Detrimental effects of Notch1 signaling activated by cadmium in renal proximal tubular epithelial cells

Cell Death Dis. 2014 Aug 14;5(8):e1378. doi: 10.1038/cddis.2014.339.

Abstract

We examined the roles of Notch1 signaling and its cross-talk with other signaling pathways, including p53 and phosphatidylinositol-3-kinase (PI3K)/Akt, in cadmium-induced cellular damage in HK-2 human renal proximal tubular epithelial cells. Following exposure to cadmium chloride (CdCl2), the level of Notch intracellular domain (NICD), the cleaved form of the Notch1 receptor, was increased and accumulated in the nuclear fraction. Knockdown of Notch1 with siRNA or treatment with the γ-secretase inhibitor, DAPT (N-[N-(3,5-difluorophenacetyl-L-alanyl)]-S-phenylglycine t-butyl ester), prevented CdCl2-induced morphological change of HK-2 cells and reduction of cell viability. Knockdown of Jagged1 or Jagged2, the ligands of the Notch1 receptor, partially suppressed cadmium cytotoxicity. Inhibition of p53 activity with pifithrin-α or inhibition of PI3K with LY294002 suppressed CdCl2-induced cellular damage and elevation of Notch1-NICD. In addition, treatment with the epidermal growth factor receptor (EGFR) inhibitor, AG1478, and the insulin-like growth factor-1 receptor inhibitor, PPP, suppressed both Notch1-NICD accumulation and Akt phosphorylation in HK-2 cells exposed to CdCl2. However, knockdown of Notch1 did not affect CdCl2-induced p53 accumulation and phosphorylation but suppressed phosphorylation of EGFR, Akt, and p70 S6 kinase. Depletion of Notch1 suppressed CdCl2-induced reduction of E-cadherin expression and elevation of Snail expression. Furthermore, treatment with SB216763, an inhibitor of glycogen synthase kinase-3, suppressed the potency of LY294002 treatment to reduce Snail expression in HK-2 cells exposed to CdCl2. Knockdown of Snail with siRNA partially prevented HK-2 cells from CdCl2-induced reduction of E-cadherin expression and cellular damage. These results suggest that cadmium exposure induces the activation of Notch1 signaling in renal proximal tubular cells with cooperative activation by the p53 and PI3K/Akt signaling pathways; the resultant expression of Snail, a repressor of E-cadherin expression, might lead to cellular damage by decreasing cell-cell adhesion.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cadmium Chloride / toxicity*
  • Calcium-Binding Proteins / antagonists & inhibitors
  • Calcium-Binding Proteins / genetics
  • Calcium-Binding Proteins / metabolism
  • Cell Line
  • Chromones / pharmacology
  • Down-Regulation / drug effects
  • Epithelial Cells / cytology
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • ErbB Receptors / antagonists & inhibitors
  • ErbB Receptors / metabolism
  • Humans
  • Indoles / pharmacology
  • Intercellular Signaling Peptides and Proteins / genetics
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Jagged-1 Protein
  • Jagged-2 Protein
  • Kidney Tubules, Proximal / cytology
  • Maleimides / pharmacology
  • Membrane Proteins / antagonists & inhibitors
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Morpholines / pharmacology
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphoinositide-3 Kinase Inhibitors
  • Phosphorylation / drug effects
  • Quinazolines / pharmacology
  • RNA Interference
  • RNA, Small Interfering / metabolism
  • Receptor, Notch1 / antagonists & inhibitors
  • Receptor, Notch1 / genetics
  • Receptor, Notch1 / metabolism*
  • Serrate-Jagged Proteins
  • Signal Transduction / drug effects*
  • Snail Family Transcription Factors
  • Transcription Factors / antagonists & inhibitors
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Tumor Suppressor Protein p53 / metabolism
  • Tyrphostins / pharmacology

Substances

  • Calcium-Binding Proteins
  • Chromones
  • Indoles
  • Intercellular Signaling Peptides and Proteins
  • JAG1 protein, human
  • JAG2 protein, human
  • Jagged-1 Protein
  • Jagged-2 Protein
  • Maleimides
  • Membrane Proteins
  • Morpholines
  • NOTCH1 protein, human
  • Phosphoinositide-3 Kinase Inhibitors
  • Quinazolines
  • RNA, Small Interfering
  • Receptor, Notch1
  • SB 216763
  • Serrate-Jagged Proteins
  • Snail Family Transcription Factors
  • Transcription Factors
  • Tumor Suppressor Protein p53
  • Tyrphostins
  • RTKI cpd
  • 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one
  • EGFR protein, human
  • ErbB Receptors
  • Cadmium Chloride