Protease-activated receptor-1 can mediate responses to SFLLRN in thrombin-desensitized cells: evidence for a novel mechanism for preventing or terminating signaling by PAR1's tethered ligand

Biochemistry. 1999 Feb 23;38(8):2486-93. doi: 10.1021/bi982527i.

Abstract

The thrombin receptor PAR1 is activated when thrombin cleaves the receptor's amino-terminal exodomain to reveal the new N-terminal sequence SFLLRN which then acts as a tethered peptide ligand. Free SFLLRN activates PAR1 independent of receptor cleavage and has been used to probe PAR1 function in various cells and tissues. PAR1-expressing cells desensitized to thrombin retain responsiveness to SFLLRN. Toward determining the mechanism of such responses, we utilized fibroblasts derived from a PAR1-deficient mouse. These cells were unresponsive to thrombin and SFLLRN and became sensitive to both ligands after transfection with human PAR1 cDNA. Moreover, PAR1-transfected cells responded to SFLLRN after thrombin-desensitization, indicating that signaling of thrombin-desensitized cells to SFLLRN was mediated by PAR1 itself. SFLLRN caused signaling in thrombin-desensitized cells when no uncleaved PAR1 was detectable on the cell surface; however, cleaved PAR1 was present. To determine whether the cleaved receptors could still signal, fibroblasts were transfected with a PAR1 mutant containing a trypsin site/SFLLRN sequence carboxyl terminal to the native thrombin site. These cells retained responsiveness to trypsin after thrombin-desensitization. Conversely, fibroblasts expressing a PAR1 mutant with the trypsin site/SFLLRN sequence amino terminal to the native thrombin site retained responsiveness to thrombin after trypsin-desensitization. This suggests that a population of thrombin-cleaved PAR1 can respond both to exogenous SFLLRN and to a second tethered ligand. In this population, the tethered ligand unmasked by thrombin cleavage must not be functional, suggesting the possibility of a novel mechanism of receptor shutoff involving sequestration or modification of the tethered ligand to prevent or terminate its function.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Binding Sites / genetics
  • Calcium / metabolism
  • Cell Line
  • Fibroblasts / enzymology
  • Fibroblasts / metabolism
  • Humans
  • Hydrolysis
  • Ligands
  • Lung / cytology
  • Mice
  • Mice, Knockout
  • Molecular Sequence Data
  • Peptide Fragments / pharmacology*
  • Receptor, PAR-1
  • Receptors, Thrombin / biosynthesis
  • Receptors, Thrombin / genetics
  • Receptors, Thrombin / metabolism
  • Receptors, Thrombin / physiology*
  • Signal Transduction* / drug effects
  • Signal Transduction* / genetics
  • Thrombin / agonists
  • Thrombin / pharmacology*
  • Time Factors

Substances

  • Ligands
  • Peptide Fragments
  • Receptor, PAR-1
  • Receptors, Thrombin
  • thrombin receptor peptide (42-47)
  • Thrombin
  • Calcium