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J. Biol. Chem., Vol. 260, Issue 3, 1493-1500, 02, 1985
RA Cerione, C Staniszewski, JL Benovic, RJ Lefkowitz, MG Caron, P Gierschik, R Somers, AM Spiegel, J Codina and L Birnbaumer
We have assessed the functional interactions of two pure receptor proteins
with three different pure guanine nucleotide regulatory proteins in
phosphatidylcholine vesicles. The receptor proteins are the guinea pig lung
beta-adrenergic receptor (beta AR) and the retinal photon receptor
rhodopsin. The guanine nucleotide regulatory proteins were the stimulatory
(Ns) and inhibitory (Ni) proteins of the adenylate cyclase system and
transducin (T), the regulatory protein from the light-activated cyclic GMP
phosphodiesterase system in retinal rod outer segments. The insertion of Ns
with beta AR in lipid vesicles increases the extent of binding of [35S] GTP
gamma S to Ns and in parallel, the total GTPase activity. However, there is
little change in the actual rate of catalytic turnover of GTPase activity
(defined as mol of Pi released/min/mol of Ns-guanine nucleotide complexes).
Enhancement of this turnover rate requires the beta-agonist isoproterenol
and is accounted for by an isoproterenol-promoted increase in the rate and
extent of [35S]GTP gamma S binding to Ns. The co-insertion of the beta AR
with Ni or transducin results in markedly lower stimulation by
isoproterenol of both the GTPase activity and [35S]GTP gamma S binding to
these nucleotide regulatory proteins indicating that their preferred order
of interaction with beta AR is Ns much greater than Ni greater than T. This
contrasts with the preferred order of interaction of these different
nucleotide regulatory proteins with light-activated rhodopsin which we find
to be T approximately equal to Ni much greater than Ns. Nonetheless the
fold stimulation of GTPase activity and [35S]GTP gamma S binding in T,
induced by light- activated rhodopsin, is significantly greater than the
"fold" stimulation of these activities in Ni. This reflects the greater
intrinsic ability of Ni to hydrolyze GTP and bind guanine nucleotides (at
10 mM MgCl2, 100-200 nM GTP or [35S] GTP gamma S) compared to T. The
maximum turnover numbers for the rhodopsin-stimulated GTPase in both Ni and
T are similar to those obtained for isoproterenol- stimulated activity in
Ns. This suggests that the different nucleotide regulatory proteins are
capable of a common upper limit of catalytic efficiency which can best be
attained when coupled to the appropriate receptor.
Specificity of the functional interactions of the beta-adrenergic receptor and rhodopsin with guanine nucleotide regulatory proteins reconstituted in phospholipid vesicles
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