Thrombin Enhanced Matrix Metalloproteinase-9 Expression and Migration of SK-N-SH Cells via PAR-1, c-Src, PYK2, EGFR, Erk1/2 and AP-1

Mol Neurobiol. 2017 Jul;54(5):3476-3491. doi: 10.1007/s12035-016-9916-0. Epub 2016 May 16.

Abstract

Neuroinflammation is a hallmark of neurodegenerative disorders in the central nerve system (CNS). Thrombin has been known as one of the factors in pathological processes including migration, blood-brain barrier breakdown, brain edema formation, neuroinflammation, and neuronal death. Thrombin has been shown to be a regulator of matrix metalloproteinase (MMPs) expression leading to cell migration. Among MMPs, the elevated expression of MMP-9 has been observed in patients with brain diseases, which may contribute to the pathology of neuroinflammatory and neurodegenerative diseases. However, the mechanisms underlying thrombin-induced MMP-9 expression in SK-N-SH cells were not completely understood. Here, we used gelatin zymography, Western blot, real-time PCR, promoter activity assay, and cell migration assay to demonstrate that thrombin induced the expression of pro-form MMP-9 protein and messenger RNA (mRNA), and promoter activity in SK-N-SH cells, which were attenuated by pretreatment with the pharmacological inhibitor of protease-activated receptor-1 (PAR-1, SCH79797), Gi-coupled receptor (GPA2), c-Src (PP1), Pyk2 (PF431396), EGFR (AG1478), PI3K (LY294002), Akt (SH-5), MEK1/2 (U0126), or AP-1 (TanshinoneIIA) and transfection with small interfering RNA (siRNA) of PAR-1, Gi, c-Src, Pyk2, EGFR, Akt, p44, p42, or c-Jun. Moreover, thrombin-stimulated c-Src, Pyk2, EGFR, Akt, p42/p44 MAPK, or c-Jun phosphorylation was attenuated by their respective inhibitor of PP1, PF431396, AG1478, SH-5, U0126, or TanshinoneIIA. Finally, pretreatment with these inhibitors also blocked thrombin-induced SK-N-SH cell migration. Our results concluded that thrombin binding to PAR-1 receptor activated Gi-protein/c-Src/Pyk2/EGFR/PI3K/Akt/p42/p44 MAPK cascade, which in turn elicited AP-1 activation and ultimately evoked MMP-9 expression and cell migration in SK-N-SH cells.

Keywords: Matrix metalloproteinase-9; Neurodegeneration; Signaling pathway; Thrombin.

MeSH terms

  • CSK Tyrosine-Protein Kinase
  • Cell Line, Tumor
  • Cell Movement / drug effects*
  • ErbB Receptors / metabolism*
  • Extracellular Signal-Regulated MAP Kinases / metabolism*
  • Focal Adhesion Kinase 2 / metabolism*
  • GTP-Binding Protein alpha Subunits, Gi-Go / metabolism
  • Humans
  • Matrix Metalloproteinase 9 / metabolism*
  • Models, Biological
  • Phosphatidylinositol 3-Kinases / metabolism
  • Proto-Oncogene Proteins c-akt / metabolism
  • Receptor, PAR-1 / metabolism*
  • Signal Transduction / drug effects
  • Thrombin / pharmacology*
  • Transcription Factor AP-1 / metabolism*
  • Transcriptional Activation / drug effects
  • src-Family Kinases / metabolism*

Substances

  • Receptor, PAR-1
  • Transcription Factor AP-1
  • ErbB Receptors
  • CSK Tyrosine-Protein Kinase
  • Focal Adhesion Kinase 2
  • src-Family Kinases
  • CSK protein, human
  • Proto-Oncogene Proteins c-akt
  • Extracellular Signal-Regulated MAP Kinases
  • Thrombin
  • Matrix Metalloproteinase 9
  • GTP-Binding Protein alpha Subunits, Gi-Go