The Nf1-Q181X point mutation induces M2 macrophage polarization via the AKT/STAT pathway to promote smooth muscle cell proliferation and migration

Mol Biol Rep. 2024 Aug 31;51(1):946. doi: 10.1007/s11033-024-09887-7.

Abstract

Background: Increased case reports have shown that patients with NF1 have an increased risk of extensive vascular vasculopathy. Previous studies demonstrated the presence of macrophages and smooth muscle cells in the neoplastic intima of carotid arteries after injury in Nf1+/- mice. However, whether NF1 gene mutations affect macrophage polarization and macrophage-smooth muscle cell interactions remains to be elucidated.

Methods: Scratch assay and transwell assay were utilized to detect cell migration ability. The dye 2',7'dichlorofluorescin diacetate and neutral red stain were used to assess intracellular ROS production and cell phagocytosis function, respectively. Proteins and mRNA expression were determined by western blot, RT-qPCR, and immunofluorescence. Finally, the macrophage (MAC) and vascular smooth muscle cell (VSMC) co-culture system was used to detect cellular crosstalk.

Results: Cell function assays confirmed that the Nf1-Q181X point mutation attenuated the phagocytosis of bone marrow-derived macrophages (BMDMs) and promoted the migration and ROS production of BMDMs. Moreover, we found that the Nf1-Q181X point mutation inhibited M1 but promoted M2 macrophage polarization by down-regulating p38, ERK, and JNK and up-regulating the Akt/STAT3 signaling pathway, respectively. Furthermore, in the MAC-VSMC co-culture system, we demonstrated that Nf1-Q181X point mutation-activated M2 BMDMs promoted proliferation and migration of VSMCs and induced the transformation of VSMCs from contractile phenotype to synthetic phenotype.

Conclusion: The findings suggest that the Nf1-Q181X point mutation can mediate macrophage polarization and promote smooth muscle cell proliferation and migration, providing clinical clues for the treatment of NF1-complicated vasculopathy.

Keywords: M2 macrophage polarization; NF1; Phenotype switching; Vascular smooth muscle cell.

MeSH terms

  • Animals
  • Cell Movement* / genetics
  • Cell Proliferation* / genetics
  • Coculture Techniques
  • Macrophages* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Muscle, Smooth, Vascular / cytology
  • Muscle, Smooth, Vascular / metabolism
  • Myocytes, Smooth Muscle* / metabolism
  • Neurofibromin 1* / genetics
  • Neurofibromin 1* / metabolism
  • Phagocytosis / genetics
  • Point Mutation*
  • Proto-Oncogene Proteins c-akt* / metabolism
  • Reactive Oxygen Species / metabolism
  • STAT3 Transcription Factor / genetics
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction*

Substances

  • Proto-Oncogene Proteins c-akt
  • Neurofibromin 1
  • STAT3 Transcription Factor
  • Reactive Oxygen Species