Targeting hyaluronan synthesis enhances the therapeutic effectiveness of biologics in inflammatory bowel disease

JCI Insight. 2025 Jan 9;10(1):e180425. doi: 10.1172/jci.insight.180425.

Abstract

Although biologics have been revolutionizing the treatment of inflammatory bowel diseases (IBD) over the past decade, a significant number of patients still fail to benefit from these drugs. Overcoming the nonresponse to biologics is one of the top challenges in IBD treatment. In this study, we revealed that hyaluronan (HA), an extracellular matrix (ECM) component in the gut, is associated with nonresponsiveness to infliximab and vedolizumab therapy in patients with IBD. In murine colitis models, inhibition of HA synthase 2-mediated (HAS2-mediated) HA synthesis sensitized the therapeutic response to infliximab. Mechanistically, HA induced the expression of MMP3 in colonic fibroblasts by activating STAT3 signaling, thereby mediating the proteolytic cleavage of multiple IgG1 biologics. Finally, we found that macrophage-derived factors upregulated HAS2 expression in fibroblasts, thereby contributing to infliximab nonresponse. In summary, we identified a pathogenic connection between abnormal ECM remodeling and biologics nonresponse and provided insights for the precise therapy for IBD.

Keywords: Extracellular matrix; Gastroenterology; Immunology; Immunotherapy; Inflammatory bowel disease.

MeSH terms

  • Adult
  • Animals
  • Antibodies, Monoclonal, Humanized* / pharmacology
  • Antibodies, Monoclonal, Humanized* / therapeutic use
  • Biological Products / pharmacology
  • Biological Products / therapeutic use
  • Disease Models, Animal
  • Extracellular Matrix / metabolism
  • Female
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Humans
  • Hyaluronan Synthases* / genetics
  • Hyaluronan Synthases* / metabolism
  • Hyaluronic Acid* / metabolism
  • Inflammatory Bowel Diseases* / drug therapy
  • Inflammatory Bowel Diseases* / metabolism
  • Infliximab* / pharmacology
  • Infliximab* / therapeutic use
  • Male
  • Matrix Metalloproteinase 3 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Middle Aged
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction / drug effects

Substances

  • Hyaluronic Acid
  • Infliximab
  • Antibodies, Monoclonal, Humanized
  • vedolizumab
  • Hyaluronan Synthases
  • STAT3 Transcription Factor
  • Biological Products
  • HAS2 protein, human
  • Matrix Metalloproteinase 3
  • STAT3 protein, human