A permissive role of pertussis toxin substrate G-protein in P2-purinergic stimulation of phosphoinositide turnover and arachidonate release in FRTL-5 thyroid cells. Cooperative mechanism of signal transduction systems

J Biol Chem. 1989 Aug 5;264(22):13029-37.

Abstract

Extracellular ATP and other purinergic agonists were found to inhibit cAMP accumulation by depressing adenylate cyclase as an "inhibitory action" and/or to stimulate arachidonate release in association with phospholipase C or A2 activation and Ca2+ mobilization as "stimulatory actions" in FRTL-5 cells. The stimulatory actions of a group of P2-agonists represented by ATP were partially inhibited by the pretreatment of the cells with islet-activating protein (IAP), pertussis toxin, even when an about 41-kDa membrane protein(s) was completely ADP-ribosylated. Only the IAP-sensitive part of the stimulatory actions was antagonized by 1,3-diethyl-8-phenylxanthine (DPX), an adenosine antagonist. GTP and 8-bromoadenosine 5'-triphosphate (Br-ATP) at two to three orders of higher concentrations than ATP also exerted the stimulatory actions, although they were entirely insensitive to both IAP and DPX. Ligand binding experiments with, [35S]ATP gamma S and [3H]DPX showed that ATP occupies both DPX-sensitive and insensitive receptor sites, whereas GTP does only ATP-displaceable DPX-insensitive sites. Thus, lack of sensitivity of GTP action to DPX was associated with its inability to occupy the DPX-sensitive sites. Adenosine 5'-O-(1-thiotriphosphate) (ATP alpha S), adenosine 5'-O-(2-thiodiphosphate) (ADP beta S) and P1-agonists such as AMP and N6-(L-2-phenylisopropyl-adenosine (PIA) did not show any stimulatory action. Nevertheless, the agonists remarkably enhanced the stimulatory actions of GTP or Br-ATP. Such permissive actions of PIA and others were sensitive to both IAP and DPX, as were shown for a part of the stimulatory actions of ATP as well as the "inhibitory actions" of both PIA and ATP. We conclude that an IAP substrate G-protein(s) which mediates the inhibitory action of purinergic agonists via a DPX-sensitive purinergic receptor(s) may not directly link to the phospholipase C or A2 system but enhance the system which links to a DPX-insensitive P2-receptor, in an indirect or permissive manner.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Diphosphate / metabolism
  • Adenosine Diphosphate / pharmacology
  • Adenosine Triphosphate / metabolism
  • Adenosine Triphosphate / pharmacology
  • Adenylate Cyclase Toxin*
  • Animals
  • Arachidonic Acid
  • Arachidonic Acids / metabolism*
  • Calcium / metabolism
  • Cell Line
  • Cyclic AMP / antagonists & inhibitors
  • Cyclic AMP / metabolism
  • GTP-Binding Proteins / physiology*
  • Guanosine Triphosphate / pharmacology
  • Pertussis Toxin*
  • Phenylisopropyladenosine / antagonists & inhibitors
  • Phenylisopropyladenosine / pharmacology
  • Phosphatidylinositols / metabolism*
  • Rats
  • Receptors, Purinergic / drug effects
  • Receptors, Purinergic / physiology*
  • Signal Transduction* / drug effects
  • Thyroid Gland / metabolism*
  • Thyroid Gland / physiology
  • Thyrotropin / pharmacology
  • Virulence Factors, Bordetella / antagonists & inhibitors
  • Virulence Factors, Bordetella / physiology*
  • Xanthines / pharmacology

Substances

  • Adenylate Cyclase Toxin
  • Arachidonic Acids
  • Phosphatidylinositols
  • Receptors, Purinergic
  • Virulence Factors, Bordetella
  • Xanthines
  • Arachidonic Acid
  • Phenylisopropyladenosine
  • 1,3-diethyl-8-phenylxanthine
  • Adenosine Diphosphate
  • Guanosine Triphosphate
  • Adenosine Triphosphate
  • Thyrotropin
  • Cyclic AMP
  • Pertussis Toxin
  • GTP-Binding Proteins
  • Calcium