Home LiteratureArticle Details
PMID: 15958532 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Highly effective phosphorylation by G protein-coupled receptor kinase 7 of light-activated visual pigment in cones.

Tachibanaki S, Arinobu D, Shimauchi-Matsukawa Y, Tsushima S, Kawamura S

Abstract

Cone photoreceptors show briefer photoresponses than rod photoreceptors. Our previous study showed that visual pigment phosphorylation, a quenching mechanism of light-activated visual pigment, is much more rapid in cones than in rods. Here, we measured the early time course of this rapid phosphorylation with good time resolution and directly compared it with the photoresponse time course in cones. At the time of photoresponse recovery, almost two phosphates were incorporated into a bleached cone pigment molecule, which indicated that the visual pigment phosphorylation coincides with the photoresponse recovery. The rapid phosphorylation in cones is attributed to very high activity of visual pigment kinase [G protein-coupled receptor kinase (GRK) 7] in cones. Because of this high activity, cone pigment is readily phosphorylated at very high bleach levels, which probably explains why cone photoresponses recover quickly even after a very bright light and do not saturate under intense background light. The high GRK7 activity is brought about by high content of a highly potent enzyme. The expression level of GRK7 was 10 times higher than that of rod kinase (GRK1), and the specific activity of a single GRK7 molecule was approximately 10 times higher than that of GRK1. The specific activity of GRK7 is the highest among the GRKs so far known. Our result seems to explain the response characteristics of cone photoreceptors in many aspects, including the nonsaturation of the cone responses during daylight vision.

MeSH Terms
Animals Carps Cell Membrane/metabolism Electrophysiology Eye Proteins/metabolism G-Protein-Coupled Receptor Kinase 1 G-Protein-Coupled Receptor Kinases Glutathione Transferase/metabolism Kinetics Light Phosphorylation Photoreceptor Cells/metabolism,physiology Protein Binding Protein Kinases/metabolism Protein Serine-Threonine Kinases/chemistry,metabolism Protein Structure, Tertiary Recombinant Proteins/chemistry Retinal Cone Photoreceptor Cells/metabolism Retinal Pigments/metabolism Retinal Rod Photoreceptor Cells/metabolism Time Factors Vision, Ocular
Chemicals
Eye Proteins Recombinant Proteins Retinal Pigments Glutathione Transferase Protein Kinases Protein Serine-Threonine Kinases G-Protein-Coupled Receptor Kinase 1 GRK7 protein, human G-Protein-Coupled Receptor Kinases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Tachibanaki Shuji
Graduate School of Frontier Biosciences, Osaka University, Suita, Osaka 565-0871, Japan.
Arinobu Daisuke
Shimauchi-Matsukawa Yoshie
Tsushima Sawae
Kawamura Satoru
References (39)
39 references, click to expand
  1. A novel subtype of G-protein-coupled receptor kinase, GRK7, in teleost cone photoreceptors.
    FEBS Lett. 1998 Mar 13;424(3):159-64 PMID: 9539142
  2. Prolonged photoresponses in transgenic mouse rods lacking arrestin.
    Nature. 1997 Oct 2;389(6650):505-9 PMID: 9333241
  3. Visual pigment: G-protein-coupled receptor for light signals.
    Cell Mol Life Sci. 1998 Dec;54(12):1299-315 PMID: 9893707
  4. Light-dependent changes in outer segment free-Ca2+ concentration in salamander cone photoreceptors.
    J Gen Physiol. 1999 Feb;113(2):267-77 PMID: 9925824
  5. Abnormal photoresponses and light-induced apoptosis in rods lacking rhodopsin kinase.
    Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3718-22 PMID: 10097103
  6. In situ microspectrophotometric studies on the pigments of single retinal rods.
    Biophys J. 1962 Mar;2:161-78 PMID: 14465191
  7. Photoreceptors of Nrl -/- mice coexpress functional S- and M-cone opsins having distinct inactivation mechanisms.
    J Gen Physiol. 2005 Mar;125(3):287-304 PMID: 15738050
  8. Light adaptation and photopigment bleaching in cone photoreceptors in situ in the retina of the turtle.
    J Neurosci. 1994 Mar;14(3 Pt 1):1091-105 PMID: 8120614
  9. Expression, purification, and characterization of the G protein-coupled receptor kinase GRK6.
    J Biol Chem. 1994 Sep 9;269(36):22691-7 PMID: 8077221
  10. Ca(2+)-dependent interaction of recoverin with rhodopsin kinase.
    J Biol Chem. 1995 Jul 28;270(30):18060-6 PMID: 7629115
  11. Amino acid residues of S-modulin responsible for interaction with rhodopsin kinase.
    J Biol Chem. 2000 Feb 4;275(5):3313-9 PMID: 10652319
  12. Mice lacking G-protein receptor kinase 1 have profoundly slowed recovery of cone-driven retinal responses.
    J Neurosci. 2000 Mar 15;20(6):2209-17 PMID: 10704496
  13. Rapid and reproducible deactivation of rhodopsin requires multiple phosphorylation sites.
    Neuron. 2000 Oct;28(1):153-64 PMID: 11086991
  14. Species-specific differences in expression of G-protein-coupled receptor kinase (GRK) 7 and GRK1 in mammalian cone photoreceptor cells: implications for cone cell phototransduction.
    J Neurosci. 2001 Dec 1;21(23):9175-84 PMID: 11717351
  15. Low amplification and fast visual pigment phosphorylation as mechanisms characterizing cone photoresponses.
    Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):14044-9 PMID: 11707584
  16. Cone deactivation kinetics and GRK1/GRK7 expression in enhanced S cone syndrome caused by mutations in NR2E3.
    Invest Ophthalmol Vis Sci. 2003 Mar;44(3):1268-74 PMID: 12601058
  17. Rhodopsin phosphorylation: 30 years later.
    Prog Retin Eye Res. 2003 Jul;22(4):417-34 PMID: 12742390
  18. Role of visual pigment properties in rod and cone phototransduction.
    Nature. 2003 Oct 2;425(6957):526-31 PMID: 14523449
  19. Visual pigment phosphorylation but not transducin translocation can contribute to light adaptation in zebrafish cones.
    Neuron. 2004 Mar 25;41(6):915-28 PMID: 15046724
  20. Control of retinal sensitivity. I. Light and dark adaptation of vertebrate rods and cones.
    J Gen Physiol. 1974 Jan;63(1):37-61 PMID: 4359063
  21. Absorption spectra and linear dichroism of some amphibian photoreceptors.
    J Gen Physiol. 1975 Sep;66(3):357-82 PMID: 808586
  22. Sensitivity of toad rods: Dependence on wave-length and background illumination.
    J Physiol. 1976 Sep;261(1):71-101 PMID: 825637
  23. Light-dependent phosphorylation of rhodopsin. Purification and properties of rhodopsin kinase.
    J Biol Chem. 1978 Oct 10;253(19):7040-6 PMID: 690139
  24. Lipid mixing during freeze-thawing of liposomal membranes as monitored by fluorescence energy transfer.
    Biochim Biophys Acta. 1983 Nov 9;735(2):243-51 PMID: 6688739
  25. Rhodopsin kinase prepared from bovine rod disk membranes quenches light activation of cGMP phosphodiesterase in a reconstituted system.
    Biochemistry. 1986 Sep 23;25(19):5460-8 PMID: 3022791
  26. Characterization of a bovine cone photoreceptor phosphodiesterase purified by cyclic GMP-sepharose chromatography.
    J Biol Chem. 1988 Jun 15;263(17):8133-41 PMID: 2836413
  27. Purification and characterization of rhodopsin kinase.
    J Biol Chem. 1988 Oct 5;263(28):14067-73 PMID: 2844754
  28. Phosphorylation of iodopsin, chicken red-sensitive cone visual pigment.
    Biochemistry. 1990 Oct 30;29(43):10102-6 PMID: 2271641
  29. Calcium-dependent regulation of cyclic GMP phosphodiesterase by a protein from frog retinal rods.
    Nature. 1991 Jan 31;349(6308):420-3 PMID: 1846944
  30. Recoverin: a calcium sensitive activator of retinal rod guanylate cyclase.
    Science. 1991 Feb 22;251(4996):915-8 PMID: 1672047
  31. Light-dependent delay in the falling phase of the retinal rod photoresponse.
    Vis Neurosci. 1992 Jan;8(1):9-18 PMID: 1739680
  32. Primary structures of chicken cone visual pigments: vertebrate rhodopsins have evolved out of cone visual pigments.
    Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):5932-6 PMID: 1385866
  33. Rhodopsin phosphorylation as a mechanism of cyclic GMP phosphodiesterase regulation by S-modulin.
    Nature. 1993 Apr 29;362(6423):855-7 PMID: 8386803
  34. Expression, purification, and characterization of the G protein-coupled receptor kinase GRK5.
    J Biol Chem. 1994 Jan 14;269(2):1099-105 PMID: 8288567
  35. Phototransduction mechanism in retinal rods and cones. The Friedenwald Lecture.
    Invest Ophthalmol Vis Sci. 1994 Jan;35(1):9-32 PMID: 7507907
  36. Identification, purification, and characterization of GRK5, a member of the family of G protein-coupled receptor kinases.
    J Biol Chem. 1994 Mar 4;269(9):6832-41 PMID: 8120045
  37. Photoreceptor protein s26, a cone homologue of S-modulin in frog retina.
    J Biol Chem. 1996 Aug 30;271(35):21359-64 PMID: 8702916
  38. Activation of transducin by a Xenopus short wavelength visual pigment.
    J Biol Chem. 1997 Jan 10;272(2):1095-100 PMID: 8995408
  39. The cloning of GRK7, a candidate cone opsin kinase, from cone- and rod-dominant mammalian retinas.
    Mol Vis. 1998 Dec 8;4:27 PMID: 9852166
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
Published
2005-06-28
Epub
2005-00-15
Pages
9329-34
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1166601
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com