SGK1 inhibits cellular apoptosis and promotes proliferation via the MEK/ERK/p53 pathway in colitis

World J Gastroenterol. 2015 May 28;21(20):6180-93. doi: 10.3748/wjg.v21.i20.6180.

Abstract

Aim: To investigate the role of serum-and-glucocorticoid-inducible-kinase-1 (SGK1) in colitis and its potential pathological mechanisms.

Methods: SGK1 expression in mucosal biopsies from patients with active Crohn's disease (CD) and normal controls was detected by immunohistochemistry. We established an acute colitis model in mice induced by 2,4,6-trinitrobenzene sulfonicacid, and demonstrated the presence of colitis using the disease activity index, the histologic activity index and hematoxylin and eosin staining. The cellular events and potential mechanisms were implemented with small interference RNA and an inhibitor of signaling molecule (i.e., U0126) in intestinal epithelial cells (IECs). The interaction between SGK1 and the signaling molecule was assessed by co-immunoprecipitation.

Results: SGK1 expression was significantly increased in the inflamed epithelia of patients with active CD and TNBS-induced colitis model (0.58 ± 0.055 vs 0.85 ± 0.06, P < 0.01). At the cellular level, silencing of SGK1 by small interference RNA (siSGK1) significantly inhibited the phosphorylation of mitogen-activated protein kinase kinase 1 (MEK1) and the downstream molecule extracellular signal regulated protein kinase (ERK) 1/2, which induced the upregulation of p53 and Bcl-2-associated X protein, mediating the subsequent cellular apoptosis and proliferation in IECs. Cells treated with MEK1 inhibitor (i.e., U0126) before siSGK1 transfection showed a reversal of the siSGK1-induced cellular apoptosis.

Conclusion: Our data suggested that SGK1 may protect IECs in colitis from tumor necrosis factor-α-induced apoptosis partly by triggering MEK/ERK activation.

Keywords: Apoptosis; Colitis; MEK/ERK; Serum-and-glucocorticoid-inducible-kinase-1; p53.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis* / drug effects
  • Cell Proliferation* / drug effects
  • Colitis / chemically induced
  • Colitis / enzymology*
  • Colitis / pathology
  • Colon / drug effects
  • Colon / enzymology*
  • Colon / pathology
  • Crohn Disease / enzymology
  • Crohn Disease / pathology
  • Disease Models, Animal
  • Dose-Response Relationship, Drug
  • Epithelial Cells / drug effects
  • Epithelial Cells / enzymology*
  • Epithelial Cells / pathology
  • Extracellular Signal-Regulated MAP Kinases / antagonists & inhibitors
  • Extracellular Signal-Regulated MAP Kinases / metabolism*
  • Female
  • HCT116 Cells
  • Humans
  • Immediate-Early Proteins / genetics
  • Immediate-Early Proteins / metabolism*
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / enzymology*
  • Intestinal Mucosa / pathology
  • MAP Kinase Kinase 1 / antagonists & inhibitors
  • MAP Kinase Kinase 1 / metabolism*
  • Mice, Inbred BALB C
  • Protein Kinase Inhibitors / pharmacology
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*
  • RNA Interference
  • Rabbits
  • Signal Transduction
  • Time Factors
  • Transfection
  • Trinitrobenzenesulfonic Acid
  • Tumor Necrosis Factor-alpha / pharmacology
  • Tumor Suppressor Protein p53 / metabolism*

Substances

  • Immediate-Early Proteins
  • Protein Kinase Inhibitors
  • TP53 protein, human
  • Tumor Necrosis Factor-alpha
  • Tumor Suppressor Protein p53
  • Trinitrobenzenesulfonic Acid
  • Protein Serine-Threonine Kinases
  • serum-glucocorticoid regulated kinase
  • Extracellular Signal-Regulated MAP Kinases
  • MAP Kinase Kinase 1
  • MAP2K1 protein, human