H3K18 lactylation-hexokinase 2 positive feedback loop promotes osteogenesis of ASPCs in facial infiltrating lipomatosis

  • Stem Cell Res Ther. 2025 Oct 1;16(1):538. doi: 10.1186/s13287-025-04651-5.
Hongrui Chen  #  1 Chen Hua  #  1 Shih-Jen Chang  1 Yajing Qiu  1 Xiaoxi Lin  2 Bin Sun  3
Affiliations
  • 1. Department of Plastic & Reconstructive Surgery , Shanghai Ninth People's Hospital Shanghai Jiao Tong University School of Medicine , Shanghai, 200011, P.R. China.
  • 2. Department of Plastic & Reconstructive Surgery , Shanghai Ninth People's Hospital Shanghai Jiao Tong University School of Medicine , Shanghai, 200011, P.R. China. [email protected].
  • 3. Department of Plastic & Reconstructive Surgery , Shanghai Ninth People's Hospital Shanghai Jiao Tong University School of Medicine , Shanghai, 200011, P.R. China. [email protected].
  • # Contributed equally.
Abstract

Background: Facial infiltrating lipomatosis (FIL) is a rare congenital disorder characterized by adipose hyperplasia and osseous overgrowth, driven by somatic PIK3CA mutations. While PIK3CA-induced metabolic reprogramming elevates lactate levels, the role of histone lactylation in FIL pathogenesis remains unclear.

Methods: Adipose stem and progenitor cells (ASPCs) from FIL adipose tissue were isolated. Glycolysis inhibitors (2-DG, oxamate), lactate supplementation, and siRNA-mediated knockdown were used to modulate lactylation. CUT&Tag Sequencing, Western blot, qPCR, ChIP-qPCR and functional assays (osteogenic/adipogenic differentiation) were performed to elucidate the potential mechanism.

Results: FIL-ASPCs exhibited hyperlactylation, particularly at H3K18. H3K18la promoted osteogenesis by activating osteogenic genes, while adipogenesis remained unaffected. Inhibition of lactylation via glycolysis inhibitors or LDHA/LDHB knockdown suppressed osteogenic differentiation, whereas lactate supplementation reversed these effects. TGF-β1 stimulation could increase lactylation levels and promote osteogenic differentiation. Moreover, H3K18la upregulated Hexokinase 2 (HK2), enhancing glycolysis and lactate production, thereby forming a lactate-H3K18la-HK2 positive feedback loop.

Conclusions: This study identified H3K18 lactylation as a key epigenetic driver of FIL-associated osseous hyperplasia via a lactate-H3K18la-HK2 feedback loop. Targeting this axis may offer therapeutic potential for FIL and related metabolic bone disorders.

Keywords
Adipose stem and progenitor cells; Facial infiltrating lipomatosis; H3K18 lactylation; Hexokinase 2; Osteogenesis.
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