Isovalerylspiramycin I suppresses small cell lung cancer proliferation via ATR/CHK1 mediated DNA damage response and PERK/eIF2α/ATF4/CHOP mediated ER stress

Biochem Pharmacol. 2024 Dec;230(Pt 1):116557. doi: 10.1016/j.bcp.2024.116557. Epub 2024 Sep 29.

Abstract

Small cell lung cancer (SCLC) urgently needs new therapeutic approaches. We found that the antibiotic-derived compound Isovalerylspiramycin I (ISP-I) has potent anti-tumor activity against SCLC cell lines H1048 and DMS53 both in vitro and in vivo. ISP-I induced apoptosis, G2/M phase cell cycle arrest, and mitochondrial respiratory chain dysfunction in both cell lines. Comprehensive RNA sequencing revealed that the anti-SCLC effects of ISP-I were primarily attributed to ATR/CHK1-mediated DNA damage response and PERK/eIF2α/ATF4/CHOP-mediated ER stress. Importantly, the induction of DNA damage, ER stress, and apoptosis by ISP-I was mitigated by the reactive oxygen species (ROS) scavenger N-acetyl-L-cysteine (NAC), underscoring the critical role of ROS in the anti-SCLC mechanism of ISP-I. Moreover, ISP-I treatment induced immunogenic cell death (ICD) in SCLC cells, as evidenced by increased adenosine triphosphate (ATP) secretion, elevated release of high-mobility group box 1 (HMGB1), and enhanced exposure of calreticulin (CRT) on the cell surface. Additionally, network pharmacology analysis, combined with cellular thermal shift assay (CETSA) and cycloheximide (CHX) chase experiments, demonstrated that ISP-I acted as a ligand for apurinic/apyrimidinic endonuclease 1 (APEX1) and promoted its degradation, leading to the accumulation of ROS. In conclusion, our findings elucidate the multifaceted mechanisms underlying the anti-cancer effects of ISP-I, highlighting its potential as a promising therapeutic candidate for SCLC treatment.

Keywords: Apoptosis; DNA damage response; ER stress; Immunogenic cell death; Isovalerylspiramycin I; Small cell lung cancer.

MeSH terms

  • Activating Transcription Factor 4* / genetics
  • Activating Transcription Factor 4* / metabolism
  • Animals
  • Anthracyclines / pharmacology
  • Ataxia Telangiectasia Mutated Proteins* / metabolism
  • Cell Line, Tumor
  • Cell Proliferation* / drug effects
  • Checkpoint Kinase 1* / metabolism
  • DNA Damage* / drug effects
  • Endoplasmic Reticulum Stress* / drug effects
  • Eukaryotic Initiation Factor-2* / metabolism
  • Humans
  • Lung Neoplasms* / drug therapy
  • Lung Neoplasms* / metabolism
  • Lung Neoplasms* / pathology
  • Mice
  • Mice, Nude
  • Small Cell Lung Carcinoma* / drug therapy
  • Small Cell Lung Carcinoma* / metabolism
  • Small Cell Lung Carcinoma* / pathology
  • Transcription Factor CHOP* / genetics
  • Transcription Factor CHOP* / metabolism
  • eIF-2 Kinase* / metabolism

Substances

  • Checkpoint Kinase 1
  • Activating Transcription Factor 4
  • eIF-2 Kinase
  • CHEK1 protein, human
  • Transcription Factor CHOP
  • Eukaryotic Initiation Factor-2
  • ATF4 protein, human
  • DDIT3 protein, human
  • Ataxia Telangiectasia Mutated Proteins
  • ATR protein, human
  • EIF2AK3 protein, human
  • EIF2S1 protein, human
  • Anthracyclines