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PMID: 6285349 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Functional exchange of components between light-activated photoreceptor phosphodiesterase and hormone-activated adenylate cyclase systems.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 79 ·No. 11 ·1982-06-00 ·Pages 3408-12

Bitensky MW, Wheeler MA, Rasenick MM, Yamazaki A, Stein PJ, Halliday KR, Wheeler GL

Abstract

Previous studies have noted profound similarities between the regulation of light-activated 3',5'-cyclic nucleotide phosphodiesterase (3',5'-cyclic-nucleotide 5'-nucleotidohydrolase, EC 3.1.4.17) in retinal rods and hormone-activated adenylate cyclase [ATP pyrophosphate-lyase (cyclizing), EC 4.6.1.1] in a variety of tissues. We report here the functional exchange of components isolated from the photoreceptor system, which displayed predicted functional characteristics when incubated with recipient adenylate cyclase systems from rat cerebral cortical and hypothalamic synaptic membranes and frog erythrocyte ghosts. We demonstrate functional exchange of photoreceptor components at each of three loci: the hormone receptor, the GTP-binding protein (GBP), and the catalytic moiety of adenylate cyclase. Illuminated (but not unilluminated) rhodopsin was fund to mimic the hormone-receptor complex, causing GTP-dependent activation of adenylate cyclase. The photoreceptor GBP complexed with guanosine 5'-[beta, gamma)imidotriphosphate (p[NH]ppG) produced a marked activation of recipient adenylate cyclase systems. Much smaller activation was observed when GBP was not complexed with p[NH]ppG. A heat-stable photoreceptor phosphodiesterase inhibitor reduced both basal and Mn2+-activated adenylate cyclase activities and this inhibition was reversed by photoreceptor GBP.p[NH]ppG. These data demonstrate a remarkable functional compatibility between subunits of both systems and furthermore imply that specialized peptide domains responsible for protein-protein interactions are highly conserved.

MeSH Terms

3',5'-Cyclic-GMP Phosphodiesterases/metabolism Adenylyl Cyclases/metabolism Animals Bufo marinus Enzyme Activation Erythrocyte Membrane/enzymology Erythrocytes/enzymology GTP-Binding Proteins Photoreceptor Cells/enzymology Rats Receptors, Cell Surface/metabolism Rhodopsin/metabolism Rod Cell Outer Segment/enzymology Species Specificity Synaptic Membranes/enzymology

Chemicals

Receptors, Cell Surface Rhodopsin 3',5'-Cyclic-GMP Phosphodiesterases GTP-Binding Proteins Adenylyl Cyclases

Authors & Affiliations

7 authors, click to expand affiliations / ORCID

Bitensky M W

Wheeler M A

Rasenick M M

Yamazaki A

Stein P J

Halliday K R

Wheeler G L

References (28)

28 references, click to expand

A second ouabain-sensitive sodium-dependent adenosine triphosphate in brain microsomes.
J Biol Chem. 1969 Dec 10;244(23):6493-7 PMID: 4242925
A simple and sensitive saturation assay method for the measurement of adenosine 3':5'-cyclic monophosphate.
Biochem J. 1971 Feb;121(3):561-2 PMID: 4330379
Preparation and properties of phospholipid bilayers containing rhodopsin.
Proc Natl Acad Sci U S A. 1972 Sep;69(9):2617-21 PMID: 4341702
Regulation of cyclic nucleotide concentrations in photoreceptors: an ATP-dependent stimulation of cyclic nucleotide phosphodiesterase by light.
Proc Natl Acad Sci U S A. 1973 Dec;70(12):3820-4 PMID: 4359491
Role of adenine and guanine nucleotides in the activity and response of adenylate cyclase systems to hormones: evidence for multisite transition states.
Adv Cyclic Nucleotide Res. 1975;5:3-29 PMID: 236641
Identification of adenylate cyclase-coupled beta-adrenergic receptors in frog erythrocytes with (minus)-[3-H] alprenolol.
J Biol Chem. 1975 Jul 10;250(13):4869-76 PMID: 238972
Assay of picomole amounts of ATP, ADP, and AMP using the luciferase enzyme system.
Anal Biochem. 1975 Nov;69(1):187-206 PMID: 2029
Protein inhibitor of cyclic adenosine 3':5'-monophosphate phosphodiesterase in retina.
Biochim Biophys Acta. 1976 Apr 8;429(2):474-8 PMID: 177072
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
GTP-binding proteins in membranes and the control of adenylate cyclase activity.
J Biol Chem. 1977 Oct 25;252(20):7224-34 PMID: 903360
A light-activated GTPase in vertebrate photoreceptors: regulation of light-activated cyclic GMP phosphodiesterase.
Proc Natl Acad Sci U S A. 1977 Oct;74(10):4238-42 PMID: 200909
Light- and GTP-activated photoreceptor phosphodiesterase: regulation by a light-activated GTPase and identification of rhodopsin as the phosphodiesterase binding site.
Adv Cyclic Nucleotide Res. 1978;9:553-72 PMID: 27082
Implications of RNA-RNA splicing in evolution of eukaryotic cells.
Science. 1978 Dec 22;202(4374):1257-60 PMID: 364651
Split genes and RNA splicing.
Science. 1979 Apr 20;204(4390):264-71 PMID: 373120
Predictive value of the analogy between hormone-sensitive adenylate cyclase and light-sensitive photoreceptor cyclic GMP phosphodiesterase: a specific role for a light-sensitive GTPase as a component in the activation sequence.
J Supramol Struct. 1979;10(2):185-90 PMID: 222967
Fluoride stimulation of adenylate cyclase is dependent on the guanine nucleotide regulatory protein.
J Biol Chem. 1980 Feb 10;255(3):949-54 PMID: 6243302
Light- and GTP-regulated interaction of GTPase and other proteins with bovine photoreceptor membranes.
Nature. 1980 Feb 7;283(5747):587-9 PMID: 6101903
Isolation and recombination of bovine rod outer segment cGMP phosphodiesterase and its regulators.
Biochem Biophys Res Commun. 1980 Jan 29;92(2):505-10 PMID: 6101951
Two mRNAs with different 3' ends encode membrane-bound and secreted forms of immunoglobulin mu chain.
Cell. 1980 Jun;20(2):303-12 PMID: 6771019
Biochemical properties of hormone-sensitive adenylate cyclase.
Annu Rev Biochem. 1980;49:533-64 PMID: 6105841
Partial purification and characterization of a macromolecule which enhances fluoride activation of adenylate cyclase.
Proc Natl Acad Sci U S A. 1980 Aug;77(8):4628-32 PMID: 6933510
Cyclic GMP-specific, high affinity, noncatalytic binding sites on light-activated phosphodiesterase.
J Biol Chem. 1980 Dec 10;255(23):11619-24 PMID: 6254976
Purification of the regulatory component of adenylate cyclase.
Proc Natl Acad Sci U S A. 1980 Nov;77(11):6516-20 PMID: 6935665
Hormone-sensitive adenylate cyclase. Mutant phenotype with normally regulated beta-adrenergic receptors uncoupled with catalytic adenylate cyclase.
Mol Pharmacol. 1981 Sep;20(2):435-41 PMID: 6272096
The regulatory subunit of adenylate cyclase interacts with cytoskeletal components.
Nature. 1981 Dec 10;294(5841):560-2 PMID: 7312044
Agaridoxin: a fungal catecholamine which acts as an alpha 1 agonist of mammalian hypothalamic adenylate cyclase.
Brain Res. 1982 Jan 14;231(2):387-98 PMID: 6120025
A GTP-protein activator of phosphodiesterase which forms in response to bleached rhodopsin.
J Cyclic Nucleotide Res. 1981;7(2):95-104 PMID: 6278004
Reciprocal effects of an inhibitory factor on catalytic activity and noncatalytic cGMP binding sites of rod phosphodiesterase.
Proc Natl Acad Sci U S A. 1982 Jun;79(12):3702-6 PMID: 6285360

Article Info

Journal

Proceedings of the National Academy of Sciences of the United States of America

Abbr.

Proc Natl Acad Sci U S A

ISSN

0027-8424

DOI

10.1073/pnas.79.11.3408

Published

1982-06-00

Pages

3408-12

Language

English

Region

United States

NLM ID

7505876

PMCID

PMC346429

Subset

External Links

PubMed source DOI: 10.1073/pnas.79.11.3408 PMC Full Text View journal details

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Functional exchange of components between light-activated photoreceptor phosphodiesterase and hormone-activated adenylate cyclase systems.

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