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PIM1-HDAC2 axis modulates intestinal homeostasis through epigenetic modification.

Jianming Yang1, Yawen Xiao1, Ningning Zhao1

  • 1Key Laboratory of Immune Microenvironment and Disease (Ministry of Education), Tianjin Institute of Immunology, State Key Laboratory of Experimental Hematology, the Province and Ministry Co-sponsored Collaborative Innovation Center for Medical Epigenetics, Department of Immunology, School of Basic Medical Sciences, Tianjin Institute of Urology, the Second Hospital of Tianjin Medical University, Tianjin Key Laboratory of Cellular and Molecular Immunology, Tianjin Medical University, Tianjin 300070, China.

Acta Pharmaceutica Sinica. B
|July 19, 2024
PubMed
Summary

Proviral integration site for Moloney murine leukemia virus-1 (PIM1) kinase is elevated in colitis, reducing goblet cells. This PIM1-HDAC2 axis impairs gut barrier integrity and promotes colitis-associated colorectal cancer.

Keywords:
CACEpigenetic modificationGoblet cellGut microbiotaHDAC2Intestinal homeostasisPIM1Ulcerative colitis

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Area of Science:

  • Gastroenterology
  • Molecular Biology
  • Oncology

Background:

  • The intestinal mucosal barrier is vital for gut homeostasis.
  • Goblet cells are key to maintaining mucosal barrier integrity.
  • The role of PIM1 kinase in colitis-induced intestinal dysfunction was previously unknown.

Purpose of the Study:

  • To investigate the role of PIM1 kinase in intestinal homeostasis during colitis.
  • To elucidate the molecular mechanisms by which PIM1 affects goblet cell differentiation.
  • To explore the PIM1-HDAC2 axis in the pathogenesis of ulcerative colitis and colitis-associated colorectal cancer (CAC).

Main Methods:

  • Analysis of PIM1 expression in colonic tissues from ulcerative colitis patients and murine models.
  • Assessment of goblet cell numbers and gut barrier function in PIM1-manipulated mice.
  • Investigation of PIM1's interaction with histone deacetylase 2 (HDAC2) and its effect on Wnt and Notch signaling pathways.

Main Results:

  • PIM1 expression is significantly elevated in the colonic epithelia of ulcerative colitis patients and murine models.
  • Epithelial PIM1 overexpression leads to a decrease in goblet cells, impairing colitis resistance and promoting CAC in mice.
  • PIM1 phosphorylates and downregulates HDAC2, altering epigenetic profiles of Wnt signaling genes and modulating goblet cell differentiation.

Conclusions:

  • The PIM1-HDAC2 axis plays a critical role in goblet cell differentiation and intestinal homeostasis.
  • PIM1 contributes to the pathogenesis of ulcerative colitis and CAC by impairing goblet cell function.
  • Targeting the PIM1-HDAC2 axis represents a potential therapeutic strategy for ulcerative colitis and CAC.