Smad4 Deficiency in S100A4+ Macrophages Enhances Colitis-associated Tumorigenesis by Promoting Macrophage Lipid Metabolism Augmented M2 Polarization

Int J Biol Sci. 2024 Nov 11;20(15):6114-6129. doi: 10.7150/ijbs.98529. eCollection 2024.

Abstract

S100A4 is primarily expressed in intestinal macrophages, and promotes colonic inflammation and colitis-associated colon tumorigenesis. Smad4 is also expressed in the colon; however, it inhibits colitis-associated cancer (CAC) development. The specific role of Smad4 in S100A4+ cells in CAC remains unknown. In this study, an azoxymethane (AOM)/dextran sodium sulfate (DSS)-induced CAC model was established in mice with S100A4+ cell-specific Smad4 deletion (S100A4 Smad4-/-). Smad4 deficiency in S100A4+ cells exacerbated DSS-induced colitis and promoted colorectal tumorigenesis. In addition, S100A4+ cell-specific Smad4 ablation promoted the M2 polarization of macrophages in CAC. Mechanistically, Smad4 depletion in macrophages enhanced lipid metabolism by activating the FA binding protein 2 (Fabp2)/STAT6 pathway. Furthermore, Smad4 deficiency in macrophages promoted MC38 tumor growth in myeloid-specific Smad4 deficient (Lyz Smad4-/-) mice, whereas blocking Fabp2 expression reversed the tumor growth. Additionally, high Smad4 expression was associated with prolonged survival in patients with colorectal cancer. Thus, Smad4 in S100A4+ macrophages plays a tumor-inhibiting role in CAC development and supports its use as a prognostic marker in CRC patients.

Keywords: Fabp2; S100A4; STAT6; Smad4; macrophage; metabolism..

MeSH terms

  • Animals
  • Azoxymethane
  • Carcinogenesis / metabolism
  • Colitis / chemically induced
  • Colitis / complications
  • Colitis / metabolism
  • Colitis-Associated Neoplasms / etiology
  • Colitis-Associated Neoplasms / metabolism
  • Colitis-Associated Neoplasms / pathology
  • Dextran Sulfate
  • Humans
  • Lipid Metabolism*
  • Macrophages* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • S100 Calcium-Binding Protein A4* / genetics
  • S100 Calcium-Binding Protein A4* / metabolism
  • Smad4 Protein* / genetics
  • Smad4 Protein* / metabolism

Substances

  • Smad4 Protein
  • S100 Calcium-Binding Protein A4
  • Smad4 protein, mouse
  • Dextran Sulfate
  • S100a4 protein, mouse
  • Azoxymethane