Lamin A/C loss promotes R-loop-mediated genomic instability and poor survival in small-cell lung cancer

Proc Natl Acad Sci U S A. 2025 Oct 28;122(43):e2503387122. doi: 10.1073/pnas.2503387122. Epub 2025 Oct 23.

Abstract

Lamin A/C (LMNA), a key component of the nuclear envelope, is essential for maintaining nuclear integrity and genome organization [W. Xie et al., Curr. Biol. 26, 2651-2658 (2016)]. While LMNA dysregulation has been implicated in genomic instability across cancer and aging, the underlying mechanisms remain poorly understood [S. Graziano et al., Nucleus 9, 258-275 (2018)]. Here, we define a mechanistic role for LMNA in preserving genome stability in small-cell lung cancer (SCLC), a malignancy marked by extreme genomic instability [N. Takahashi et al., Cancer Res. Commun. 2, 503-517 (2022)]. LMNA depletion promotes R-loop accumulation, transcription-replication conflicts, replication stress, DNA breaks, and micronuclei formation. Mechanistically, LMNA deficiency disrupts nuclear pore complex organization, specifically reducing phenylalanine-glycine (FG)-nucleoporin incorporation, resulting in impaired RNA export and nuclear retention of RNA. LMNA expression is repressed by EZH2 and reexpressed during SCLC differentiation from neuroendocrine (NE) to non-NE states, and low LMNA levels correlate with poor clinical outcomes. These findings establish LMNA as a key regulator of nuclear transport and genome integrity, linking nuclear architecture to SCLC progression and therapeutic vulnerability.

Keywords: R-loops; aging; cancer; replication stress; small-cell lung cancer (SCLC).

MeSH terms

  • Cell Line, Tumor
  • DNA Replication
  • Genomic Instability*
  • Humans
  • Lamin Type A* / genetics
  • Lamin Type A* / metabolism
  • Lung Neoplasms* / genetics
  • Lung Neoplasms* / metabolism
  • Lung Neoplasms* / mortality
  • Lung Neoplasms* / pathology
  • Small Cell Lung Carcinoma* / genetics
  • Small Cell Lung Carcinoma* / metabolism
  • Small Cell Lung Carcinoma* / mortality
  • Small Cell Lung Carcinoma* / pathology

Substances

  • Lamin Type A
  • LMNA protein, human