Senescent human hepatocytes express a unique secretory phenotype and promote macrophage migration

World J Gastroenterol. 2014 Dec 21;20(47):17851-62. doi: 10.3748/wjg.v20.i47.17851.

Abstract

Aim: To develop a model of stress-induced senescence to study the hepatocyte senescence associated secretory phenotype (SASP).

Methods: Hydrogen peroxide treatment was used to induce senescence in the human HepG2 hepatocyte cell line. Senescence was confirmed by cytochemical staining for a panel of markers including Ki67, p21, heterochromatin protein 1β, and senescence-associated-β-galactosidase activity. Senescent hepatocytes were characterised by gene expression arrays and quantitative polymerase chain reaction (qPCR), and conditioned media was used in proteomic analyses, a human chemokine protein array, and cell migration assays to characterise the composition and function of the hepatocyte SASP.

Results: Senescent hepatocytes induced classical markers of senescence (p21, heterochromatin protein 1β, and senescence-associated-β-galactosidase activity); and downregulated the proliferation marker, Ki67. Hepatocyte senescence induced a 4.6-fold increase in total secreted protein (P = 0.06) without major alterations in the protein profile. Senescence-induced genes were identified by microarray (Benjamini Hochberg-corrected P < 0.05); and, consistent with the increase in secreted protein, gene ontology analysis revealed a significant enrichment of secreted proteins among inducible genes. The hepatocyte SASP included characteristic factors such as interleukin (IL)-8 and IL-6, as well as novel components such as SAA4, IL-32 and Fibrinogen, which were validated by qPCR and/or chemokine protein array. Senescent hepatocyte-conditioned medium elicited migration of inflammatory (granulocyte-macrophage colony stimulating factor, GM-CSF-derived), but not non-inflammatory (CSF-1-derived) human macrophages (P = 0.022), which could contribute to a pro-inflammatory microenvironment in vivo, or facilitate the clearance of senescent cells.

Conclusion: Our novel model of hepatocyte senescence provides insights into mechanisms by which senescent hepatocytes may promote chronic liver disease pathogenesis.

Keywords: Cell aging; Chemokines; Hepatocytes; Inflammation; Liver diseases; Macrophages.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Biomarkers / metabolism
  • Cell Cycle Checkpoints
  • Cellular Senescence* / drug effects
  • Chemotaxis*
  • Coculture Techniques
  • Culture Media, Conditioned / metabolism
  • Cytokines / genetics
  • Cytokines / metabolism
  • Dose-Response Relationship, Drug
  • Gene Expression Regulation
  • Hep G2 Cells
  • Hepatocytes / drug effects
  • Hepatocytes / metabolism*
  • Humans
  • Hydrogen Peroxide / pharmacology
  • Inflammation Mediators / metabolism
  • Macrophages / metabolism*
  • Oxidative Stress
  • Paracrine Communication*
  • Phenotype
  • Transcriptome

Substances

  • Biomarkers
  • Culture Media, Conditioned
  • Cytokines
  • Inflammation Mediators
  • Hydrogen Peroxide