Calcium Channel-Dependent Molecular Maturation of Photoreceptor Synapses
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{"title"=>"Calcium Channel-Dependent Molecular Maturation of Photoreceptor Synapses", "type"=>"journal", "authors"=>[{"first_name"=>"Nawal", "last_name"=>"Zabouri", "scopus_author_id"=>"15825715100"}, {"first_name"=>"Silke", "last_name"=>"Haverkamp", "scopus_author_id"=>"6603883197"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"368900176", "sgr"=>"84877674003", "pmid"=>"23675510", "scopus"=>"2-s2.0-84877674003", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "doi"=>"10.1371/journal.pone.0063853", "issn"=>"19326203"}, "id"=>"4b9e922b-d293-366d-a291-ace893742d49", "abstract"=>"Several studies have shown the importance of calcium channels in the development and/or maturation of synapses. The Ca(V)1.4(α(1F)) knockout mouse is a unique model to study the role of calcium channels in photoreceptor synapse formation. It features abnormal ribbon synapses and aberrant cone morphology. We investigated the expression and targeting of several key elements of ribbon synapses and analyzed the cone morphology in the Ca(V)1.4(α(1F)) knockout retina. Our data demonstrate that most abnormalities occur after eye opening. Indeed, scaffolding proteins such as Bassoon and RIM2 are properly targeted at first, but their expression and localization are not maintained in adulthood. This indicates that either calcium or the Ca(V)1.4 channel, or both are necessary for the maintenance of their normal expression and distribution in photoreceptors. Other proteins, such as Veli3 and PSD-95, also display abnormal expression in rods prior to eye opening. Conversely, vesicle related proteins appear normal. Our data demonstrate that the Ca(V)1.4 channel is important for maintaining scaffolding proteins in the ribbon synapse but less vital for proteins related to vesicular release. This study also confirms that in adult retinae, cones show developmental features such as sprouting and synaptogenesis. Overall we present evidence that in the absence of the Ca(V)1.4 channel, photoreceptor synapses remain immature and are unable to stabilize.", "link"=>"http://www.mendeley.com/research/calcium-channeldependent-molecular-maturation-photoreceptor-synapses", "reader_count"=>29, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>8, "Student > Ph. D. Student"=>8, "Student > Master"=>9, "Other"=>1, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>8, "Student > Ph. D. Student"=>8, "Student > Master"=>9, "Other"=>1, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>17, "Medicine and Dentistry"=>2, "Neuroscience"=>4, "Veterinary Science and Veterinary Medicine"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Neuroscience"=>{"Neuroscience"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>17}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Germany"=>1}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1556037"], "description"=>"<p>(<b>A–F</b>) Vertical sections from WT (<b>A, F</b>) and Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO (<b>B–E</b>) at different ages. S-opsin labeling shows the morphology of cones in Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO at P13 (<b>B</b>), P15 (<b>C</b>), P18 (<b>D</b>) and P23 (<b>E</b>), and in WT at P13 (<b>A</b>) and P23 (<b>F</b>). Arrowheads indicate the various cone branches and synapse-like terminals. Scale bar = 5 µm.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Neurological system", "neuroanatomy", "synapses", "neuroscience", "Developmental neuroscience", "ophthalmology", "Retinal disorders"], "article_id"=>1075707, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Nawal Zabouri", "Silke Haverkamp"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063853.g008", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cones_in_Ca_V_1_4_945_1F_KO_at_different_ages_/1075707", "title"=>"Cones in Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO at different ages.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-13 10:36:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1555927"], "description"=>"<p>In photoreceptor synapses, proteins are divided in several compartments: the ribbon associated proteins are shown in red, the active zone associated proteins in blue, and vesicle associated proteins in green. Additional proteins are important for synaptic functions and some of these proteins are presented in grey.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Neurological system", "neuroanatomy", "synapses", "neuroscience", "Developmental neuroscience", "ophthalmology", "Retinal disorders", "proteins", "investigated"], "article_id"=>1075596, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Nawal Zabouri", "Silke Haverkamp"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063853.g001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Synaptic_proteins_investigated_in_the_Ca_V_1_4_945_1F_KO_/1075596", "title"=>"Synaptic proteins investigated in the Ca<sub>V</sub>1.4(α<sub>1F</sub>)-KO.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-13 10:36:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1555935"], "description"=>"<p>Photoreceptor terminals are visualized with complexin 4 (Cplx4). <b>A–J</b>: Vertical sections from P9-WT (<b>A</b>), P9-KO (<b>B</b>), P11-KO (<b>C</b>), P13-KO (<b>D</b>), P15-KO (<b>E</b>), P18-KO (<b>F</b>), P23-KO (<b>G</b>), P25-KO (<b>H</b>), P30-KO (<b>I</b>) and P30-WT (<b>J</b>) mouse retinae. At all ages, ectopic terminals are distinguishable as indicated with white arrowheads. Scale bar = 5 µm.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Neurological system", "neuroanatomy", "synapses", "neuroscience", "Developmental neuroscience", "ophthalmology", "Retinal disorders", "photoreceptor", "terminals", "ages"], "article_id"=>1075605, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Nawal Zabouri", "Silke Haverkamp"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063853.g002", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_photoreceptor_terminals_at_different_ages_in_the_Ca_V_1_4_945_1F_KO_/1075605", "title"=>"Distribution of photoreceptor terminals at different ages in the Ca<sub>V</sub>1.4(α<sub>1F</sub>)-KO.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-13 10:36:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1556014"], "description"=>"<p>(<b>A–I</b>) Vertical sections from P13-KO (<b>A, D and G</b>), P25-KO (<b>B, E and H</b>), and P25-WT (<b>C, F and I</b>). Confocal micrographs of retinae immunolabeled for vGluT 1 (<b>A–C</b>), VAMP2. (<b>D–F</b>) and synaptophysin (<b>G–I</b>). Scale bar = 5 µm.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Neurological system", "neuroanatomy", "synapses", "neuroscience", "Developmental neuroscience", "ophthalmology", "Retinal disorders", "vesicular"], "article_id"=>1075686, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Nawal Zabouri", "Silke Haverkamp"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063853.g006", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_vesicular_proteins_/1075686", "title"=>"Expression of vesicular proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-13 10:36:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1555949"], "description"=>"<p>(<b>A–F</b>) Vertical sections from P15 (<b>A, B</b>), P25 (<b>C, D</b>) and P30 (<b>E–F</b>) mouse Ca<sub>V</sub>1.4(α<sub>1F</sub>)-KO retinae. (<b>A–F</b>) Confocal micrographs of retinae co-immunolabeled for complexin 4 (Cplx4) and C-terminal binding protein 2 (CtBP2). CtBP2 is presented alone in grayscale in the top row, the CtBP2 (magenta) and Cplx4 (green) signals are presented merged in the bottom row. Potentially quickly retracting isolated terminals that are Cplx4-positive/CtBP2-positive are indicated by white arrows, new or degenerating terminals that are Cplx4-positive/CtBP2-negative are indicated by grey arrows (see text for explanation). Scale bar = 5 µm.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Neurological system", "neuroanatomy", "synapses", "neuroscience", "Developmental neuroscience", "ophthalmology", "Retinal disorders", "terminals"], "article_id"=>1075619, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Nawal Zabouri", "Silke Haverkamp"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063853.g003", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Some_isolated_terminals_are_new_terminals_in_Ca_V_1_4_945_1F_KO_retinae_/1075619", "title"=>"Some isolated terminals are new terminals in Ca<sub>V</sub>1.4(α<sub>1F</sub>)-KO retinae.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-13 10:36:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1556025"], "description"=>"<p>(<b>A–E</b>) Vertical sections from P46 Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO (<b>A, C, E</b>) and P46-WT (<b>B,D</b>). <b>A</b>: S-opsin labeling shows the morphology of cones in Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO. Arrowheads indicate the various cone branches and synapse-like terminals. The expression of two cone markers, PNA (<b>B–C</b>) and mCar (<b>D–E</b>) is presented in <b>B–E</b>. Arrowheads indicate the immunopositive outer segments of cones in both WT and Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO. (<b>F–K</b>) Glycogen phosphorylase (glypho) immunoreactivity shows the overall cone population in the dorsal (<b>F–H</b>) and ventral (<b>I–K</b>) retina of WT at 6 months (<b>F, I</b>) and of Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO at 6 months (<b>G, J)</b> and 10 months(<b>H, K</b>). Scale bars = 10 µm.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Neurological system", "neuroanatomy", "synapses", "neuroscience", "Developmental neuroscience", "ophthalmology", "Retinal disorders", "cones"], "article_id"=>1075695, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Nawal Zabouri", "Silke Haverkamp"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063853.g007", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mature_cones_in_Ca_V_1_4_945_1F_KO_/1075695", "title"=>"Mature cones in Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-13 10:36:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1556071"], "description"=>"<p>Antibodies.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Neurological system", "neuroanatomy", "synapses", "neuroscience", "Developmental neuroscience", "ophthalmology", "Retinal disorders"], "article_id"=>1075741, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Nawal Zabouri", "Silke Haverkamp"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063853.t001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Antibodies_/1075741", "title"=>"Antibodies.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-05-13 10:36:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1556070"], "description"=>"<p>Several protein–protein interactions are affected such as the association of Ribeye, Piccolo and Bassoon. The investigated proteins in the model are depicted with a red outline. The proteins with an abnormal expression and/or distribution are shown in grey. Synaptic ribbons form a complex with several other proteins such as CAST, RIM2, Rab3a, and Munc13. In the Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO, RIM2 expression is compromised. The vesicle related machinery (VAMP2, synaptophysin and complexin 3 and 4) is not affected in the Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO. Other presynaptic proteins such PMCA, PSD-95 and Veli3 are also affected in the Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO. Furthermore, β-Dystroglycan, a protein necessary for the invagination of bipolar cells is absent from the photoreceptor synapses in the Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Neurological system", "neuroanatomy", "synapses", "neuroscience", "Developmental neuroscience", "ophthalmology", "Retinal disorders", "elements", "affected", "photoreceptor", "terminals"], "article_id"=>1075740, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Nawal Zabouri", "Silke Haverkamp"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063853.g010", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_the_elements_affected_in_the_photoreceptor_terminals_in_the_Ca_V_1_4_945_1F_KO_/1075740", "title"=>"Summary of the elements affected in the photoreceptor terminals in the Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-13 10:36:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1556001"], "description"=>"<p>(<b>A–L</b>) Vertical sections from P13-WT (<b>A, E and I</b>), P13-KO (<b>B, F, and J</b>), P30-KO (<b>C, G and K</b>) and P30-WT (<b>D, H and L</b>). The immunoreactivity of Veli3 is presented alone in the top row in grayscale (<b>A–D</b>). In the second row Veli3 (magenta) and glycogen phosphorylase (Glypho, green) signals are presented merged (<b>E–H</b>). PSD-95 immunoreactivity is shown in panels (<b>I–L</b>). Scale bar = 5 µm.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Neurological system", "neuroanatomy", "synapses", "neuroscience", "Developmental neuroscience", "ophthalmology", "Retinal disorders", "presynaptic"], "article_id"=>1075671, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Nawal Zabouri", "Silke Haverkamp"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063853.g005", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_additional_presynaptic_proteins_/1075671", "title"=>"Expression of additional presynaptic proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-13 10:36:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1556064"], "description"=>"<p>(<b>A–D</b>) Vertical sections from Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO at different ages (<b>A–C</b>) and WT (<b>D</b>). S-opsin (green) and calbindin (magenta) labeling show the morphology of cones in Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO and sprouting of horizontal cells at P13 (<b>A</b>), P15 (<b>B</b>), P18 (<b>C–D</b>). Arrowheads indicate the fasciculation or apposition of HC neurites onto cones and the arrow points to a cone sprout. (<b>E–H</b>) Vertical sections from Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO at different ages (<b>E–G</b>) and WT (<b>H</b>). S-opsin (green) and complexin 3 (magenta) immunoreactivity shows progressive appearance of Cplx3 in new cone synapses (white arrowheads). Grey arrowheads indicate the Cplx3-positve cone pedicles. (<b>I–L</b>) Vertical sections from Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO at different ages (<b>I–K</b>) and WT (<b>L</b>). S-opsin (green) and CtPB2 (magenta) expression shows progressive appearance of ribbons in new cone synapses (white arrowheads). Scale bar = 5 µm.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Neurological system", "neuroanatomy", "synapses", "neuroscience", "Developmental neuroscience", "ophthalmology", "Retinal disorders"], "article_id"=>1075734, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Nawal Zabouri", "Silke Haverkamp"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063853.g009", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cones_in_Ca_V_1_4_945_1F_KO_establish_new_synapses_/1075734", "title"=>"Cones in Ca<sub>V</sub>1.4<sub>(α1F)</sub>-KO establish new synapses.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-13 10:36:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1555982"], "description"=>"<p>(<b>A–H</b>) Vertical sections from P13 WT (<b>A</b>) and Ca<sub>V</sub>1.4(α<sub>1F</sub>)-KO (<b>B–D</b>), and P30 WT (<b>E</b>) and Ca<sub>V</sub>1.4(α<sub>1F</sub>)-KO (<b>F–H</b>) retinae. Confocal micrographs of retinae co-immunolabeled for Bassoon (Bsn - magenta) and CtPB2 (green) are merged in <b>A–B</b> (P13) and <b>E–F</b> (P30); in addition each staining is presented separately in grayscale: <b>C and G</b> depict Bassoon staining; <b>D and H</b> show CtBP2 distribution. White arrowheads indicate the terminals where CtBP2 and Bassoon are associated, grey arrowheads indicate isolated Bassoon in the ONL, and grey arrows indicate isolated CtBP2 in the ONL. Scale bar = 5 µm. <b>I–K:</b> Electron micrographs of cone pedicles in WT and CaV1.4(α1F)-KO at different ages. (<b>I</b>) Cone pedicle containing three presynaptic ribbons in a P13 WT mouse. (<b>J</b>) Cone pedicle containing two presynaptic ribbons in a P13 Ca<sub>V</sub>1.4(α1F)-KO. (<b>K</b>) Synaptic terminal containing two spherical presynaptic ribbons (white arrowheads) in an adult Ca<sub>V</sub>1.4(α<sub>1F</sub>)-KO. Scale bar = 0.5 µm.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Neurological system", "neuroanatomy", "synapses", "neuroscience", "Developmental neuroscience", "ophthalmology", "Retinal disorders", "ribeye", "bassoon"], "article_id"=>1075652, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Nawal Zabouri", "Silke Haverkamp"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063853.g004", "stats"=>{"downloads"=>0, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Association_of_Ribeye_and_Bassoon_at_different_ages_/1075652", "title"=>"Association of Ribeye and Bassoon at different ages.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-13 10:36:47"}

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