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PMID: 15173221 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Recoverin regulates light-dependent phosphodiesterase activity in retinal rods.

The Journal of general physiology ·Vol. 123 ·No. 6 ·2004-06-00 ·Pages 729-41

Makino CL, Dodd RL, Chen J, Burns ME, Roca A, Simon MI, Baylor DA

Abstract

The Ca2+-binding protein recoverin may regulate visual transduction in retinal rods and cones, but its functional role and mechanism of action remain controversial. We compared the photoresponses of rods from control mice and from mice in which the recoverin gene was knocked out. Our analysis indicates that Ca2+-recoverin prolongs the dark-adapted flash response and increases the rod's sensitivity to dim steady light. Knockout rods had faster Ca2+ dynamics, indicating that recoverin is a significant Ca2+ buffer in the outer segment, but incorporation of exogenous buffer did not restore wild-type behavior. We infer that Ca2+-recoverin potentiates light-triggered phosphodiesterase activity, probably by effectively prolonging the catalytic activity of photoexcited rhodopsin.

MeSH Terms
Adaptation, Physiological/physiology,radiation effects Animals Calcium Signaling/physiology,radiation effects Calcium-Binding Proteins/deficiency,genetics,metabolism Cells, Cultured Dose-Response Relationship, Radiation Enzyme Activation/radiation effects Eye Proteins/genetics,metabolism Light Lipoproteins/deficiency,genetics,metabolism Membrane Potentials/drug effects,physiology Mice Mice, Inbred C57BL Mice, Knockout Phosphoric Diester Hydrolases/metabolism Recombinant Proteins/metabolism Recoverin Retinal Rod Photoreceptor Cells/physiology,radiation effects
Chemicals
Calcium-Binding Proteins Eye Proteins Lipoproteins Rcvrn protein, mouse Recombinant Proteins Recoverin Phosphoric Diester Hydrolases
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Makino Clint L
Department of Ophthalmology, Harvard Medical School and the Massachusetts Eye and Ear Infirmary, 243 Charles Street, Boston, MA 02114, USA. cmakino@meei.harvard.edu
Dodd R L
Chen J
Burns M E
Roca A
Simon M I
Baylor D A
References (56)
56 references, click to expand
  1. Slowed recovery of rod photoresponse in mice lacking the GTPase accelerating protein RGS9-1.
    Nature. 2000 Feb 3;403(6769):557-60 PMID: 10676965
  2. Rhodopsin phosphorylation as a mechanism of cyclic GMP phosphodiesterase regulation by S-modulin.
    Nature. 1993 Apr 29;362(6423):855-7 PMID: 8386803
  3. The role of steady phosphodiesterase activity in the kinetics and sensitivity of the light-adapted salamander rod photoresponse.
    J Gen Physiol. 2000 Dec;116(6):795-824 PMID: 11099349
  4. Phototransduction in transgenic mice after targeted deletion of the rod transducin alpha -subunit.
    Proc Natl Acad Sci U S A. 2000 Dec 5;97(25):13913-8 PMID: 11095744
  5. Analysis of Ca++-dependent gain changes in PDE activation in vertebrate rod phototransduction.
    Mol Vis. 2000 Dec 31;6:265-86 PMID: 11139649
  6. Adaptation in vertebrate photoreceptors.
    Physiol Rev. 2001 Jan;81(1):117-151 PMID: 11152756
  7. Molecular evidence that human ocular ciliary epithelium expresses components involved in phototransduction.
    Biochem Biophys Res Commun. 2001 Jun 8;284(2):317-25 PMID: 11394879
  8. Evaluation of the contributions of recoverin and GCAPs to rod photoreceptor light adaptation and recovery to the dark state.
    Prog Brain Res. 2001;131:395-405 PMID: 11420958
  9. Role of guanylate cyclase-activating proteins (GCAPs) in setting the flash sensitivity of rod photoreceptors.
    Proc Natl Acad Sci U S A. 2001 Aug 14;98(17):9948-53 PMID: 11493703
  10. Measurement of cytoplasmic calcium concentration in the rods of wild-type and transducin knock-out mice.
    J Physiol. 2002 Aug 1;542(Pt 3):843-54 PMID: 12154183
  11. Dynamics of cyclic GMP synthesis in retinal rods.
    Neuron. 2002 Sep 26;36(1):81-91 PMID: 12367508
  12. Light-dependent phosphorylation of rhodopsin. Purification and properties of rhodopsin kinase.
    J Biol Chem. 1978 Oct 10;253(19):7040-6 PMID: 690139
  13. Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy.
    J Comp Neurol. 1979 Nov 15;188(2):245-62 PMID: 500858
  14. Spatial spread of activation and background desensitization in toad rod outer segments.
    J Physiol. 1981;319:463-96 PMID: 6798202
  15. Application of acrylamide as an embedding medium in studies of lectin and antibody binding in the vertebrate retina.
    Curr Eye Res. 1984 Jul;3(7):969-74 PMID: 6432446
  16. Light-induced reduction of cytoplasmic free calcium in retinal rod outer segment.
    Nature. 1985 Feb 14-20;313(6003):579-82 PMID: 2578628
  17. Rhodopsin's amino terminus is a principal antigenic site.
    Exp Eye Res. 1986 Apr;42(4):363-73 PMID: 2423355
  18. The 35- and 36-kDa beta subunits of GTP-binding regulatory proteins are products of separate genes.
    J Biol Chem. 1988 Apr 15;263(11):5008-11 PMID: 3128533
  19. Extrusion of calcium from rod outer segments is driven by both sodium and potassium gradients.
    Nature. 1989 Feb 23;337(6209):740-3 PMID: 2537471
  20. Epitope mapping of bovine retinal S-antigen with monoclonal antibodies.
    Curr Eye Res. 1988 Nov;7(11):1137-47 PMID: 2468451
  21. Light adaptation in cat retinal rods.
    Science. 1989 Aug 18;245(4919):755-8 PMID: 2772634
  22. Cytoplasmic calcium as the messenger for light adaptation in salamander rods.
    J Physiol. 1989 Sep;416:215-43 PMID: 2607449
  23. Calcium-dependent regulation of cyclic GMP phosphodiesterase by a protein from frog retinal rods.
    Nature. 1991 Jan 31;349(6308):420-3 PMID: 1846944
  24. Inhibition of rhodopsin kinase by recoverin. Further evidence for a negative feedback system in phototransduction.
    J Biol Chem. 1995 Jul 7;270(27):16147-52 PMID: 7608179
  25. Differential distribution of six calcium-binding proteins in the rat olfactory epithelium during postnatal development and adulthood.
    J Comp Neurol. 1995 Apr 10;354(3):395-409 PMID: 7541806
  26. Ca(2+)-dependent interaction of recoverin with rhodopsin kinase.
    J Biol Chem. 1995 Jul 28;270(30):18060-6 PMID: 7629115
  27. Recoverin, a photoreceptor-specific calcium-binding protein, is expressed by the tumor of a patient with cancer-associated retinopathy.
    Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9176-80 PMID: 7568096
  28. The cGMP-phosphodiesterase and its contribution to sensitivity regulation in retinal rods.
    J Gen Physiol. 1995 Nov;106(5):891-921 PMID: 8648297
  29. Static and dynamic actions of cytoplasmic Ca2+ in the adaptation of responses to saturating flashes in salamander rods.
    J Physiol. 1996 Jan 1;490 ( Pt 1):1-15 PMID: 8745275
  30. Photoreceptor protein s26, a cone homologue of S-modulin in frog retina.
    J Biol Chem. 1996 Aug 30;271(35):21359-64 PMID: 8702916
  31. Actions of Ca2+ on an early stage in phototransduction revealed by the dynamic fall in Ca2+ concentration during the bright flash response.
    J Gen Physiol. 1997 Feb;109(2):141-6 PMID: 9041444
  32. Recoverin has S-modulin activity in frog rods.
    J Biol Chem. 1993 Jul 15;268(20):14579-82 PMID: 8392055
  33. The presence of a calcium-sensitive p26-containing complex in bovine retina rod cells.
    FEBS Lett. 1993 Dec 6;335(2):277-9 PMID: 7902818
  34. Expression of recoverin mRNA in the human retina: localization by in situ hybridization.
    Exp Eye Res. 1993 Dec;57(6):763-9 PMID: 8150028
  35. A rhodopsin gene mutation responsible for autosomal dominant retinitis pigmentosa results in a protein that is defective in localization to the photoreceptor outer segment.
    J Neurosci. 1994 Oct;14(10):5818-33 PMID: 7523628
  36. Mechanisms of rhodopsin inactivation in vivo as revealed by a COOH-terminal truncation mutant.
    Science. 1995 Jan 20;267(5196):374-7 PMID: 7824934
  37. Amino-terminal myristoylation induces cooperative calcium binding to recoverin.
    J Biol Chem. 1995 Mar 3;270(9):4526-33 PMID: 7876221
  38. Two eye guanylyl cyclases are expressed in the same photoreceptor cells and form homomers in preference to heteromers.
    J Biol Chem. 1997 May 23;272(21):13738-42 PMID: 9153227
  39. Molecular forms of human rhodopsin kinase (GRK1).
    J Biol Chem. 1998 Feb 27;273(9):5124-31 PMID: 9478965
  40. The effect of recombinant recoverin on the photoresponse of truncated rod photoreceptors.
    Proc Natl Acad Sci U S A. 1998 May 26;95(11):6474-9 PMID: 9600991
  41. Origin of reproducibility in the responses of retinal rods to single photons.
    Biophys J. 1998 Oct;75(4):1836-57 PMID: 9746525
  42. Phosphorylation of photolyzed rhodopsin is calcium-insensitive in retina permeabilized by alpha-toxin.
    Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):15014-9 PMID: 9844007
  43. Core mutations that promote the calcium-induced allosteric transition of bovine recoverin.
    Biochemistry. 1998 Dec 15;37(50):17408-19 PMID: 9860856
  44. 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
  45. Molecular mechanisms of vertebrate photoreceptor light adaptation.
    Curr Opin Neurobiol. 1999 Aug;9(4):410-8 PMID: 10448166
  46. Aberrant expression of photoreceptor-specific calcium-binding protein (recoverin) in cancer cell lines.
    Cancer Res. 2000 Apr 1;60(7):1914-20 PMID: 10766180
  47. Recoverin: a calcium sensitive activator of retinal rod guanylate cyclase.
    Science. 1991 Feb 22;251(4996):915-8 PMID: 1672047
  48. Light adaptation in retinal rods of the rabbit and two other nonprimate mammals.
    J Gen Physiol. 1991 Mar;97(3):413-35 PMID: 2037836
  49. Calcium feedback and sensitivity regulation in primate rods.
    J Gen Physiol. 1991 Jul;98(1):95-130 PMID: 1719127
  50. Isoprenylation of a protein kinase. Requirement of farnesylation/alpha-carboxyl methylation for full enzymatic activity of rhodopsin kinase.
    J Biol Chem. 1992 Jan 25;267(3):1422-5 PMID: 1730692
  51. Light-dependent delay in the falling phase of the retinal rod photoresponse.
    Vis Neurosci. 1992 Jan;8(1):9-18 PMID: 1739680
  52. Noncatalytic cGMP-binding sites of amphibian rod cGMP phosphodiesterase control interaction with its inhibitory gamma-subunits. A putative regulatory mechanism of the rod photoresponse.
    J Biol Chem. 1992 Dec 5;267(34):24501-7 PMID: 1332960
  53. Recoverin in pineal organs and retinae of various vertebrate species including man.
    Brain Res. 1992 Nov 6;595(1):57-66 PMID: 1467959
  54. Calcium homeostasis in the outer segments of retinal rods from the tiger salamander.
    J Physiol. 1992 Sep;455:111-42 PMID: 1282928
  55. Recoverin immunoreactivity in mammalian cone bipolar cells.
    Vis Neurosci. 1993 Jan-Feb;10(1):1-12 PMID: 8424920
  56. The effect of recoverin-like calcium-binding proteins on the photoresponse of retinal rods.
    Neuron. 1993 Mar;10(3):523-31 PMID: 8461139
Article Info
Journal
The Journal of general physiology
Abbr.
J Gen Physiol
ISSN
0022-1295
Published
2004-06-00
Pages
729-41
Language
English
Region
United States
NLM ID
2985110R
PMCID
PMC2234569
Subset
IM
Grants
NEI NIH HHS · R01 EY014047-04 · United States
NEI NIH HHS · R01 EY014047 · United States
NEI NIH HHS · R01 EY012703 · United States
NEI NIH HHS · EY12703 · United States
NEI NIH HHS · EY05750 · United States
NEI NIH HHS · R01 EY012944 · United States
NEI NIH HHS · EY14047 · United States
NIA NIH HHS · AG12288 · United States
NEI NIH HHS · EY12944 · United States
Corrections
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