Abstract
Teleost fishes like medaka fish (Oryzias latipes), zebrafish (Danio rerio), and pufferfish (Fugu rubripes) contain in their genomes a larger number of guanylate cyclases and guanylate cyclase-activating proteins than mammals. Based on amino acid sequence alignments a group of transmembrane sensory guanylate cyclases can be identified, which are mainly if not exclusively expressed in sensory organs like the retina and olfactory tissue. Retina specific guanylate cyclases and guanylate cyclase-activating proteins in the zebrafish show dynamic changes in their spatial–temporal expression patterns and transcripts of the corresponding genes appear coincidently with the beginning of cone cell maturation at 3 days post-fertilization. Expression patterns of the guanylate cyclase signaling systems during larval development are correlated with the special habitat challenges of zebrafishes in the wild.
Similar content being viewed by others
References
Sharma RK (2002) Evolution of the membrane guanylate cyclase transduction system. Mol Cell Biochem 230:3–30
Baker DA, Kelly JM (2004) Structure, function and evolution of microbial adenylyl and guanylyl cyclases. Mol Microbiol 52:1229–1242
Fitzpatrick DA, O’Halloran DM, Burnell AM (2006) Multiple lineage specific expansions within the guanylyl cyclase gene family. BMC Evol Biol 6:26
Linder JU, Schultz JE (2002) Guanylyl cyclases in unicellular organisms. Mol Cell Biochem 230:149–158
Russwurm M, Koesling D (2002) Isoforms of NO-sensitive guanylyl cyclase. Mol Cell Biochem 230:159–164
Bellamy TC, Garthwaite J (2002) The receptor-like properties of nitric oxide-activated soluble guanylyl cyclase in intact cells. Mol Cell Biochem 230:165–176
Tamura N, Chrisman TD, Garbers DL (2001) The regulation, physiological roles of the guanylyl cyclase receptors. Endocr J 48:611–634
Koch KW, Duda T, Sharma RK (2002) Photoreceptor specific guanylate cyclases in vertebrate phototransduction. Mol Cell Biochem 230:97–106
Koch K-W, Stryer L (1988) Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature 334:64–66
Dizhoor AM, Lowe DG, Olshevskaya EV, Laura RP, Hurley JB (1994) The human photoreceptor membrane guanylyl cyclase, RetGC, is present in outer segments and is regulated by calcium and a soluble activator. Neuron 12:1345–1352
Gorczyca WA, Gray-Keller MP, Detwiler PB, Palczewski K (1994) Purification and physiological evaluation of a guanylate cyclase activating protein from retinal rods. Proc Natl Acad Sci USA 91:4014–4018
Palczewski K, Subbaraya I, Gorczyca WA, Helekar BS, Ruiz CC, Ohguro H, Huang J, Zhao X, Crabb JW, Johnson RS, Walsh KA, Gray-Keller MP, Detwiler PB, Baehr W (1994) Molecular cloning and characterization of retinal photoreceptor guanylyl cyclase-activating protein. Neuron 13:395–404
Dizhoor AM, Olshevskaya EV, Henzel WJ, Wong SC, Stults JT, Ankoudinova I, Hurley JB (1995) Cloning, sequencing, and expression of a 24-kDa Ca2+-binding protein activating photoreceptor guanylyl cyclase. J Biol Chem 270:25200–25206
Gorczyca WA, Polans AS, Surgucheva IG, Subbaraya I, Baehr W, Palczewski K (1995) Guanylyl cyclase activating protein. J Biol Chem 270:22029–22036
Frins S, Bönigk W, Müller F, Kellner R, Koch K-W (1996) Functional characterization of a guanylyl cyclase-activating protein from vertebrate rods. J Biol Chem 271:8022–8027
Mendez A, Burns ME, Sokal I, Dizhoor AM, Baehr W, Palczewski K, Baylor DA, Chen J (2001) Role of guanylate cyclase-activating proteins (GCAPs) in setting the flash sensitivity of rod photoreceptors. Proc Natl Acad Sci USA 98:9948–9953
Howes KA, Pennesi ME, Sokal I, Church-Kopish J, Schmidt B, Margolis D, Frederick JM, Rieke F, Palczewski K, Wu SM, Detwiler PB, Baehr W (2002) GCAP1 rescues rod photoreceptor response in GCAP1/GCAP2 knockout mice. EMBO J 21:1545–1554
Burns ME, Mendez A, Chen J, Baylor DA (2002) Dynamics of cyclic GMP synthesis in retinal rods. Neuron 36:81–91
Makino CL, Peshenko IV, Wen XH, Olshevskaya EV, Barrett R, Dizhoor AM (2008) A role for GCAP2 in regulating the photoresponse: guanylyl cyclase activation and rod electrophysiology in GUCA1B knock-out mice. J Biol Chem 283:29135–29143
Yang RB, Robinson SW, Xiong WH, Yau KW, Birch DG, Garbers DL (1999) Disruption of a retinal guanylyl cyclase gene leads to cone-specific distrophy and paradoxical rod behavior. J Neurosci 19:5889–5897
Baehr W, Karan S, Maeda T, Luo DG, Li S, Bronson JD, Watt CB, Yau KW, Frederick JM, Palczewski K (2007) The function of guanylate cyclase 1 (GC1) and guanylate cyclase 2 (GC2) in rod and cone photoreceptors. J Biol Chem 282:8837–8847
Juilfs DM, Fülle HJ, Zhao AZ, Hously MD, Garbers DL (1997) A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanyly cyclase-D define a unique olfactory signal transduction pathway. Proc Natl Acad Sci USA 94:3388–3395
Meyer MR, Angele A, Kremmer E, Kaupp UB, Müller F (2000) A cGMP-signaling pathway in a subset of olfactory sensory neurons. Proc Natl Acad Sci USA 97:10595–10600
Leinders-Zufall T, Cockerham RE, Michalakis S, Biel M, Garbers DL, Reed RR, Zufall F, Munger SD (2007) Contribution of the receptor guanyly cyclase GC-D to chemosensory function in the olfactory epithelium. Proc Natl Acad Sci USA 104:14507–14512
Duda T, Jankowska A, Venkataraman V, Nagele RG, Sharma RK (2001) A novel calcium-regulated membrane guanylate cyclase transduction system in the olfactory neuroepithelium. Biochemistry 40:12067–12077
Chinen A, Hamaoka T, Yamada Y, Kawamura S (2003) Gene duplication and spectral diversification of cone visual pigments of zebrafish. Genetics 163:663–675
Takechi M, Kawamura S (2005) Temporal and spatial changes in the expression pattern of multiple red and green subtype opsin genes during zebrafish development. J Exp Biol 208:1337–1345
Brockerhoff SE, Hurley JB, Janssen-Bienhold U, Neuhauss SCF, Driever W, Dowling JE (1995) A behavioral screen for isolating zebrafish mutants with visual system defects. Proc Natl Acad Sci USA 92:10545–10549
Neuhauss SCF, Biehlmaier O, Seeliger MW, Das T, Kohler K, Harris WA, Baier H (1999) Genetic disorders of vision revealed by a behavioral screen of 400 essential loci in zebrafish. J Neurosci 19:8603–8615
Bilotta J, Saszik S (2001) The zebrafish as a model visual system. Int J Dev Neurosci 19:621–629
Rinner O, Rick JM, Neuhauss SCF (2005) Contrast sensitivity, spatial and temporal tuning of the larval zebrafish optokinetic response. Invest Ophthalmol Vis Sci 46:137–142
Seimiya M, Kusakabe T, Suzuki N (1997) Primary structure and differential gene expression of three membrane forms of guanylyl cyclase found in the eye of the teleost Oryzias latipes. J Biol Chem 272:23407–23417
Hisatome O, Honkawa H, Imanishsi Y, Satoh T, Tokunaga F (1999) Three kinds of guanylate cyclase expressed in medaka photoreceptor cells in both retina and pineal organ. Biochem Biophys Res Commun 255:216–220
Kusakabe T, Suzuke N (2000) Photoreceptors and olfactory cells express the same retinal guanyly cyclase isoform in medaka: visualization by promote transgenics. FEBS Lett 483:143–148
Harumi T, Watanabe T, Yamamoto T, Tanabe Y, Suzuki N (2003) Expression of membrane-bound and soluble guanylyl-cyclase mRNAs in embryonic and adult retina of the medaka fish Oryzias latipes. Zool Sci 20:133–140
Yamagami S, Suzuki N (2005) Diverse forms of guanylyl cyclases in medaka fish—their genomic structure and phylogenetic relationships to those in vertebrates and invertebrates. Zool Sci 22:819–835
Imanishi Y, Yang L, Sokal I, Filipek S, Palczewski K, Baehr W (2004) 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 59:204–217
Brockerhoff SE, Rieke F, Matthews HR, Taylor MR, Kennedy B, Ankoudinova I, Niemi GA, Tucker CL, Xiao M, Cilluffo MC, Fain GL, Hurley JB (2003) Light stimulates a transducin-independent increase of cytoplasmic Ca2+ and suppression of current in cones from the Zebrafish mutant nof. J Neurosci 23:470–480
Rätscho N, Scholten A, Koch KW (2009) Expression profiles of three novel sensory guanylate cyclases and guanylate cyclase-activating proteins in the zebrafish retina. Biochim Biophys Acta 1793:1110–1114
Imanishi Y, Li N, Sokal I, Sowa ME, Lichtarge O, Wensel TG, Saperstein DA, Baehr W, Palczewski K (2002) Characterization of retinal guanylate cyclase-activating protein 3 (GCAP3) from zebrafish to man. Eur J Neurosci 15:63–78
Takemoto N, Tachibanaki S, Kawamura S (2009) High cGMP synthetic activity in carp cones. Proc Natl Acad Sci USA 106:11788–11793
Schwartz RM, Dayhoff MO (1978) Atlas of protein sequence and structure, vol 5. National Biomedical Research Foundation, Washington, pp 353–358
Duda T, Koch KW, Venkataraman V, Lange C, Beyermann M, Sharma RK (2002) Ca2+-sensor S100β modulated sites of membrane guanylate cyclase in the photoreceptor-bipolar synapse. EMBO J 21:2547–2556
Venkataraman V, Duda T, Ravichandran S, Sharma RK (2008) Neurocalcin δ modulation of ROS-GC1, a new model of Ca2+ signaling. Biochemistry 47:6590–6601
Koch KW (2002) Target recognition of guanylate cyclase by guanylate cyclase-activating proteins. Adv Exp Med Biol 514:349–360
Lange C, Duda T, Beyermann M, Sharma R, Koch KW (1999) Regions in vertebrate photoreceptor guanylyl cyclase ROS-GC1 involved in Ca2+-dependent regulation by guanyly cyclase-activating protein GCAP-1. FEBS Lett 460:27–31
Behnen P, Scholten A, Rätscho N, Koch KW (2009) The cone-specific calcium sensor guanylate cyclase activating protein 4 from the zebrafish retina. J Biol Inorg Chem 14:89–99
Ochocinska MJ, Hitchcock PF (2007) Dynamic expression of the basic helix-loop-helix transcription factor neuroD in the rod and cone photoreceptor lineages in the retina of the embryonic and larval zebrafish. J Comp Neurol 501:1–12
Engeszer RE, Patterson LB, Rao AA, Parichy DM (2007) Zebrafish in the wild: a review of natural history and new notes from the field. Zebrafish 4:21–40
Spence R, Gerlach G, Lawrence C, Smith C (2008) The behaviour and ecology of the zebrafish, Danio rerio. Biol Rev Camb Philos Soc 83:13–34
Cameron DA (2002) Mapping absorbance spectra, cone fractions, and neuronal mechanisms to photopic spectral sensitivity in the zebrafish. Vis Neurosci 19:365–372
Losey GS, Cronin TW, Goldsmith TH, Hyde D, Marshall NJ, McFarland WN (1999) The UV visual world of fishes: a review. J Fish Biol 54:921–943
Chinen A, Matsumoto Y, Kawamura S (2005) Spectral differentiation of blue opsins between phylogenetically close but ecologically distant goldfish and zebrafish. J Biol Chem 280:9460–9466
Woods IG, Kelly PD, Chu F, Ngo-Hazelett P, Yan YN, Huang H, Postlethwait JH, Talbot WS (2000) A comparative map of the zebrafish genome. Genome Res 10:1903–1914
Taylor JS, Braasch I, Frickey T, Meyer A, van de Peer Y (2003) Genome duplication, a trait shared by 22,000 species of ray-finned fish. Genome Res 13:382–390
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Rinner O, Makhankov YV, Biehlmaier O, Neuhauss SCF (2005) Knockdown of cone-specific kinase GRK7 in larval zebrafish leads to impaired cone response recovery and delayed dark adaptation. Neuron 47:231–242
Liu Q, Frey RA, Babb-Clendenon SG, Liu B, Franci J, Wilson AL, Marrs JA, Stenkamp DL (2007) Differential expression of photoreceptor-specific genes in the retina of a zebrafish cadherin2 mutant glass onion and zebrafish cadherin4 morphants. Exp Eye Res 84:163–175
Stearns G, Evangelista M, Fadool JM, Brockerhoff SE (2007) A mutation in the cone-specific pde6 gene causes rapid cone photoreceptor degeneration in zebrafish. J Neurosci 27:13866–13874
Acknowledgment
Experimental work in the laboratory of the corresponding author (K.-W.K.) is supported by a grant from the Deutsche Forschungsgemeinschaft (Ko948/7-1/7-2).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rätscho, N., Scholten, A. & Koch, KW. Diversity of sensory guanylate cyclases in teleost fishes. Mol Cell Biochem 334, 207–214 (2010). https://doi.org/10.1007/s11010-009-0320-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11010-009-0320-1