Squid Rhodopsin and GTP-binding Protein Crossreact with Vertebrate Photoreceptor Enzymes

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1984 Aug 1

PMID 6147847

Citations 17

Authors

H R Saibil

Affiliations

Soon will be listed here.

Abstract

The activation of photoreceptor GTP-binding protein by rhodopsin was studied in squid photoreceptors and in crossreactions between the squid and bovine proteins. Turbidity changes were observed in the far-red after photoexcitation of rhodopsin with brief flashes and were used to probe interactions between photoreceptor membrane suspensions and soluble protein extracts. Our findings are squid photoreceptors contain a GTP-binding protein detectable by light- and GTP-sensitive turbidity changes and by limited sequence homology of a 46-kilodalton polypeptide to the alpha-subunit of bovine GTP-binding protein; the squid membranes activate bovine GTP-binding protein qualitatively in the same way as bovine rhodopsin; the 46-kilodalton component is present in a membrane-bound fraction but is more abundant in a crude, soluble fraction of squid rhabdomes, and this soluble fraction can interact with either squid or bovine rhodopsin-containing membranes; light-activated GTPase activities in all of these preparations are consistent with the light-induced turbidity changes. These results show that rhodopsin activation of GTP-binding protein is highly conserved in vertebrate and cephalopod photoreceptors. Since squid rhodopsin is immobilized in precisely ordered microvilli, this suggests that activation of GTP-binding protein in cephalopod photoreceptors occurs in the absence of rhodopsin diffusion. The rhodopsin immobility may be compensated by higher mobility of the soluble GTP-binding protein.

Citing Articles

Crystal structure of squid rhodopsin with intracellularly extended cytoplasmic region.

Shimamura T, Hiraki K, Takahashi N, Hori T, Ago H, Masuda K J Biol Chem. 2008; 283(26):17753-6.

PMID: 18463093 PMC: 2440622. DOI: 10.1074/jbc.C800040200.

The molecular cloning of the squid (Loligo forbesi) visual Gq-alpha subunit and its expression in Saccharomyces cerevisiae.

Ryba N, Findlay J, REID J Biochem J. 1993; 292 ( Pt 2):333-41.

PMID: 8503868 PMC: 1134214. DOI: 10.1042/bj2920333.

Spatial properties of the prolonged depolarizing afterpotential in barnacle photoreceptors. I. The induction process.

Almagor E, Hillman P, Minke B J Gen Physiol. 1986; 87(3):391-405.

PMID: 3958692 PMC: 2217611. DOI: 10.1085/jgp.87.3.391.

Photoenergetics of octopus rhodopsin. Convergent evolution of biological photon counters?.

Cooper A, Dixon S, Tsuda M Eur Biophys J. 1986; 13(4):195-201.

PMID: 3709418 DOI: 10.1007/BF00260367.

Nontransducing rhodopsin.

Levine E, Crain E, Robinson P, Lisman J J Gen Physiol. 1987; 90(4):575-86.

PMID: 3681262 PMC: 2228870. DOI: 10.1085/jgp.90.4.575.

References

Calhoon R, Tsuda M, Ebrey T . A light-activated GTPase from octopus photoreceptors. Biochem Biophys Res Commun. 1980; 94(4):1452-7. DOI: 10.1016/0006-291x(80)90582-3. View

Vandenberg C, Montal M . Light-regulated biochemical events in invertebrate photoreceptors. 1. Light-activated guanosinetriphosphatase, guanine nucleotide binding, and cholera toxin catalyzed labeling of squid photoreceptor membranes. Biochemistry. 1984; 23(11):2339-47. DOI: 10.1021/bi00306a003. View

Fung B, Hurley J, Stryer L . Flow of information in the light-triggered cyclic nucleotide cascade of vision. Proc Natl Acad Sci U S A. 1981; 78(1):152-6. PMC: 319009. DOI: 10.1073/pnas.78.1.152. View

Kuhn H, Bennett N, Chabre M . Interactions between photoexcited rhodopsin and GTP-binding protein: kinetic and stoichiometric analyses from light-scattering changes. Proc Natl Acad Sci U S A. 1981; 78(11):6873-7. PMC: 349154. DOI: 10.1073/pnas.78.11.6873. View

Morrissey J . Silver stain for proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Anal Biochem. 1981; 117(2):307-10. DOI: 10.1016/0003-2697(81)90783-1. View

Henis Y, Hekman M, Elson E, Helmreich E . Lateral motion of beta receptors in membranes of cultured liver cells. Proc Natl Acad Sci U S A. 1982; 79(9):2907-11. PMC: 346317. DOI: 10.1073/pnas.79.9.2907. View

Bitensky M, Wheeler M, Rasenick M, Yamazaki A, STEIN P, Halliday K . Functional exchange of components between light-activated photoreceptor phosphodiesterase and hormone-activated adenylate cyclase systems. Proc Natl Acad Sci U S A. 1982; 79(11):3408-12. PMC: 346429. DOI: 10.1073/pnas.79.11.3408. View

Emeis D, Kuhn H, Reichert J, Hofmann K . Complex formation between metarhodopsin II and GTP-binding protein in bovine photoreceptor membranes leads to a shift of the photoproduct equilibrium. FEBS Lett. 1982; 143(1):29-34. DOI: 10.1016/0014-5793(82)80266-4. View

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

10.

Miki N, Keirns J, Marcus F, Freeman J, Bitensky M . 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; 70(12):3820-4. PMC: 427336. DOI: 10.1073/pnas.70.12.3820. View

11.

Rodbell M, Lin M, Salomon Y, Londos C, Harwood J, Martin B . 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. View

12.

Cleveland D, Fischer S, Kirschner M, Laemmli U . Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J Biol Chem. 1977; 252(3):1102-6. View

13.

Wheeler G, Bitensky M . A light-activated GTPase in vertebrate photoreceptors: regulation of light-activated cyclic GMP phosphodiesterase. Proc Natl Acad Sci U S A. 1977; 74(10):4238-42. PMC: 431914. DOI: 10.1073/pnas.74.10.4238. View

14.

Calvert R, Gratzer W . Proteolytic digestion patterns of spectrin subunits. FEBS Lett. 1978; 86(2):247-9. DOI: 10.1016/0014-5793(78)80572-9. View

15.

Hanski E, Rimon G, Levitzki A . Adenylate cyclase activation by the beta-adrenergic receptors as a diffusion-controlled process. Biochemistry. 1979; 18(5):846-53. DOI: 10.1021/bi00572a017. View

16.

Woodruff M, Bownds M . Amplitude, kinetics, and reversibility of a light-induced decrease in guanosine 3',5'-cyclic monophosphate in frog photoreceptor membranes. J Gen Physiol. 1979; 73(5):629-53. PMC: 2215193. DOI: 10.1085/jgp.73.5.629. View

17.

Liebman P, Pugh Jr E . The control of phosphodiesterase in rod disk membranes: kinetics, possible mechanisms and significance for vision. Vision Res. 1979; 19(4):375-80. DOI: 10.1016/0042-6989(79)90097-x. View

18.

Kuhn H . Light- and GTP-regulated interaction of GTPase and other proteins with bovine photoreceptor membranes. Nature. 1980; 283(5747):587-9. DOI: 10.1038/283587a0. View

19.

Saibil H . An ordered membrane-cytoskeleton network in squid photoreceptor microvilli. J Mol Biol. 1982; 158(3):435-56. DOI: 10.1016/0022-2836(82)90208-x. View

20.

Bennett N, Kuhn H . Light-induced interaction between rhodopsin and the GTP-binding protein. Metarhodopsin II is the major photoproduct involved. Eur J Biochem. 1982; 127(1):97-103. DOI: 10.1111/j.1432-1033.1982.tb06842.x. View