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A Tale of Two Kinases in Rods and Cones

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Book cover Retinal Degenerative Diseases

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 723))

Abstract

Members of the G protein-coupled receptor kinase family play essential roles in signal turnoff for the majority of G protein-coupled receptors. GRK1, first identified almost 40 years ago, and GRK7, the most recently identified member of the GRK family, are retina-specific GRKs involved in the recovery and adaptation of rod and cone photoreceptors in the vertebrate retina. This report reviews the expression patterns of these two kinases, as well as the effect of their interaction with their substrates and binding partners. The phosphorylation of GRK1 and GRK7 by cAMP-dependent protein kinase (PKA) is also discussed.

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References

  • Arinobu D, Tachibanaki S, Kawamura S (2010) Larger inhibition of visual pigment kinase in cones than in rods. J Neurochem 115:259–268

    Article  PubMed  CAS  Google Scholar 

  • Bauer PH, Müller S, Puzicha M et al (1992) Phosducin is a protein kinase A-regulated G-protein regulator. Nature 358:73–76

    Article  PubMed  CAS  Google Scholar 

  • Baylor DA (1987) Photoreceptor signals and vision. The Proctor lecture. Invest Ophthalmol Vis Sci 28:34–49

    PubMed  CAS  Google Scholar 

  • Caenepeel S, Charydczak G, Sudarsanam S et al (2004) The mouse kinome: discovery and comparative genomics of all mouse protein kinases. Proc Natl Acad Sci USA 101:11707–11712

    Article  PubMed  CAS  Google Scholar 

  • Chen CK, Burns ME, Spencer M et al (1999) Abnormal photoresponses and light-induced apoptosis in rods lacking rhodopsin kinase. Proc Natl Acad Sci USA 96:3718–3722

    Article  PubMed  CAS  Google Scholar 

  • Chen CK, Inglese J, Lefkowitz RJ et al (1995) Ca2+-dependent interaction of recoverin with rhodopsin kinase. J Biol Chem 270:18060–18066

    Article  PubMed  CAS  Google Scholar 

  • Chen CK, Woodruff ML, Chen FS et al (2010) Background light produces a recoverin-dependent modulation of activated-rhodopsin lifetime in mouse rods. J Neurosci 30:1213–1220

    Article  PubMed  CAS  Google Scholar 

  • Chen CK, Zhang K, Church-Kopish J et al (2001) Characterization of human GRK7 as a potential cone opsin kinase. Mol Vis 7:305–313

    PubMed  CAS  Google Scholar 

  • Chen CY, Dion SB, Kim CM et al (1993) Beta-adrenergic receptor kinase. Agonist-dependent receptor binding promotes kinase activation. J Biol Chem 268:7825–7831

    PubMed  CAS  Google Scholar 

  • Cideciyan AV, Jacobson SG, Gupta N et al (2003) G-protein-coupled receptor kinase 1 (GRK1) and GRK7 expression and cone deactivation kinetics in enhanced S-cone syndrome (ESCS) caused by mutations in NR2E3. Invest Ophthalmol Vis Sci 44:1268–1274

    Article  PubMed  Google Scholar 

  • Cideciyan AV, Zhao X, Nielsen L et al (1998) Null mutation in the rhodopsin kinase gene slows recovery kinetics of rod and cone phototransduction in man. Proc Natl Acad Sci USA 95:328–333

    Article  PubMed  CAS  Google Scholar 

  • Cohen AI, Todd RD, Harmon S et al (1992) Photoreceptors of mouse retinas possess D4 receptors coupled to adenylate cyclase. Proc Natl Acad Sci USA 89:12093–12097

    Article  PubMed  CAS  Google Scholar 

  • Dryja TP (2000) Molecular genetics of Oguchi disease, fundus albipunctatus, and other forms of stationary night blindness: LVII Edward Jackson Memorial Lecture. Am J Ophthalmol 130:547–563

    Article  PubMed  CAS  Google Scholar 

  • Farber DB, Souza DW, Chase DG et al (1981) Cyclic nucleotides of cone-dominant retinas. Reduction of cyclic AMP levels by light and by cone degeneration. Invest Ophthalmol Vis Sci 20:24–31

    PubMed  CAS  Google Scholar 

  • Fowles C, Sharma R, Akhtar M (1988) Mechanistic studies on the phosphorylation of photorexcited rhodopsin. FEBS Lett 238:56–60

    Article  CAS  Google Scholar 

  • Futuyama DJ (1998) Evolutionary Biology, 3 rd Edition. Sunderland, MA: Sinauer Associates, Inc.

    Google Scholar 

  • Ganguly S, Gastel JA, Weller JL et al (2001) Role of a pineal cAMP-operated arylalkylamine N-acetyltransferase/14–3-3-binding switch in melatonin synthesis. Proc Natl Acad Sci USA 98:8083–8088

    Article  PubMed  CAS  Google Scholar 

  • Hisatomi O, Matsuda S, Satoh T et al (1998) A novel subtype of G-protein-coupled receptor kinase, GRK7, in teleost cone photoreceptors. FEBS Lett 424:159–164

    Article  PubMed  CAS  Google Scholar 

  • Horner TJ, Osawa S, Schaller MD et al (2005) Phosphorylation of GRK1 and GRK7 by cAMP-dependent protein kinase attenuates their enzymatic activities. J Biol Chem 280:28241–28250

    Article  PubMed  CAS  Google Scholar 

  • Huang CC, Yoshino-Koh K, Tesmer JJ (2009) A surface of the kinase domain critical for the allosteric activation of G protein-coupled receptor kinases. J Biol Chem 284:17206–17215

    Article  PubMed  CAS  Google Scholar 

  • Imanishi Y, Hisatomi O, Yamamoto S et al (2007) A third photoreceptor-specific GRK found in the retina of Oryzias latipes (Japanese killifish). Zool Sci 24:87–93

    Article  PubMed  CAS  Google Scholar 

  • Ivanova TN, Iuvone PM (2003) Circadian rhythm and photic control of cAMP level in chick retinal cell cultures: a mechanism for coupling the circadian oscillator to the melatonin-synthesizing enzyme, arylalkylamine N-acetyltransferase, in photoreceptor cells. Brain Res 991:96–103

    Article  PubMed  CAS  Google Scholar 

  • Kawamura S (1993) Rhodopsin phosphorylation as a mechanism of cyclic GMP phosphodiesterase regulation by S-modulin. Nature 362:855–857

    Article  PubMed  CAS  Google Scholar 

  • Kawamura S, Tachibanaki S (2008) Rod and cone photoreceptors: molecular basis of the difference in their physiology. Comp Biochem Physiol A Mol Integr Physiol 150:369–377

    Article  PubMed  Google Scholar 

  • Klenchin VA, Calvert PD, Bownds MD (1995) Inhibition of rhodopsin kinase by recoverin. Further evidence for a negative feedback system in phototransduction. J Biol Chem 270:16147–16152

    Article  PubMed  CAS  Google Scholar 

  • Knox BE, Solessio E (2006) Shedding light on cones. J Gen Physiol 127:355–358

    Article  PubMed  Google Scholar 

  • Kühn H, Wilden U (1987) Deactivation of photoactivated rhodopsin by rhodopsin-kinase and arrestin. J Recept Res 7:283–298

    PubMed  Google Scholar 

  • Lee RH, Ting TD, Lieberman BS et al (1992) Regulation of retinal cGMP cascade by phosducin in bovine rod photoreceptor cells. Interaction of phosducin and transducin. J Biol Chem 267:25104–25112

    PubMed  CAS  Google Scholar 

  • Liu P, Osawa S, Weiss ER (2005) M opsin phosphorylation in intact mammalian retinas. J Neurochem 93:135–144

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Green CB (2002) Circadian regulation of nocturnin transcription by phosphorylated CREB in Xenopus retinal photoreceptor cells. Mol Cell Biol 22:7501–7511

    Article  PubMed  CAS  Google Scholar 

  • Lyubarsky AL, Chen C-K, Simon MI et al (2000) Mice lacking G-protein receptor kinase 1 have profoundly slowed recovery of cone-driven retinal responses. J Neurosci 20:2209–2217

    PubMed  CAS  Google Scholar 

  • Maeda T, Imanishi Y, Palczewski K (2003) Rhodopsin phosphorylation: 30 years later. Prog Ret Eye Res 22:417–434

    Article  CAS  Google Scholar 

  • Makino CL, Dodd RL, Chen J et al (2004) Recoverin regulates light-dependent phosphodiesterase activity in retinal rods. J Gen Physiol 123:729–741

    Article  PubMed  CAS  Google Scholar 

  • Osawa S, Jo R, Weiss ER (2008) Phosphorylation of GRK7 by PKA in cone photoreceptor cells is regulated by light. J Neurochem 107:1314–1324

    Article  PubMed  CAS  Google Scholar 

  • Palczewski K, Buczylko J, Kaplan MW et al (1991) Mechanism of rhodopsin kinase activation. J Biol Chem 266:12949–12955

    PubMed  CAS  Google Scholar 

  • Rinner O, Makhankov YV, Biehlmaier O et al (2005) Knockdown of cone-specific kinase GRK7 in larval zebrafish leads to impaired cone response recovery and delayed dark adaptation. Neuron 47:231–242

    Article  PubMed  CAS  Google Scholar 

  • Shimauchi-Matsukawa Y, Aman Y, Tachibanaki S et al (2005) Isolation and characterization of visual pigment kinase-related genes in carp retina: polyphyly in GRK1 subtypes, GRK1A and 1B. Mol Vis 11:1220–1228

    PubMed  CAS  Google Scholar 

  • Tachibanaki S, Arinobu D, Shimauchi-Matsukawa Y et al (2005) Highly effective phosphorylation by G protein-coupled receptor kinase 7 of light-activated visual pigment in cones. Proc Natl Acad Sci USA 102:9329–9334

    Article  PubMed  CAS  Google Scholar 

  • Tosini G, Pozdeyev N, Sakamoto K et al (2008) The circadian clock system in the mammalian retina. Bioessays 30:624–633

    Article  PubMed  CAS  Google Scholar 

  • Wada Y, Sugiyama J, Okano T et al (2006) GRK1 and GRK7: unique cellular distribution and widely different activities of opsin phosphorylation in the zebrafish rods and cones. J Neurochem 98:824–837

    Article  PubMed  CAS  Google Scholar 

  • Weiss ER, Ducceschi MH, Horner TJ et al (2001) 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 21:9175–9184

    PubMed  CAS  Google Scholar 

  • Weiss ER, Jo R, Osawa S (2008) GRK1 Is Phosphorylated in Dark-Adapted Mice in vivo. ARVO Meeting Abstracts 49:1668

    Google Scholar 

  • Weiss ER, Raman D, Shirakawa S et al (1998) The cloning of GRK7, a candidate cone opsin kinase, from cone- and rod-dominant mammalian retinas. Mol Vis 4, 27:<http://www.molvis.org/molvis/v4/p27>

  • Wiechmann AF, Summers JA (2008) Circadian rhythms in the eye: the physiological significance of melatonin receptors in ocular tissues. Prog Ret Eye Res 27:137–160

    Article  CAS  Google Scholar 

  • Wilden U, Kühn H (1982) Light-dependent phosphorylation of rhodopsin: the number of phosphorylation sites. Biochemistry 21:3014–3022

    Article  PubMed  CAS  Google Scholar 

  • Xu LX, Tanaka Y, Bonderenko VA et al (1998) Phosphorylation of the gamma subunit of the retinal photoreceptor cGMP phosphodiesterase by the cAMP-dependent protein kinase and its effect on the gamma subunit interaction with other proteins. Biochemistry 37:6205–6213

    Article  PubMed  CAS  Google Scholar 

  • Yu CJ, Gao Y, Willis CL et al (2007) Mitogen-associated protein kinase- and protein kinase A-dependent regulation of rhodopsin promoter expression in zebrafish rod photoreceptor cells. J Neurosci Res 85:488–496

    Article  PubMed  CAS  Google Scholar 

  • Zhao X, Yokoyama K, Whitten ME et al (1999) A novel form of rhodopsin kinase from chicken retina and pineal gland. FEBS Lett 454:115–121

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to acknowledge financial support from the NEI (EY072224 and EY019758) and from the NIH Core Grant for Vision Research (EY5722; Duke University).

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Authors and Affiliations

  1. Department of Cell and Developmental Biology, The University of North Carolina at Chapel Hill, CB# 7090, 108 Taylor Hall, Chapel Hill, NC, 27599, USA

    Shoji Osawa & Ellen R. Weiss

  2. Lineberger Comprehensive Cancer Center, The University of North Carolina at Chapel Hill, Chapel Hill, NC, 27599-7090, USA

    Ellen R. Weiss

Authors
  1. Shoji Osawa
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  2. Ellen R. Weiss
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Corresponding author

Correspondence to Ellen R. Weiss .

Editor information

Editors and Affiliations

  1. University of California, San Francisco, n/a, San Francisco, 94143, USA

    Matthew M. LaVail

  2. University of Oklahoma Health Sciences C, Oklahoma City, 73104, USA

    John D. Ash

  3. Health Science Center, Dean A. McGee Eye Inst., University of Oklahoma, Stanton L. Young Blvd. 608, OKLAHOMA CITY, 73104, Oklahoma, USA

    Robert E. Anderson

  4. Division of Ophthalmology, Cole Eye Institute at the Cleveland Clin, Euclid Ave. 9500, Cleveland, 44195, Ohio, USA

    Joe G. Hollyfield

  5. Experimental Ophthalmology, University of Zurich, ZURICH, 8091, Switzerland

    Christian Grimm

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Osawa, S., Weiss, E.R. (2012). A Tale of Two Kinases in Rods and Cones. In: LaVail, M., Ash, J., Anderson, R., Hollyfield, J., Grimm, C. (eds) Retinal Degenerative Diseases. Advances in Experimental Medicine and Biology, vol 723. Springer, Boston, MA. https://doi.org/10.1007/978-1-4614-0631-0_105

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