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Discipline
Biological
Keywords
Retina
Calcium Binding Protein
Bipolar Cells
Zebrafish
Observation Type
Standalone
Nature
Orphan Data
Submitted
Mar 14th, 2016
Published
Apr 27th, 2016
  • Abstract

    Ca2+-binding proteins play important roles in neuronal function by transducing Ca2+ signals and thereby regulating crucial processes like synaptic signaling and neuronal development, growth and survival. The Ca2+-binding protein (CaBP) subfamily is part of the vast EF-hand containing calmodulin superfamily. Eight genes encoding CaBPs have been identified in zebrafish, and many of them are expressed in specific subpopulations of retinal neurons during development. Among them, cabp2a and cabp5b have been shown to be expressed in the retinal inner nuclear layer (INL). Here, we demonstrate that their paralogues, cabp2b and cabp5a, are also specifically expressed in the INL of the developing retina. By extending expression analysis of cabp2a, cabp2b, cabp5a and cabp5b to the adult retina, we reveal exclusive expression of all four genes in the INL after retinal development is completed. Thus, our findings suggest functions of cabp2a, cabp2b, cabp5a and cabp5b in Ca2+ signaling in mature retinal neurons, besides a role in the developing retina.

  • Figure
  • Introduction

    Ca2+ signaling is required for many fundamental aspects of neuronal function, such as signaling at pre- and postsynaptic sites, gene activation, growth, development and survival. Ca2+-binding proteins sense and transduce Ca2+ signals by undergoing conformational changes upon Ca2+ binding, and consequently regulating target proteins. The largest group of Ca2+-binding proteins are structurally conserved EF-hand containing proteins belonging to the calmodulin superfamily. Within this superfamily, the vertebrate-specific CaBP subfamily comprises CaBP1, CaBP2, CaBP4 and CaBP5 in mammals. In zebrafish, the CaBP subfamily is expanded to 8 members encoded by cabp1a, cabp1b, cabp2a, cabp2b, cabp4a, cabp4b, cabp5a and cabp5b, most likely due to duplicate gene retention after teleost-specific whole genome duplication.

    CaBPs are specifically expressed in parts of the nervous system, including the retina. The role of CaBP4 in retinal function is currently best understood. CaBP4, being within the retina specifically expressed in photoreceptors, has an established role in retinal disease and photoreceptor synaptic function. Functions of CaBPs expressed in second-order retinal neurons (i.e. bipolar and horizontal cells) are less well understood. Bipolar cells of the mouse retina have been reported to express CaBP5, and cabp2 transcripts have also been detected in this cell type. Characterization of the CaBP family in zebrafish has revealed two orthologues for each mammalian CaBP-encoding gene, and expression analysis was performed in the developing embryo. Similar to mammals zebrafish cabp4b is expressed in photoreceptors, while no specific expression pattern was detected for cabp4acabp1a and cabp1b are both expressed in amacrine cells. Like the mammalian orthologues, cabp2a and cabp5b are expressed in retinal bipolar cells during development, while cabp2b expression was reported exclusively in hair cells. cabp5a expression has not been detected at these stages.

  • Objective

    Here, we evaluate expression of cabp5a in the developing zebrafish retina and extend expression analysis of cabp2a, cabp2b, cabp5a and cabp5b to the adult retina.

  • Results & Discussion

    In order to study expression of cabp2a, cabp2b, cabp5a and cabp5b in the retina, we performed RNA in situ hybridization on developing whole-mount zebrafish and on adult retinal sections. In 3 day old zebrafish larvae, all four genes studied show clear expression in the retinal inner nuclear layer (INL) (Fig. 1A-D). While staining for cabp2a, cabp5a and cabp5b results in strong labeling of the INL (Fig. 1A,B1,C1,D1), cabp2b staining is only weak in the retina (Fig. 1B1), also when compared to strong cabp2b staining observed in the inner ear (Fig. 1B2). Expression in the inner ear can also be detected for cabp5a and cabp5b (Fig. 1C2,D2). In the adult retina, all four cabps examined show exclusive and strong staining in the INL (Fig. 1G-H). Based on the shape and location of labeled cell bodies, all four genes are expressed in bipolar cells (central and distal INL), and possibly in horizontal cells (distal INL). The proximal INL, harboring amacrine and displaced ganglion cells, is devoid of staining.

    Expression patterns of cabp2a and cabp5b in developing retina and ear are consistent with the findings by Di Donato et al.. While expression of cabp2b has previously been reported only in sensory hair cells, we detected weak expression in the retinal INL, likely reflecting low abundance of cabp2b transcripts in this region. Here, we show for the first time expression of cabp5a expression, which is strongly expressed in the retinal INL and in the inner ear. Our finding that expression of cabp2a, cabp2b, cabp5a and cabp5b is maintained up to adulthood strongly suggests functions in the mature retinal INL.

    So far, no reports on zebrafish CaBP function exist. Studies of CaBP5 in mammalian cell culture and mouse retina suggest an important modulatory role in retinal signaling, possibly by regulation of voltage-gated Ca2+ channels and a function in synaptic vesicle recruitment. Since expression of cabp5 orthologues is conserved between mammals and zebrafish, it is well conceivable that cabp5a and cabp5b have similar tasks.

    The diversity of Ca2+ binding proteins expressed in the nervous system allows finely-tuned Ca2+ signaling through their different Ca2+ affinities, subcellular and cellular localizations and different binding partners, making them non-redundant regulators of neuronal signaling. This and other studies suggest that bipolar cells exploit a repertoire of CaBPs for decoding Ca2+ signals, laying out the framework for further functional studies.

  • Conclusions

    We demonstrate expression of four genes encoding CaBP subfamily members in the retinal INL of zebrafish: cabp2a, cabp2b, cabp5a and cabp5b. Since all four genes are expressed in the INL of both developing and adult zebrafish, our findings suggest functions of cabp2a, cabp2b, cabp5a and cabp5b in Ca2+ signaling in mature retinal neurons, besides possible developmental roles.

  • Limitations

    We show expression that strongly implies, but does not prove, function. The position of the cell bodies in the retina strongly suggests expression in bipolar and horizontal cells, but is not a formal proof.

  • Conjectures

    The study implies a functional of these CaBPs in retinal processing. The obvious next step is to genetically manipulate these genes (e.g. by CRISPR/Cas9 genome editing) and assess altered retinal function in these fish. Due to overlapping expression patterns of paralogues in the INL, it might be necessary to generate double knockouts to observe a phenotype.

  • Methods

    Fish husbandry

    Zebrafish were kept at 26°C under a 14/10 h light/dark cycle as previously described. Embryos were raised at 28°C in E3 medium and staged according to development in days post fertilization. All fish used for this study were from the Tü wildtype strain.

    Generation of DIG labeled RNA probes

    Fragments of cabp2a, cabp2b, cabp5a and cabp5b coding sequence were amplified from cDNA of 5dpf zebrafish by PCR and cloned into the pCRII-TOPO vector. For primer sequences, see supplementary table 1. Identity of the cloned fragments was confirmed and orientation was checked by restriction digestion and sequencing. Plasmids were linearized using appropriate restriction enzymes, and in vitro transcription of antisense and sense RNA probes was performed using the Roche DIG-RNA Labeling Kit (Roche).

    RNA in situ hybridization on whole-mount larvae and adult retinal sections

    For whole mount in situ hybridization, embryos were treated with 3 µM PTU (1-phenyl-2-thiourea, Sigma-Aldrich) to suppress pigmentation. 3 day old larvae were fixed in 4% paraformaldehyde overnight at 4°C. Whole-mount in situ hybridization was carried out as described, with modifications.

    For in situ hybridization on adult retinal sections, zebrafish were euthanized using tricaine (MS-222, Sigma-Aldrich). Eyes were excised and fixed in 4% paraformaldehyde overnight at 4°C. Tissue was washed twice in PBS for 5 min at room temperature, incubated in 30% sucrose overnight at 4°C, embedded in in Richard-Allan Scientific Neg-50 Frozen Section Medium (Thermo Fisher Scientific) and cryosectioned at 16 μm thickness. In situ hybridization on sections was performed as described. Sections were coverslipped with Kaiser’s glycerol gelatin (Merck). Whole-mount and section in situ hybridization experiments were carried out using antisense probes. Control experiments using sense probes resulted in no signal.

    Image acquisition and processing

    Images were acquired on a light microscope (Olympus Bx61) equipped with a Color Camera (ColorViewIII, Soft Imaging System, Olympus). Whole-mount larvae were imaged in the bright field mode, and adult retinal sections in the DIC mode. Images were adjusted for brightness and contrast and figure was composed using Adobe Photoshop.

  • Funding statement

    This work was supported by the Swiss Science Foundation (31003A_153289/1).

  • Acknowledgements

    We thank Ramon Maegert for assistance during an internship, and Kara Dannenhauer and Martin Walther for excellent animal care.

  • Ethics statement

    All experiments were performed in accordance with the ARVO Statement for the Use of Animals in Ophthalmic and Vision Research and were approved by the local authorities (Veterinäramt Zürich TV4206).

  • References
  • 1
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    Matters14/20

    Expression of CaBP transcripts in retinal bipolar cells of developing and adult zebrafish

    Affiliation listing not available.
    Abstractlink

    Ca2+-binding proteins play important roles in neuronal function by transducing Ca2+ signals and thereby regulating crucial processes like synaptic signaling and neuronal development, growth and survival. The Ca2+-binding protein (CaBP) subfamily is part of the vast EF-hand containing calmodulin superfamily. Eight genes encoding CaBPs have been identified in zebrafish, and many of them are expressed in specific subpopulations of retinal neurons during development. Among them, cabp2a and cabp5b have been shown to be expressed in the retinal inner nuclear layer (INL). Here, we demonstrate that their paralogues, cabp2b and cabp5a, are also specifically expressed in the INL of the developing retina. By extending expression analysis of cabp2a, cabp2b, cabp5a and cabp5b to the adult retina, we reveal exclusive expression of all four genes in the INL after retinal development is completed. Thus, our findings suggest functions of cabp2a, cabp2b, cabp5a and cabp5b in Ca2+ signaling in mature retinal neurons, besides a role in the developing retina.

    Figurelink

    Figure 1. Expression patterns of cabp2a, cabp2b, cabp5a and cabp5b analyzed by RNA in situ hybridization.

    (A-D) Expression in 3 day old zebrafish larvae. (A, B1, C1, D1) Within the retina, all four genes are expressed in the inner nuclear layer (INL, arrow heads). Note, strong labeling of the INL by cabp2a, cabp5a and cabp5b in contrast to comparatively weak cabp2b signal. (B2, C2, D2) In addition to the retina, cabp2bcabp5a and cabp5b are also expressed in the inner ear (arrows).

    (E-H) In the adult zebrafish retina, all four genes are exclusively expressed in the INL. While central and distal regions of the INL are labeled, the proximal region remains free from staining. Scale bars correspond 100 µm (D2, applies to A-D) and 50 µm (H, applies to E-H). GCL, ganglion cell layer, INL, inner nuclear layer; Ph, photoreceptor layer.

    Introductionlink

    Ca2+ signaling is required for many fundamental aspects of neuronal function, such as signaling at pre- and postsynaptic sites, gene activation, growth, development and survival[1]. Ca2+-binding proteins sense and transduce Ca2+ signals by undergoing conformational changes upon Ca2+ binding, and consequently regulating target proteins. The largest group of Ca2+-binding proteins are structurally conserved EF-hand containing proteins belonging to the calmodulin superfamily. Within this superfamily, the vertebrate-specific CaBP subfamily comprises CaBP1, CaBP2, CaBP4 and CaBP5 in mammals[2][3][4]. In zebrafish, the CaBP subfamily is expanded to 8 members encoded by cabp1a, cabp1b, cabp2a, cabp2b, cabp4a, cabp4b, cabp5a and cabp5b[5], most likely due to duplicate gene retention after teleost-specific whole genome duplication[6].

    CaBPs are specifically expressed in parts of the nervous system, including the retina[2][5][7]. The role of CaBP4 in retinal function is currently best understood. CaBP4, being within the retina specifically expressed in photoreceptors, has an established role in retinal disease and photoreceptor synaptic function[7][8][9][10][11][12][13][14]. Functions of CaBPs expressed in second-order retinal neurons (i.e. bipolar and horizontal cells) are less well understood[15][16]. Bipolar cells of the mouse retina have been reported to express CaBP5[2], and cabp2 transcripts have also been detected in this cell type[17]. Characterization of the CaBP family in zebrafish has revealed two orthologues for each mammalian CaBP-encoding gene, and expression analysis was performed in the developing embryo[18]. Similar to mammals zebrafish cabp4b is expressed in photoreceptors, while no specific expression pattern was detected for cabp4acabp1a and cabp1b are both expressed in amacrine cells. Like the mammalian orthologues, cabp2a and cabp5b are expressed in retinal bipolar cells during development, while cabp2b expression was reported exclusively in hair cells. cabp5a expression has not been detected at these stages[5].

    Objectivelink

    Here, we evaluate expression of cabp5a in the developing zebrafish retina and extend expression analysis of cabp2a, cabp2b, cabp5a and cabp5b to the adult retina.

    Results & Discussionlink

    In order to study expression of cabp2a, cabp2b, cabp5a and cabp5b in the retina, we performed RNA in situ hybridization on developing whole-mount zebrafish and on adult retinal sections. In 3 day old zebrafish larvae, all four genes studied show clear expression in the retinal inner nuclear layer (INL) (Fig. 1A-D). While staining for cabp2a, cabp5a and cabp5b results in strong labeling of the INL (Fig. 1A,B1,C1,D1), cabp2b staining is only weak in the retina (Fig. 1B1), also when compared to strong cabp2b staining observed in the inner ear (Fig. 1B2). Expression in the inner ear can also be detected for cabp5a and cabp5b (Fig. 1C2,D2). In the adult retina, all four cabps examined show exclusive and strong staining in the INL (Fig. 1G-H). Based on the shape and location of labeled cell bodies, all four genes are expressed in bipolar cells (central and distal INL), and possibly in horizontal cells (distal INL). The proximal INL, harboring amacrine and displaced ganglion cells, is devoid of staining.

    Expression patterns of cabp2a and cabp5b in developing retina and ear are consistent with the findings by Di Donato et al.[5]. While expression of cabp2b has previously been reported only in sensory hair cells, we detected weak expression in the retinal INL, likely reflecting low abundance of cabp2b transcripts in this region. Here, we show for the first time expression of cabp5a expression, which is strongly expressed in the retinal INL and in the inner ear. Our finding that expression of cabp2a, cabp2b, cabp5a and cabp5b is maintained up to adulthood strongly suggests functions in the mature retinal INL.

    So far, no reports on zebrafish CaBP function exist. Studies of CaBP5 in mammalian cell culture and mouse retina suggest an important modulatory role in retinal signaling[16], possibly by regulation of voltage-gated Ca2+ channels[17] and a function in synaptic vesicle recruitment[18]. Since expression of cabp5 orthologues is conserved between mammals and zebrafish, it is well conceivable that cabp5a and cabp5b have similar tasks.

    The diversity of Ca2+ binding proteins expressed in the nervous system allows finely-tuned Ca2+ signaling through their different Ca2+ affinities, subcellular and cellular localizations and different binding partners, making them non-redundant regulators of neuronal signaling[1]. This and other studies[2][5][15] suggest that bipolar cells exploit a repertoire of CaBPs for decoding Ca2+ signals, laying out the framework for further functional studies.

    Conclusionslink

    We demonstrate expression of four genes encoding CaBP subfamily members in the retinal INL of zebrafish: cabp2a, cabp2b, cabp5a and cabp5b. Since all four genes are expressed in the INL of both developing and adult zebrafish, our findings suggest functions of cabp2a, cabp2b, cabp5a and cabp5b in Ca2+ signaling in mature retinal neurons, besides possible developmental roles.

    Limitationslink

    We show expression that strongly implies, but does not prove, function. The position of the cell bodies in the retina strongly suggests expression in bipolar and horizontal cells, but is not a formal proof.

    Conjectureslink

    The study implies a functional of these CaBPs in retinal processing. The obvious next step is to genetically manipulate these genes (e.g. by CRISPR/Cas9 genome editing) and assess altered retinal function in these fish. Due to overlapping expression patterns of paralogues in the INL, it might be necessary to generate double knockouts to observe a phenotype.

    Methodslink

    Fish husbandry

    Zebrafish were kept at 26°C under a 14/10 h light/dark cycle as previously described[19]. Embryos were raised at 28°C in E3 medium and staged according to development in days post fertilization[20]. All fish used for this study were from the Tü wildtype strain.

    Generation of DIG labeled RNA probes

    Fragments of cabp2a, cabp2b, cabp5a and cabp5b coding sequence were amplified from cDNA of 5dpf zebrafish by PCR and cloned into the pCRII-TOPO vector. For primer sequences, see supplementary table 1. Identity of the cloned fragments was confirmed and orientation was checked by restriction digestion and sequencing. Plasmids were linearized using appropriate restriction enzymes, and in vitro transcription of antisense and sense RNA probes was performed using the Roche DIG-RNA Labeling Kit (Roche).

    RNA in situ hybridization on whole-mount larvae and adult retinal sections

    For whole mount in situ hybridization, embryos were treated with 3 µM PTU (1-phenyl-2-thiourea, Sigma-Aldrich) to suppress pigmentation. 3 day old larvae were fixed in 4% paraformaldehyde overnight at 4°C. Whole-mount in situ hybridization was carried out as described[21], with modifications[22].

    For in situ hybridization on adult retinal sections, zebrafish were euthanized using tricaine (MS-222, Sigma-Aldrich). Eyes were excised and fixed in 4% paraformaldehyde overnight at 4°C. Tissue was washed twice in PBS for 5 min at room temperature, incubated in 30% sucrose overnight at 4°C, embedded in in Richard-Allan Scientific Neg-50 Frozen Section Medium (Thermo Fisher Scientific) and cryosectioned at 16 μm thickness. In situ hybridization on sections was performed as described[22]. Sections were coverslipped with Kaiser’s glycerol gelatin (Merck). Whole-mount and section in situ hybridization experiments were carried out using antisense probes. Control experiments using sense probes resulted in no signal.

    Image acquisition and processing

    Images were acquired on a light microscope (Olympus Bx61) equipped with a Color Camera (ColorViewIII, Soft Imaging System, Olympus). Whole-mount larvae were imaged in the bright field mode, and adult retinal sections in the DIC mode. Images were adjusted for brightness and contrast and figure was composed using Adobe Photoshop.

    Funding Statementlink

    This work was supported by the Swiss Science Foundation (31003A_153289/1).

    Acknowledgementslink

    We thank Ramon Maegert for assistance during an internship, and Kara Dannenhauer and Martin Walther for excellent animal care.

    Conflict of interestlink

    The authors declare no conflicts of interest.

    Ethics Statementlink

    All experiments were performed in accordance with the ARVO Statement for the Use of Animals in Ophthalmic and Vision Research and were approved by the local authorities (Veterinäramt Zürich TV4206).

    No fraudulence is committed in performing these experiments or during processing of the data. We understand that in the case of fraudulence, the study can be retracted by ScienceMatters.

    Referenceslink
    1. Robert D. Burgoyne
      Neuronal calcium sensor proteins: generating diversity in neuronal Ca2⁺ signalling
      Nature Reviews Neuroscience, 8/2007, pages 182-193 DOI: 10.1038/nrn2093chrome_reader_mode
    2. F. Haeseleer, I. Sokal, C. L. M. J. Verlinde,more_horiz, K. Palczewski
      Five Members of a Novel Ca2⁺-binding Protein (CABP) Subfamily with Similarity to Calmodulin
      Journal of Biological Chemistry, 275/2000, pages 1247-1260 DOI: 10.1074/jbc.275.2.1247chrome_reader_mode
    3. Hannah V McCue, Lee P Haynes, Robert D Burgoyne
      Bioinformatic analysis of CaBP/calneuron proteins reveals a family of highly conserved vertebrate Ca2⁺-binding proteins
      BMC Research Notes, 3/2010, page 118 DOI: 10.1186/1756-0500-3-118chrome_reader_mode
    4. Lee P. Haynes, Hannah V. McCue, Robert D. Burgoyne
      Evolution and functional diversity of the Calcium Binding Proteins (CaBPs)
      Frontiers in Molecular Neuroscience, 5/2012, page 9 DOI: 10.3389/fnmol.2012.00009chrome_reader_mode
    5. Vincenzo Di Donato, Thomas O. Auer, Karine Duroure, Filippo Del Bene
      Characterization of the Calcium Binding Protein Family in Zebrafish
    6. Stella M. K. Glasauer, Stephan C. F. Neuhauss
      Whole-genome duplication in teleost fishes and its evolutionary consequences
      Molecular Genetics and Genomics, 289/2014, pages 1045-1060 DOI: 10.1007/s00438-014-0889-2chrome_reader_mode
    7. Françoise Haeseleer, Yoshikazu Imanishi, Tadao Maeda,more_horiz, Krzysztof Palczewski
      Essential role of Ca2⁺-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function
      Nature Neuroscience, 7/2004, pages 1079-1087 DOI: 10.1038/nn1320chrome_reader_mode
    8. Tadao Maeda, Janis Lem, Krzysztof Palczewski, Françoise Haeseleer
      A Critical Role of CaBP4 in the Cone Synapse
      Investigative Opthalmology & Visual Science, 46/2005, pages 4320-4327 DOI: 10.1167/iovs.05-0478chrome_reader_mode
    9. Christina Zeitz, Barbara Kloeckener-Gruissem, Ursula Forster,more_horiz, Wolfgang Berger
      Mutations in CABP4, the Gene Encoding the Ca2⁺-Binding Protein 4, Cause Autosomal Recessive Night Blindness
      The American Journal of Human Genetics, 79/2006, pages 657-667 DOI: 10.1086/508067chrome_reader_mode
    10. Karin W. Littink, Maria M. van Genderen, Rob W. J. Collin,more_horiz, L. Ingeborgh van Den Born
      A Novel Homozygous Nonsense Mutation in CABP4 Causes Congenital Cone–Rod Synaptic Disorder
      Investigative Opthalmology & Visual Science, 50/2009, page 2344 DOI: 10.1167/iovs.08-2553chrome_reader_mode
    11. Mohammed A. Aldahmesh, Mohammed Al-Owain, Faisal Alqahtani,more_horiz, Fowzan S. Alkuraya
      A null mutation in CABP4 causes Leber’s congenital amaurosis-like phenotype
      Molecular Vision, 16/2010, page 207–212 chrome_reader_mode
    12. L. Shaltiel, C. Paparizos, S. Fenske,more_horiz, C. A. Wahl-Schott
      Complex Regulation of Voltage-dependent Activation and Inactivation Properties of Retinal Voltage-gated Cav1.4 L-type Ca2⁺ Channels by Ca2⁺-binding Protein 4 (CaBP4)
      Journal of Biological Chemistry, 287/2012, pages 36312-36321 DOI: 10.1074/jbc.m112.392811chrome_reader_mode
    13. Xiaoni Liu, Vasily Kerov, Françoise Haeseleer,more_horiz, Amy Lee
      Dysregulation of Ca v 1.4 channels disrupts the maturation of photoreceptor synaptic ribbons in congenital stationary night blindness type 2
      Channels, 7/2013, pages 514-523 DOI: 10.4161/chan.26376chrome_reader_mode
    14. Arif O. Khan
      CABP4 Mutations Do Not Cause Congenital Stationary Night Blindness
      Ophthalmology, 121/2014, page e15 DOI: 10.1016/j.ophtha.2013.11.005chrome_reader_mode
    15. Fred Rieke, Amy Lee, Françoise Haeseleer
      Characterization of Ca2+-Binding Protein 5 Knockout Mouse Retina
      Investigative Opthalmology & Visual Science, 49/2008, pages 5126-5135 DOI: 10.1167/iovs.08-2236chrome_reader_mode
    16. Izabela Sokal, Françoise Haeseleer
      Insight into the Role of Ca2+-Binding Protein 5 in Vesicle Exocytosis
      Investigative Opthalmology & Visual Science, 52/2011, page 9131 DOI: 10.1167/iovs.11-8246chrome_reader_mode
    17. Y. Nakajima, M. Moriyama, M. Hattori,more_horiz, S. Nakanishi
      Isolation of ON Bipolar Cell Genes via hrGFP-coupled Cell Enrichment Using the mGluR6 Promoter
      Journal of Biochemistry, 145/2009, pages 811-818 DOI: 10.1093/jb/mvp038chrome_reader_mode
    18. Vincenzo Di Donato, Thomas O. Auer, Karine Duroure, Filippo Del Bene,
      Characterization of the Calcium Binding Protein Family in Zebrafish
    19. Guiying Cui, Alexander C. Meyer, Irina Calin-Jageman,more_horiz, Amy Lee
      Ca 2⁺ -binding proteins tune Ca 2⁺ -feedback to Ca v 1.3 channels in mouse auditory hair cells
      The Journal of Physiology, 585/2007, pages 791-803 DOI: 10.1113/jphysiol.2007.142307chrome_reader_mode
    20. Mary C. Mullins, Matthias Hammerschmidt, Pascal Haffter, Christiane Nüsslein-Volhard
      Large-scale mutagenesis in the zebrafish: in search of genes controlling development in a vertebrate
      Current Biology, 4/1994, pages 189-202 DOI: 10.1016/s0960-9822(00)00048-8chrome_reader_mode
    21. Charles B. Kimmel, William W. Ballard, Seth R. Kimmel,more_horiz, Thomas F. Schilling
      Stages of embryonic development of the zebrafish
      Developmental Dynamics, 203/1995, pages 253-310 DOI: 10.1002/aja.1002030302chrome_reader_mode
    22. Christine Thisse, Bernard Thisse
      High-resolution in situ hybridization to whole-mount zebrafish embryos
      Nature Protocols, 3/2008, pages 59-69 DOI: 10.1038/nprot.2007.514chrome_reader_mode
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