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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)

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Abstract

The guanylate cyclase-activating proteins (GCAPs) are Ca2+-binding proteins of the calmodulin (CaM) gene superfamily that function in the regulation of photoreceptor guanylate cyclases (GCs). In the mammalian retina, two GCAPs (GCAP 1-2) and two transmembrane GCs have been identified as part of a complex regulatory system responsive to fluctuating levels of free Ca2+. A third GCAP, GCAP3, is expressed in human and zebrafish (Danio rerio) retinas, and a guanylate cyclase-inhibitory protein (GCIP) has been shown to be present in frog cones. To explore the diversity of GCAPs in more detail, we searched the pufferfish (Fugu rubripes) and zebrafish (Danio rerio) genomes for GCAP-related gene sequences (fuGCAPs and zGCAPs, respectively) and found that at least five additional GCAPs (GCAP4-8) are predicted to be present in these species. We identified genomic contigs encoding fuGCAPl-8, fuGCIP, zGCAPl-5, zGCAP7 and zGCIP. We describe cloning, expression and localization of three novel GCAPs present in the zebrafish retina (zGCAP4, zGCAP5, and zGCAP7). The results show that recombinant zGCAP4 stimulated bovine rod outer segment GC in a Ca2+-dependent manner. RT-PCR with zGCAP specific primers showed specific expression of zGCAPs and zGCIP in the retina, while zGCAPl mRNA is also present in the brain. In situ hybridization with anti-sense zGCAP4, zGCAP5 and zGCAP7 RNA showed exclusive expression in zebrafish cone photoreceptors. The presence of at least eight GCAP genes suggests an unexpected diversity within this subfamily of Ca2+-binding proteins in the teleost retina, and suggests additional functions for GCAPs apart from stimulation of GC. Based on genome searches and EST analyses, the mouse and human genomes do not harbor GCAP4-8 or GCIP genes.

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Acknowledgments

We would like to thank Darin Bronson for expert technical assistance with this project. This research was supported by grants from the NIH (EY08123, to W.B., and EY08061, to K.P.), the Ruth and Milton Steinbach Fund, the E.k. Bishop Foundation, the Alcon Research Institute, and Research to Prevent Blindness, Inc. (RPB), to the Departments of Ophthalmology at the University of Washington and the University of Utah, and a Center Grant from Foundation Fighting Blindness, Inc., to the University of Utah. W.B. and K.P. are recipients of an RPB Senior Investigator Award. W.B. acknowledges an endowment from Ralph and Mary Tuck to the Department of Ophthalmology at the University of Utah.

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Authors and Affiliations

  1. Department of Ophthalmology, University of Washington, Seattle, WA, 98195, USA

    Yoshikazu Imanishi, Izabela Sokal & Krzysztof Palczewski

  2. Department of Biology, University of Utah, Salt Lake City, UT, 84112, USA

    Lili Yang & Wolfgang Baehr

  3. International Institute of Molecular and Cell Biology, Warsaw, PL, 02109, Poland

    Sławomir Filipek

  4. Department of Pharmacology, University of Washington, Seattle, WA, 98195, USA

    Krzysztof Palczewski

  5. Department of Chemistry, University of Washington, Seattle, WA, 98195, USA

    Krzysztof Palczewski

  6. Department of Ophthalmology, University of Utah, Salt Lake City, UT, 84112, USA

    Wolfgang Baehr

  7. Department of Neurobiology and Anatomy, University of Utah, Salt Lake City, UT, 84112, USA

    Wolfgang Baehr

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  1. Yoshikazu Imanishi
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  2. Lili Yang
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  3. Izabela Sokal
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  4. Sławomir Filipek
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  5. Krzysztof Palczewski
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Correspondence to Krzysztof Palczewski or Wolfgang Baehr.

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(Yoshikazu Imanishi and Lili Yang)These authors contributed equally.

[Reviewing Editor: Martin Kreitman]

Abbreviations Used: CaM, calmodulin; DC, double cones; EST, expressed sequence tag; GC, guanylate cyclase; GCAP, GC-activating protein; fuGCAP, fugu GCAP; zGCAP, zebrafish GCAP; GCIP, GC-inhibitory protein; LS, long single cones; NCBP, neuronal Ca2+-binding protein; PAGE, polyacrylamide gel electrophoresis; PB, phosphate buffer; PBS, phosphate-buffered saline; PBST, phosphate-buffered saline with 0.1% Triton X-100; TBST, Tris-buffered saline with 0.1% Tween 20; PCR, polymerase chain reaction; ROS, rod outer segments; SS, short single cones; SDS, sodium dodecyl sulfate; PVDF, polyvinylidene difluoride; RT, reverse transcriptase; NJ, neighbor joining; ORF, open reading frame

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Imanishi, Y., Yang, L., Sokal, I. et al. 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 (2004). https://doi.org/10.1007/s00239-004-2614-y

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