Defensin expression by the cornea: multiple signalling pathways mediate IL-1beta stimulation of hBD-2 expression by human corneal epithelial cells

Invest Ophthalmol Vis Sci. 2003 May;44(5):1859-65. doi: 10.1167/iovs.02-0787.

Abstract

Purpose: To investigate the expression of human beta-defensins (hBDs) by human corneal epithelium and determine the effects of proinflammatory cytokines on expression of human beta-defensin (hBD)-2 by human corneal epithelial cells (HCECs) in culture.

Methods: RNA was extracted from corneal epithelial cells scraped from cadaveric corneas and from cultured HCECs, and RT-PCR was performed to detect hBD-1, -2, and -3 mRNA. To study the effects of proinflammatory cytokines on expression of defensin, HCECs were cultured and then exposed to interleukin (IL)-1beta or tumor necrosis factor (TNF)-alpha for up to 36 hours, with a range of concentrations (0.01-100 ng/mL). In some experiments, cells were pretreated with various cell signaling pathway inhibitors before the addition of IL-1beta. At the end of the incubations, the cells were harvested for RT-PCR and the culture media collected for the detection by immunoblot analysis of secreted defensin peptide.

Results: All epithelial tissue collected from cadaveric corneas expressed mRNA for hBD-1. hBD-2 was detectable in two of eight donors corneas, whereas hBD-3 was detected in five. All primary cultures of HCECs expressed hBD-1 and -3. A faint band for hBD-2 was detectable in three of eight cultures. Cultures of simian virus (SV)40-transformed HCECs always expressed hBD-1 and -3, but did not express hBD-2 under control conditions. IL-1beta and TNFalpha each stimulated the expression of hBD-2 in HCECs and were more effective in combination than alone. The effects of IL-1beta were concentration- (maximal at 10 ng/mL) and time-dependent (maximal at 12 hours and 24 hours for hBD-2 mRNA expression and protein secretion, respectively). The upregulation of hBD-2 mRNA persisted for at least 24 hours after removal of IL-1beta. The NFkappaB inhibitors pyrrolidinedithiocarbamate (PDTC; 100 microM), caffeic acid phenethyl ester (CAPE; 90 microM), and MG-132 (25 microM), blocked IL-1beta-stimulated expression of hBD-2. The p38 mitogen-activated protein (MAP) kinase inhibitor SB203580 (5 microM) and the c-Jun NH2-terminal kinase (JNK) inhibitor SP600125 (25 microM) partially blocked (by 47% and 59%, respectively) the effect of IL-1beta. However, PD98059, an ERK inhibitor, had no effect. Genistein (50 microM) and dexamethasone (1 microM) also partially blocked (by 26% and 28%, respectively) the effect of IL-1beta.

Conclusions: Human corneal epithelium expresses hBD-1 and -3. hBD-2 is not typically present, but its expression can be stimulated by proinflammatory cytokines such as IL-1beta, acting through mitogen-activated protein (MAP) kinase and nuclear factor (NF)-kappaB pathways. Because IL-1 is known to be increased at the ocular surface after injury, the current observations provide a mechanism to explain the previous finding that hBD-2 is upregulated in regenerating corneal epithelium. Cytokine stimulation of hBD-2 expression most likely provides additional protection against infection and raises the possibility that this defensin in particular may be involved in the wound-healing response, per se.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Aged
  • Anti-Infective Agents / metabolism*
  • Cell Line, Transformed
  • Cells, Cultured
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Epithelium, Corneal / drug effects*
  • Epithelium, Corneal / metabolism
  • Gene Expression
  • Humans
  • Interleukin-1 / pharmacology*
  • Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • Mitogen-Activated Protein Kinases / physiology
  • NF-kappa B / antagonists & inhibitors
  • NF-kappa B / physiology
  • RNA / isolation & purification
  • RNA, Messenger / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / physiology*
  • Tumor Necrosis Factor-alpha / pharmacology
  • Up-Regulation
  • beta-Defensins / genetics*
  • beta-Defensins / metabolism

Substances

  • Anti-Infective Agents
  • DEFB1 protein, human
  • DEFB103A protein, human
  • DEFB4A protein, human
  • Interleukin-1
  • NF-kappa B
  • RNA, Messenger
  • Tumor Necrosis Factor-alpha
  • beta-Defensins
  • RNA
  • Mitogen-Activated Protein Kinases