Ca(2+)-modulated Vision-linked ROS-GC Guanylate Cyclase Transduction Machinery

Overview

Journal Mol Cell Biochem

Publisher Springer

Specialty Biochemistry

Date 2009 Nov 28

PMID 19943184

Citations 33

Authors

Karl-W Koch

Teresa Duda

Rameshwar K Sharma

Affiliations

Soon will be listed here.

Abstract

Vertebrate phototransduction depends on the reciprocal relationship between two-second messengers, cyclic GMP and Ca(2+). The concentration of both is reciprocally regulated including the dynamic synthesis of cyclic GMP by a membrane bound guanylate cyclase. Different from hormone receptor guanylate cyclases, the cyclases operating in phototransduction are regulated by the intracellular Ca(2+)-concentration via small Ca(2+)-binding proteins. Based on the site of their expression and their Ca(2+) modulation, this sub-branch of the cyclase family was named sensory guanylate cyclases, of which the retina specific forms are named ROS-GCs (rod outer segment guanylate cyclases). This review focuses on the structure and function of the ROS-GC subfamily present in the mammalian retinal neurons: photoreceptors and inner layers of the retinal neurons. Portions and excerpts of the review are from a previous chapter (Curr Top Biochem Res 6:111-144, 2004).

Citing Articles

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References

Burgess W, Jemiolo D, Kretsinger R . Interaction of calcium and calmodulin in the presence of sodium dodecyl sulfate. Biochim Biophys Acta. 1980; 623(2):257-70. DOI: 10.1016/0005-2795(80)90254-8. View

Imanishi Y, Yang L, Sokal I, Filipek S, Palczewski K, Baehr W . Diversity of guanylate cyclase-activating proteins (GCAPs) in teleost fish: characterization of three novel GCAPs (GCAP4, GCAP5, GCAP7) from zebrafish (Danio rerio) and prediction of eight GCAPs (GCAP1-8) in pufferfish (Fugu rubripes). J Mol Evol. 2004; 59(2):204-217. PMC: 1351297. DOI: 10.1007/s00239-004-2614-y. View

Hwang J, Koch K . Calcium- and myristoyl-dependent properties of guanylate cyclase-activating protein-1 and protein-2. Biochemistry. 2002; 41(43):13021-8. DOI: 10.1021/bi026618y. View

Redburn D, Thomas T . Isolation of synaptosomal fractions from rabbit retina. J Neurosci Methods. 1979; 1(3):235-42. DOI: 10.1016/0165-0270(79)90034-7. View

Olshevskaya E, Ermilov A, Dizhoor A . Dimerization of guanylyl cyclase-activating protein and a mechanism of photoreceptor guanylyl cyclase activation. J Biol Chem. 1999; 274(36):25583-7. DOI: 10.1074/jbc.274.36.25583. View

Hwang J, Lange C, Helten A, Hoppner-Heitmann D, Duda T, Sharma R . Regulatory modes of rod outer segment membrane guanylate cyclase differ in catalytic efficiency and Ca(2+)-sensitivity. Eur J Biochem. 2003; 270(18):3814-21. DOI: 10.1046/j.1432-1033.2003.03770.x. View

Lim S, Peshenko I, Dizhoor A, Ames J . Effects of Ca2+, Mg2+, and myristoylation on guanylyl cyclase activating protein 1 structure and stability. Biochemistry. 2009; 48(5):850-62. PMC: 2637916. DOI: 10.1021/bi801897p. View

Perrault I, Rozet J, Calvas P, Gerber S, Camuzat A, Dollfus H . Retinal-specific guanylate cyclase gene mutations in Leber's congenital amaurosis. Nat Genet. 1996; 14(4):461-4. DOI: 10.1038/ng1296-461. View

Duda T, Koch K, Venkataraman V, Lange C, Beyermann M, Sharma R . Ca(2+) sensor S100beta-modulated sites of membrane guanylate cyclase in the photoreceptor-bipolar synapse. EMBO J. 2002; 21(11):2547-56. PMC: 125384. DOI: 10.1093/emboj/21.11.2547. View

10.

Duda T, Goraczniak R, Sharma R . Molecular characterization of S100A1-S100B protein in retina and its activation mechanism of bovine photoreceptor guanylate cyclase. Biochemistry. 1996; 35(20):6263-6. DOI: 10.1021/bi960007m. View

11.

Peshenko I, Dizhoor A . Guanylyl cyclase-activating proteins (GCAPs) are Ca2+/Mg2+ sensors: implications for photoreceptor guanylyl cyclase (RetGC) regulation in mammalian photoreceptors. J Biol Chem. 2004; 279(17):16903-6. DOI: 10.1074/jbc.C400065200. View

12.

Sampath A, Matthews H, Cornwall M, Fain G . Bleached pigment produces a maintained decrease in outer segment Ca2+ in salamander rods. J Gen Physiol. 1998; 111(1):53-64. PMC: 1887770. DOI: 10.1085/jgp.111.1.53. View

13.

Burgoyne R, Weiss J . The neuronal calcium sensor family of Ca2+-binding proteins. Biochem J. 2000; 353(Pt 1):1-12. PMC: 1221537. View

14.

Dizhoor A, Olshevskaya E, Henzel W, Wong S, Stults J, Ankoudinova I . Cloning, sequencing, and expression of a 24-kDa Ca(2+)-binding protein activating photoreceptor guanylyl cyclase. J Biol Chem. 1995; 270(42):25200-6. DOI: 10.1074/jbc.270.42.25200. View

15.

Burgoyne R . Neuronal calcium sensor proteins: generating diversity in neuronal Ca2+ signalling. Nat Rev Neurosci. 2007; 8(3):182-93. PMC: 1887812. DOI: 10.1038/nrn2093. View

16.

Wensel T . Signal transducing membrane complexes of photoreceptor outer segments. Vision Res. 2008; 48(20):2052-61. PMC: 2615670. DOI: 10.1016/j.visres.2008.03.010. View

17.

Stephen R, Filipek S, Palczewski K, Sousa M . Ca2+ -dependent regulation of phototransduction. Photochem Photobiol. 2008; 84(4):903-10. PMC: 4118144. DOI: 10.1111/j.1751-1097.2008.00323.x. View

18.

Kelsell R, Gregory-Evans K, Payne A, Perrault I, Kaplan J, Yang R . Mutations in the retinal guanylate cyclase (RETGC-1) gene in dominant cone-rod dystrophy. Hum Mol Genet. 1998; 7(7):1179-84. DOI: 10.1093/hmg/7.7.1179. View

19.

Burns M, Baylor D . Activation, deactivation, and adaptation in vertebrate photoreceptor cells. Annu Rev Neurosci. 2001; 24:779-805. DOI: 10.1146/annurev.neuro.24.1.779. View

20.

Yu H, Olshevskaya E, Duda T, Seno K, Hayashi F, Sharma R . Activation of retinal guanylyl cyclase-1 by Ca2+-binding proteins involves its dimerization. J Biol Chem. 1999; 274(22):15547-55. DOI: 10.1074/jbc.274.22.15547. View