Thrombin mediates migration of rat brain astrocytes via PLC, Ca²⁺, CaMKII, PKCα, and AP-1-dependent matrix metalloproteinase-9 expression

Mol Neurobiol. 2013 Dec;48(3):616-30. doi: 10.1007/s12035-013-8450-6. Epub 2013 Apr 13.

Abstract

Matrix metalloproteinase-9 (MMP-9) plays a crucial role in pathological processes of brain inflammation, injury, and neurodegeneration. Thrombin has been known as a regulator of MMP-9 expression and cells migration. However, the mechanisms underlying thrombin-induced MMP-9 expression in rat brain astrocytes (RBA-1 cells) remain unclear. Here, we demonstrated that thrombin induced the expression of pro-form MMP-9 and migration of RBA-1 cells, which were inhibited by pretreatment with the inhibitor of Gq-coupled receptor (GPAnt2A), Gi/o-coupled receptor (GPAnt2), PC-PLC (D609), PI-PLC (U73122), Ca(2+)-ATPase (thapsigargin, TG), calmodulin (CaMI), CaMKII (KN62), PKC (Gö6976 or GF109203X), MEK1/2 (PD98059), p38 MAPK (SB202190), JNK1/2 (SP600125), or AP-1 (Tanshinone IIA) or the intracellular calcium chelator (BAPTA/AM) and transfection with siRNA of PKCα, Erk2, JNK1, p38 MAPK, c-Jun, or c-Fos. In addition, thrombin-induced elevation of intracellular Ca(2+) concentration was attenuated by PPACK (a thrombin inhibitor). Thrombin further induced CaMKII phosphorylation and PKCα translocation, which were inhibited by U73122, D609, KN62, TG, or BAPTA/AM. Thrombin also induced PKCα-dependent p42/p44 MAPK and JNK1/2, but not p38 MAPK activation. Finally, we showed that thrombin enhanced c-Fos expression and c-Jun phosphorylation. c-Fos mRNA levels induced by thrombin were reduced by PD98059, SP600125, and Gö6976, but not SB202190. Thrombin stimulated in vivo binding of c-Fos to the MMP-9 promoter, which was reduced by pretreatment with SP600125 or PD98059, but not SB202190. These results concluded that thrombin activated a PLC/Ca(2+)/CaMKII/PKCα/p42/p44 MAPK and JNK1/2 pathway, which in turn triggered AP-1 activation and ultimately induced MMP-9 expression in RBA-1 cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Astrocytes / cytology
  • Astrocytes / drug effects
  • Astrocytes / enzymology*
  • Brain / cytology
  • Calcium / metabolism
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism*
  • Calmodulin / metabolism
  • Cell Movement / drug effects*
  • Cells, Cultured
  • Enzyme Precursors / metabolism*
  • Matrix Metalloproteinase 9 / metabolism*
  • Mitogen-Activated Protein Kinases / metabolism
  • Protein Biosynthesis / drug effects
  • Protein Kinase C-alpha / metabolism*
  • Rats
  • Receptors, G-Protein-Coupled / metabolism
  • Signal Transduction / drug effects
  • Thrombin / pharmacology*
  • Transcription Factor AP-1 / metabolism*
  • Transcription, Genetic / drug effects
  • Type C Phospholipases / metabolism*

Substances

  • Calmodulin
  • Enzyme Precursors
  • Receptors, G-Protein-Coupled
  • Transcription Factor AP-1
  • Protein Kinase C-alpha
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Mitogen-Activated Protein Kinases
  • Type C Phospholipases
  • phosphatidylcholine-specific phospholipase C
  • Thrombin
  • pro-matrix metalloproteinase 9
  • Matrix Metalloproteinase 9
  • Calcium