and inhibits autophagy. The following two complexes contain mTOR: mTORC1 with the regulatory associated protein of mTOR (RAPTOR) and mTORC2 with the rapamycin-insensitive companion of mTOR (RICTOR). The phosphatidylinositol 3-kinase (PI3K)/Akt/mTOR signaling pathway is important in the intervertebral disk, which is the largest avascular, hypoxic, low-nutrient organ in the body. To examine gene-silencing therapeutic approaches targeting PI3K/Akt/mTOR signaling in degenerative disk cells, an in vitro comparative study was designed between small interfering RNA (siRNA)-mediated RNA interference (RNAi) and clustered regularly interspaced short palindromic repeat (CRISPR)-CRISPR-associated protein 9 (Cas9) gene editing. Surgically obtained human disk nucleus pulposus cells were transfected with a siRNA or CRISPR-Cas9 plasmid targeting mTOR, RAPTOR, or RICTOR. Both of the approaches specifically suppressed target protein expression; however, the 24-h transfection efficiency differed by 53.8-60.3% for RNAi and 88.1-89.3% for CRISPR-Cas9 (p < 0.0001). Targeting mTOR, RAPTOR, and RICTOR all induced autophagy and inhibited apoptosis, senescence, pyroptosis, and matrix catabolism, with the most prominent effects observed with RAPTOR CRISPR-Cas9. In the time-course analysis, the 168-h suppression ratio of RAPTOR protein expression was 83.2% by CRISPR-Cas9 but only 8.8% by RNAi. While RNAi facilitates transient gene knockdown, CRISPR-Cas9 provides extensive gene knockout. Our findings suggest that RAPTOR/mTORC1 is a potential therapeutic target for degenerative disk disease.

Keywords: RNA interference (RNAi); autophagy; clustered regularly interspaced short palindromic repeat (CRISPR)–CRISPR-associated protein 9 (Cas9); disk degeneration; gene-silencing therapy; intervertebral disk; nucleus pulposus (NP) cells; phosphatidylinositol 3-kinase (PI3K)/Akt/mammalian target of rapamycin (mTOR) signaling; small interfering RNA (siRNA); spine.

Publication types

  • Comparative Study

MeSH terms

  • Autophagy / genetics
  • CRISPR-Cas Systems* / genetics
  • Female
  • Gene Silencing
  • Humans
  • Intervertebral Disc / metabolism
  • Intervertebral Disc / pathology
  • Intervertebral Disc Degeneration* / genetics
  • Intervertebral Disc Degeneration* / metabolism
  • Intervertebral Disc Degeneration* / pathology
  • Intervertebral Disc Degeneration* / therapy
  • Male
  • Middle Aged
  • Nucleus Pulposus / metabolism
  • Nucleus Pulposus / pathology
  • Phosphatidylinositol 3-Kinases / metabolism
  • Proto-Oncogene Proteins c-akt* / metabolism
  • RNA Interference*
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Regulatory-Associated Protein of mTOR / genetics
  • Regulatory-Associated Protein of mTOR / metabolism
  • Signal Transduction*
  • TOR Serine-Threonine Kinases* / metabolism

Substances

  • TOR Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • Phosphatidylinositol 3-Kinases
  • Regulatory-Associated Protein of mTOR
  • RNA, Small Interfering
  • MTOR protein, human