Increased SPHK2 Transcription of Human Colon Cancer Cells in Serum-Depleted Culture: The Involvement of CREB Transcription Factor

J Cell Biochem. 2015 Oct;116(10):2227-38. doi: 10.1002/jcb.25173.

Abstract

Sphingosine kinases (SPHK) are important to determine cells' fate by producing sphingosine 1-phosphate. Reportedly, exogenous SPHK2 overexpression induces cell cycle arrest or cell death. However, the regulatory mechanism of SPHK2 expression has not been fully elucidated. Here, we analyzed this issue using human colon cancer cell lines under various stress conditions. Serum depletion (FCS(-)) but not hypoxia and glucose depletion increased mRNA, protein and enzyme activity of SPHK2 but not SPHK1. In HCT116 cells mostly used, SPHK2 activity was predominant over SPHK1, and serum depletion increased both nuclear and cytoplasmic SPHK2 activity. Based on previous reports analyzing cellular response after serum depletion, the temporal changes of intracellular signaling molecules and candidate transcription factors for SPHK2 were examined using serum-depleted HCT116 cells, and performed transfection experiments with siRNA or cDNA of candidate transcription factors. Results showed that the rapid and transient JNK activation followed by CREB activation was the major regulator of increased SPHK2 transcription in FCS(-) culture. EMSA and ChIP assay confirmed the direct binding of activated CREB to the CREB binding site of 5' SPHK2 promoter region. Colon cancer cells examined continued to grow in FCS(-) culture, although mildly, while hypoxia and glucose depletion suppressed cell proliferation or induced cell death, suggesting the different role of SPHK2 in different stress conditions. Because of the unique relationship observed after serum depletion, we examined effects of siRNA for SPHK2, and found the role of SPHK2 as a growth or survival factor but not a cell proliferation inhibitor in FCS(-) culture.

Keywords: CREB TRANSCRIPTION FACTOR; HUMAN COLON CANCER CELL LINES; JNK ACTIVATION; SERUM DEPRIVATION; SPHK2; TRANSCRIPTIONAL REGULATION.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Differentiation
  • Cell Proliferation / genetics*
  • Colonic Neoplasms / genetics*
  • Colonic Neoplasms / pathology
  • Culture Media, Serum-Free
  • Cyclic AMP Response Element-Binding Protein / genetics
  • Cyclic AMP Response Element-Binding Protein / metabolism*
  • Gene Expression Regulation, Neoplastic
  • HCT116 Cells
  • Humans
  • Phosphotransferases (Alcohol Group Acceptor) / biosynthesis*
  • Phosphotransferases (Alcohol Group Acceptor) / genetics
  • Phosphotransferases (Alcohol Group Acceptor) / metabolism
  • Protein Binding
  • RNA, Messenger / biosynthesis

Substances

  • CREB1 protein, human
  • Culture Media, Serum-Free
  • Cyclic AMP Response Element-Binding Protein
  • RNA, Messenger
  • Phosphotransferases (Alcohol Group Acceptor)
  • sphingosine kinase
  • sphingosine kinase 2, human