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Molecular and Cellular Biochemistry

, Volume 334, Issue 1–2, pp 207–214 | Cite as

Diversity of sensory guanylate cyclases in teleost fishes

  • Nina Rätscho
  • Alexander Scholten
  • Karl-Wilhelm Koch
Article

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.

Keywords

Guanylate cyclase Zebrafish Retina Cone vision 

Notes

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).

References

  1. 1.
    Sharma RK (2002) Evolution of the membrane guanylate cyclase transduction system. Mol Cell Biochem 230:3–30CrossRefPubMedGoogle Scholar
  2. 2.
    Baker DA, Kelly JM (2004) Structure, function and evolution of microbial adenylyl and guanylyl cyclases. Mol Microbiol 52:1229–1242CrossRefPubMedGoogle Scholar
  3. 3.
    Fitzpatrick DA, O’Halloran DM, Burnell AM (2006) Multiple lineage specific expansions within the guanylyl cyclase gene family. BMC Evol Biol 6:26CrossRefPubMedGoogle Scholar
  4. 4.
    Linder JU, Schultz JE (2002) Guanylyl cyclases in unicellular organisms. Mol Cell Biochem 230:149–158CrossRefPubMedGoogle Scholar
  5. 5.
    Russwurm M, Koesling D (2002) Isoforms of NO-sensitive guanylyl cyclase. Mol Cell Biochem 230:159–164CrossRefPubMedGoogle Scholar
  6. 6.
    Bellamy TC, Garthwaite J (2002) The receptor-like properties of nitric oxide-activated soluble guanylyl cyclase in intact cells. Mol Cell Biochem 230:165–176CrossRefPubMedGoogle Scholar
  7. 7.
    Tamura N, Chrisman TD, Garbers DL (2001) The regulation, physiological roles of the guanylyl cyclase receptors. Endocr J 48:611–634CrossRefPubMedGoogle Scholar
  8. 8.
    Koch KW, Duda T, Sharma RK (2002) Photoreceptor specific guanylate cyclases in vertebrate phototransduction. Mol Cell Biochem 230:97–106CrossRefPubMedGoogle Scholar
  9. 9.
    Koch K-W, Stryer L (1988) Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature 334:64–66CrossRefPubMedGoogle Scholar
  10. 10.
    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 12:1345–1352CrossRefPubMedGoogle Scholar
  11. 11.
    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 91:4014–4018CrossRefPubMedGoogle Scholar
  12. 12.
    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 13:395–404CrossRefPubMedGoogle Scholar
  13. 13.
    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 270:25200–25206CrossRefPubMedGoogle Scholar
  14. 14.
    Gorczyca WA, Polans AS, Surgucheva IG, Subbaraya I, Baehr W, Palczewski K (1995) Guanylyl cyclase activating protein. J Biol Chem 270:22029–22036CrossRefPubMedGoogle Scholar
  15. 15.
    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 271:8022–8027CrossRefPubMedGoogle Scholar
  16. 16.
    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 98:9948–9953CrossRefPubMedGoogle Scholar
  17. 17.
    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 21:1545–1554CrossRefPubMedGoogle Scholar
  18. 18.
    Burns ME, Mendez A, Chen J, Baylor DA (2002) Dynamics of cyclic GMP synthesis in retinal rods. Neuron 36:81–91CrossRefPubMedGoogle Scholar
  19. 19.
    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 283:29135–29143CrossRefPubMedGoogle Scholar
  20. 20.
    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 19:5889–5897PubMedGoogle Scholar
  21. 21.
    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 282:8837–8847CrossRefPubMedGoogle Scholar
  22. 22.
    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 94:3388–3395CrossRefPubMedGoogle Scholar
  23. 23.
    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 97:10595–10600CrossRefPubMedGoogle Scholar
  24. 24.
    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 104:14507–14512CrossRefPubMedGoogle Scholar
  25. 25.
    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 40:12067–12077CrossRefPubMedGoogle Scholar
  26. 26.
    Chinen A, Hamaoka T, Yamada Y, Kawamura S (2003) Gene duplication and spectral diversification of cone visual pigments of zebrafish. Genetics 163:663–675PubMedGoogle Scholar
  27. 27.
    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 208:1337–1345CrossRefPubMedGoogle Scholar
  28. 28.
    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 92:10545–10549CrossRefPubMedGoogle Scholar
  29. 29.
    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 19:8603–8615PubMedGoogle Scholar
  30. 30.
    Bilotta J, Saszik S (2001) The zebrafish as a model visual system. Int J Dev Neurosci 19:621–629CrossRefPubMedGoogle Scholar
  31. 31.
    Rinner O, Rick JM, Neuhauss SCF (2005) Contrast sensitivity, spatial and temporal tuning of the larval zebrafish optokinetic response. Invest Ophthalmol Vis Sci 46:137–142CrossRefPubMedGoogle Scholar
  32. 32.
    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 272:23407–23417CrossRefPubMedGoogle Scholar
  33. 33.
    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 255:216–220CrossRefGoogle Scholar
  34. 34.
    Kusakabe T, Suzuke N (2000) Photoreceptors and olfactory cells express the same retinal guanyly cyclase isoform in medaka: visualization by promote transgenics. FEBS Lett 483:143–148CrossRefPubMedGoogle Scholar
  35. 35.
    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 20:133–140CrossRefPubMedGoogle Scholar
  36. 36.
    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 22:819–835CrossRefPubMedGoogle Scholar
  37. 37.
    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 59:204–217CrossRefPubMedGoogle Scholar
  38. 38.
    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 23:470–480PubMedGoogle Scholar
  39. 39.
    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 1793:1110–1114CrossRefPubMedGoogle Scholar
  40. 40.
    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 15:63–78CrossRefPubMedGoogle Scholar
  41. 41.
    Takemoto N, Tachibanaki S, Kawamura S (2009) High cGMP synthetic activity in carp cones. Proc Natl Acad Sci USA 106:11788–11793CrossRefPubMedGoogle Scholar
  42. 42.
    Schwartz RM, Dayhoff MO (1978) Atlas of protein sequence and structure, vol 5. National Biomedical Research Foundation, Washington, pp 353–358Google Scholar
  43. 43.
    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 21:2547–2556CrossRefPubMedGoogle Scholar
  44. 44.
    Venkataraman V, Duda T, Ravichandran S, Sharma RK (2008) Neurocalcin δ modulation of ROS-GC1, a new model of Ca2+ signaling. Biochemistry 47:6590–6601CrossRefGoogle Scholar
  45. 45.
    Koch KW (2002) Target recognition of guanylate cyclase by guanylate cyclase-activating proteins. Adv Exp Med Biol 514:349–360PubMedGoogle Scholar
  46. 46.
    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 460:27–31CrossRefPubMedGoogle Scholar
  47. 47.
    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 14:89–99CrossRefPubMedGoogle Scholar
  48. 48.
    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 501:1–12CrossRefPubMedGoogle Scholar
  49. 49.
    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 4:21–40CrossRefPubMedGoogle Scholar
  50. 50.
    Spence R, Gerlach G, Lawrence C, Smith C (2008) The behaviour and ecology of the zebrafish, Danio rerio. Biol Rev Camb Philos Soc 83:13–34PubMedGoogle Scholar
  51. 51.
    Cameron DA (2002) Mapping absorbance spectra, cone fractions, and neuronal mechanisms to photopic spectral sensitivity in the zebrafish. Vis Neurosci 19:365–372CrossRefPubMedGoogle Scholar
  52. 52.
    Losey GS, Cronin TW, Goldsmith TH, Hyde D, Marshall NJ, McFarland WN (1999) The UV visual world of fishes: a review. J Fish Biol 54:921–943CrossRefGoogle Scholar
  53. 53.
    Chinen A, Matsumoto Y, Kawamura S (2005) Spectral differentiation of blue opsins between phylogenetically close but ecologically distant goldfish and zebrafish. J Biol Chem 280:9460–9466CrossRefPubMedGoogle Scholar
  54. 54.
    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 10:1903–1914CrossRefPubMedGoogle Scholar
  55. 55.
    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 13:382–390CrossRefPubMedGoogle Scholar
  56. 56.
    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 22:4673–4680CrossRefPubMedGoogle Scholar
  57. 57.
    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 47:231–242CrossRefPubMedGoogle Scholar
  58. 58.
    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 84:163–175CrossRefPubMedGoogle Scholar
  59. 59.
    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 27:13866–13874CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2009

Authors and Affiliations

  • Nina Rätscho
    • 1
  • Alexander Scholten
    • 1
  • Karl-Wilhelm Koch
    • 1
  1. 1.Biochemistry Group, Institute of Biology and Environmental Science, Faculty VCarl von Ossietzky University OldenburgOldenburgGermany

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