Loss of Synaptic Connectivity, Particularly in Second Order Neurons Is a Key Feature of Diabetic Retinal Neuropathy in the Ins2Akita Mouse
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{"title"=>"Loss of synaptic connectivity, particularly in second order neurons is a key feature of diabetic retinal neuropathy in the Ins2Akita mouse", "type"=>"journal", "authors"=>[{"first_name"=>"Jose R.", "last_name"=>"Hombrebueno", "scopus_author_id"=>"35368696600"}, {"first_name"=>"Mei", "last_name"=>"Chen", "scopus_author_id"=>"55616783100"}, {"first_name"=>"Rosana G.", "last_name"=>"Penalva", "scopus_author_id"=>"6505760221"}, {"first_name"=>"Heping", "last_name"=>"Xu", "scopus_author_id"=>"35742488300"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"24848689", "doi"=>"10.1371/journal.pone.0097970", "sgr"=>"84901320699", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "scopus"=>"2-s2.0-84901320699", "issn"=>"19326203", "pui"=>"373161054"}, "id"=>"3234761f-2273-30d3-b511-d46c1463e6f6", "abstract"=>"Retinal neurodegeneration is a key component of diabetic retinopathy (DR), although the detailed neuronal damage remains ill-defined. Recent evidence suggests that in addition to amacrine and ganglion cell, diabetes may also impact on other retinal neurons. In this study, we examined retinal degenerative changes in Ins2Akita diabetic mice. In scotopic electroretinograms (ERG), b-wave and oscillatory potentials were severely impaired in 9-month old Ins2Akita mice. Despite no obvious pathology in fundoscopic examination, optical coherence tomography (OCT) revealed a progressive thinning of the retina from 3 months onwards. Cone but not rod photoreceptor loss was observed in 3-month-old diabetic mice. Severe impairment of synaptic connectivity at the outer plexiform layer (OPL) was detected in 9-month old Ins2Akita mice. Specifically, photoreceptor presynaptic ribbons were reduced by 25% and postsynaptic boutons by 70%, although the density of horizontal, rod- and cone-bipolar cells remained similar to non-diabetic controls. Significant reductions in GABAergic and glycinergic amacrine cells and Brn3a+ retinal ganglion cells were also observed in 9-month old Ins2Akita mice. In conclusion, the Ins2Akita mouse develops cone photoreceptor degeneration and the impairment of synaptic connectivity at the OPL, predominately resulting from the loss of postsynaptic terminal boutons. Our findings suggest that the Ins2Akita mouse is a good model to study diabetic retinal neuropathy.", "link"=>"http://www.mendeley.com/research/loss-synaptic-connectivity-particularly-second-order-neurons-key-feature-diabetic-retinal-neuropathy", "reader_count"=>32, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Researcher"=>3, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>6, "Student > Postgraduate"=>1, "Other"=>3, "Student > Master"=>10, "Student > Bachelor"=>3, "Lecturer > Senior Lecturer"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Researcher"=>3, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>6, "Student > Postgraduate"=>1, "Other"=>3, "Student > Master"=>10, "Student > Bachelor"=>3, "Lecturer > Senior Lecturer"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Engineering"=>2, "Biochemistry, Genetics and Molecular Biology"=>8, "Agricultural and Biological Sciences"=>12, "Medicine and Dentistry"=>4, "Neuroscience"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Neuroscience"=>{"Neuroscience"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>12}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}, "Unspecified"=>{"Unspecified"=>4}}, "reader_count_by_country"=>{"Brazil"=>1, "Tunisia"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1505771"], "description"=>"<p>Primary antibodies used in the study.</p>", "links"=>[], "tags"=>["anatomy", "histology", "Biochemistry", "Neurochemistry", "neurotransmitters", "cell biology", "Cell processes", "Cellular stress responses", "Cellular types", "Animal cells", "neurons", "Cellular structures and organelles", "Molecular cell biology", "neuroscience", "Cellular neuroscience", "Neuronal morphology", "Sensory systems", "Visual system", "Endocrinology", "Diabetic endocrinology", "Metabolic disorders", "Diabetes mellitus", "Type 1 diabetes", "ophthalmology", "Retinal disorders", "Model organisms", "Animal models", "Mouse models", "antibodies"], "article_id"=>1033054, "categories"=>["Biological Sciences"], "users"=>["Jose R. Hombrebueno", "Mei Chen", "Rosana G. Penalva", "Heping Xu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0097970.t001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Primary_antibodies_used_in_the_study_/1033054", "title"=>"Primary antibodies used in the study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-05-21 02:59:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/1505753"], "description"=>"<p>(A) SD-OCT image from 9-month old control retina. Retinal thickness was measured at 300, 600 and 900 µm eccentricities in dorso-ventral and nasal-temporal retinal regions, from NFL-OS (total retinal thickness), NFL-INL (inner retinal thickness) and OPL-OS (outer retinal thickness). Isodensity maps (B) and quantitative analysis (C) of total retinal thickness from control and Ins2<sup>Akita</sup> mice at different ages. (D) The cumulative reduction of outer, inner and total retinal thickness in different ages of control and Ins2<sup>Akita</sup> mice. Fundus (E, H) and OCT images (F-G, I-J) taken from 9-month old control (A-C) and Ins2<sup>Akita</sup> mice (D-F). (B-D) n = 6 mice per strain/age, *<i>P</i><0.05, ** <i>P</i><0.01, *** <i>P</i><0.001 compared to control mice of the same age. Student's <i>t</i>-test. RPE, retinal pigment epithelium; IS/OS, photoreceptor inner/outer segments; ONL, outer nuclear layer; OPL, outer plexiform layer; INL, inner nuclear layer; IPL, inner plexiform layer; GCL/NFL, ganglion/nerve fibre layer.</p>", "links"=>[], "tags"=>["anatomy", "histology", "Biochemistry", "Neurochemistry", "neurotransmitters", "cell biology", "Cell processes", "Cellular stress responses", "Cellular types", "Animal cells", "neurons", "Cellular structures and organelles", "Molecular cell biology", "neuroscience", "Cellular neuroscience", "Neuronal morphology", "Sensory systems", "Visual system", "Endocrinology", "Diabetic endocrinology", "Metabolic disorders", "Diabetes mellitus", "Type 1 diabetes", "ophthalmology", "Retinal disorders", "Model organisms", "Animal models", "Mouse models", "degeneration"], "article_id"=>1033036, "categories"=>["Biological Sciences"], "users"=>["Jose R. Hombrebueno", "Mei Chen", "Rosana G. Penalva", "Heping Xu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0097970.g002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Retinal_degeneration_in_the_Ins2_Akita_mouse_/1033036", "title"=>"Retinal degeneration in the Ins2<sup>Akita</sup> mouse.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-21 02:59:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/1505762"], "description"=>"<p>(A-C) Photoreceptor synaptic ribbons immunostained with bassoon in 9-month old control and 6- and 9-month old Ins2<sup>Akita</sup> mice. Immunostaining of cone-bipolar (secretagogin) (D-F), rod-bipolar (PKCα) (G-I) and horizontal cells (calbindin) (J-L) in 9–month old control and 6- and 9-month old Ins2<sup>Akita</sup> mice. Normal dendritic arbors of cone-bipolar, rod-bipolar and horizontal cells at the OPL (arrowheads). Loss of dendritic complexity in cone-bipolar, rod-bipolar and horizontal cells in 9-month old Ins2<sup>Akita</sup> mice (open-arrowheads). Quantitative analysis of photoreceptor synaptic ribbons (<i>box1</i>) (M) and cone-bipolar (<i>box2</i>) (N) and rod-bipolar dendritic length (<i>box3</i>) (O) in control and Ins2<sup>Akita</sup> mice at different ages. (M-O) n≥20 retinal images per strain/age, *<i>P</i><0.05, **<i>P</i><0.01, ***<i>P</i><0.001. 2-way ANOVA. OPL, outer plexiform layer; INL, inner nuclear layer. Scale bar: 10 µm.</p>", "links"=>[], "tags"=>["anatomy", "histology", "Biochemistry", "Neurochemistry", "neurotransmitters", "cell biology", "Cell processes", "Cellular stress responses", "Cellular types", "Animal cells", "neurons", "Cellular structures and organelles", "Molecular cell biology", "neuroscience", "Cellular neuroscience", "Neuronal morphology", "Sensory systems", "Visual system", "Endocrinology", "Diabetic endocrinology", "Metabolic disorders", "Diabetes mellitus", "Type 1 diabetes", "ophthalmology", "Retinal disorders", "Model organisms", "Animal models", "Mouse models", "elements", "opl"], "article_id"=>1033045, "categories"=>["Biological Sciences"], "users"=>["Jose R. Hombrebueno", "Mei Chen", "Rosana G. Penalva", "Heping Xu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0097970.g004", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Synaptic_elements_in_the_OPL_of_control_and_Ins2_Akita_mice_/1033045", "title"=>"Synaptic elements in the OPL of control and Ins2<sup>Akita</sup> mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-21 02:59:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/1505761"], "description"=>"<p>(A-F) Retinal photomicrographs of rhodopsin (green) and cone-arrestin (red) immunoreactivities in 9-month old control (A-C) and Ins2<sup>Akita</sup> (D-F) mice. (G-H) Cell densities of total photoreceptors (DAPI<sup>+</sup> nuclei - <i>box1</i>), cones (<i>box2</i>) and rods (difference between DAPI<sup>+</sup> nuclei and cones) in 3-, 6- and 9-month old control and Ins2<sup>Akita</sup> mice. (G-H) n≥20 retinal images per strain/age, *<i>P</i><0.05, **<i>P</i><0.01 compared to control mice of the same age. 2-way ANOVA. OS, outer segments; IS, inner segments; ONL, outer nuclear layer; OPL, outer plexiform layer. Scale bar: 30 µm.</p>", "links"=>[], "tags"=>["anatomy", "histology", "Biochemistry", "Neurochemistry", "neurotransmitters", "cell biology", "Cell processes", "Cellular stress responses", "Cellular types", "Animal cells", "neurons", "Cellular structures and organelles", "Molecular cell biology", "neuroscience", "Cellular neuroscience", "Neuronal morphology", "Sensory systems", "Visual system", "Endocrinology", "Diabetic endocrinology", "Metabolic disorders", "Diabetes mellitus", "Type 1 diabetes", "ophthalmology", "Retinal disorders", "Model organisms", "Animal models", "Mouse models", "photoreceptor", "degeneration"], "article_id"=>1033044, "categories"=>["Biological Sciences"], "users"=>["Jose R. Hombrebueno", "Mei Chen", "Rosana G. Penalva", "Heping Xu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0097970.g003", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cone_photoreceptor_degeneration_in_the_Ins2_Akita_mouse_/1033044", "title"=>"Cone photoreceptor degeneration in the Ins2<sup>Akita</sup> mouse.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-21 02:59:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/1505770"], "description"=>"<p>Inner retina photomicrographs of GABA (A-D), GlyT1 (E, F) or Brn3a immnoreactivities (G, H) in 9-month old control and 3-, 6- and 9-month old Ins2<sup>Akita</sup> mice. Quantitative analysis of INL-GABAergic amacrine cells (<i>box1</i>) (I), INL-glycinergic amacrine cells (<i>box2</i>) (J) and retinal ganglion cells (<i>box3</i>) (K) in control and Ins2<sup>Akita</sup> mice at different ages. (I-K) n≥20 retinal images per strain/age, *<i>P</i><0.05, **<i>P</i><0.01. 2-way ANOVA. INL, inner nuclear layer; IPL, inner plexiform layer; GCL, ganglion cell layer. Scale bar: 20 µm.</p>", "links"=>[], "tags"=>["anatomy", "histology", "Biochemistry", "Neurochemistry", "neurotransmitters", "cell biology", "Cell processes", "Cellular stress responses", "Cellular types", "Animal cells", "neurons", "Cellular structures and organelles", "Molecular cell biology", "neuroscience", "Cellular neuroscience", "Neuronal morphology", "Sensory systems", "Visual system", "Endocrinology", "Diabetic endocrinology", "Metabolic disorders", "Diabetes mellitus", "Type 1 diabetes", "ophthalmology", "Retinal disorders", "Model organisms", "Animal models", "Mouse models", "retinal", "ganglion"], "article_id"=>1033053, "categories"=>["Biological Sciences"], "users"=>["Jose R. Hombrebueno", "Mei Chen", "Rosana G. Penalva", "Heping Xu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0097970.g007", "stats"=>{"downloads"=>0, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Amacrine_and_retinal_ganglion_cell_loss_in_the_Ins2_Akita_mouse_/1033053", "title"=>"Amacrine and retinal ganglion cell loss in the Ins2<sup>Akita</sup> mouse.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-21 02:59:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/1505769"], "description"=>"<p>Immunostaining and quantitative analysis of horizontal cell (<i>box1</i>) (A-E), cone-bipolar (<i>box2</i>) (F-G, J) and rod-bipolar (<i>box3</i>) (H-J) cell somata in control and Ins2<sup>Akita</sup> mice at 9 months of age. (K-L) Cone-bipolar cell axon terminals in 9 month-old control and Ins2<sup>Akita</sup> mice. (M-O) Immunostaining and quantitative analysis of rod-bipolar cell axon terminals (<i>box3</i>) in control and Ins2<sup>Akita</sup> mice at different ages. Loss of rod-bipolar cell axon terminals (open arrowheads) in Ins2<sup>Akita</sup> retinas. (E, J, O) n≥20 retinal images per strain/age, *<i>P</i><0.05, **<i>P</i><0.01. 2-way ANOVA. ONL, outer nuclear layer; OPL, outer plexiform layer; INL, inner nuclear layer; IPL, inner plexiform layer; GCL, ganglion cell layer. Scale bar: 10 µm.</p>", "links"=>[], "tags"=>["anatomy", "histology", "Biochemistry", "Neurochemistry", "neurotransmitters", "cell biology", "Cell processes", "Cellular stress responses", "Cellular types", "Animal cells", "neurons", "Cellular structures and organelles", "Molecular cell biology", "neuroscience", "Cellular neuroscience", "Neuronal morphology", "Sensory systems", "Visual system", "Endocrinology", "Diabetic endocrinology", "Metabolic disorders", "Diabetes mellitus", "Type 1 diabetes", "ophthalmology", "Retinal disorders", "Model organisms", "Animal models", "Mouse models", "neuron"], "article_id"=>1033052, "categories"=>["Biological Sciences"], "users"=>["Jose R. Hombrebueno", "Mei Chen", "Rosana G. Penalva", "Heping Xu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0097970.g006", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Second_order_neuron_changes_in_the_Ins2_Akita_mouse_/1033052", "title"=>"Second-order neuron changes in the Ins2<sup>Akita</sup> mouse.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-21 02:59:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/1505765"], "description"=>"<p>Photomicrographs of retinal sections double-labelled for bassoon (red) with PKCα (A-C) or calbindin (E-G) in 9-month control and 6- and 9-month old Ins2<sup>Akita</sup> mice. Absence of paired connectivity between photoreceptor terminals and second-order neurons in 9-month old Ins2<sup>Akita</sup> mice (insets C, G). Quantitative analysis of rod-bipolar (<i>box1</i>) (D) and horizontal cell (<i>box2</i>) (H) dendritic boutons in control and Ins2<sup>Akita</sup> mice at different ages. (D-H) n≥20 retinal images per strain/age, ***<i>P</i><0.001. 2-way ANOVA. Scale bar: 10 µm, inset 5 µm.</p>", "links"=>[], "tags"=>["anatomy", "histology", "Biochemistry", "Neurochemistry", "neurotransmitters", "cell biology", "Cell processes", "Cellular stress responses", "Cellular types", "Animal cells", "neurons", "Cellular structures and organelles", "Molecular cell biology", "neuroscience", "Cellular neuroscience", "Neuronal morphology", "Sensory systems", "Visual system", "Endocrinology", "Diabetic endocrinology", "Metabolic disorders", "Diabetes mellitus", "Type 1 diabetes", "ophthalmology", "Retinal disorders", "Model organisms", "Animal models", "Mouse models", "opl"], "article_id"=>1033048, "categories"=>["Biological Sciences"], "users"=>["Jose R. Hombrebueno", "Mei Chen", "Rosana G. Penalva", "Heping Xu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0097970.g005", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Synaptic_structure_in_the_OPL_of_control_and_Ins2_Akita_mice_/1033048", "title"=>"Synaptic structure in the OPL of control and Ins2<sup>Akita</sup> mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-21 02:59:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/1505781", "https://ndownloader.figshare.com/files/1505782"], "description"=>"<div><p>Retinal neurodegeneration is a key component of diabetic retinopathy (DR), although the detailed neuronal damage remains ill-defined. Recent evidence suggests that in addition to amacrine and ganglion cell, diabetes may also impact on other retinal neurons. In this study, we examined retinal degenerative changes in Ins2<sup>Akita</sup> diabetic mice. In scotopic electroretinograms (ERG), b-wave and oscillatory potentials were severely impaired in 9-month old Ins2<sup>Akita</sup> mice. Despite no obvious pathology in fundoscopic examination, optical coherence tomography (OCT) revealed a progressive thinning of the retina from 3 months onwards. Cone but not rod photoreceptor loss was observed in 3-month-old diabetic mice. Severe impairment of synaptic connectivity at the outer plexiform layer (OPL) was detected in 9-month old Ins2<sup>Akita</sup> mice. Specifically, photoreceptor presynaptic ribbons were reduced by 25% and postsynaptic boutons by 70%, although the density of horizontal, rod- and cone-bipolar cells remained similar to non-diabetic controls. Significant reductions in GABAergic and glycinergic amacrine cells and Brn3a<sup>+</sup> retinal ganglion cells were also observed in 9-month old Ins2<sup>Akita</sup> mice. In conclusion, the Ins2<sup>Akita</sup> mouse develops cone photoreceptor degeneration and the impairment of synaptic connectivity at the OPL, predominately resulting from the loss of postsynaptic terminal boutons. Our findings suggest that the Ins2<sup>Akita</sup> mouse is a good model to study diabetic retinal neuropathy.</p></div>", "links"=>[], "tags"=>["anatomy", "histology", "Biochemistry", "Neurochemistry", "neurotransmitters", "cell biology", "Cell processes", "Cellular stress responses", "Cellular types", "Animal cells", "neurons", "Cellular structures and organelles", "Molecular cell biology", "neuroscience", "Cellular neuroscience", "Neuronal morphology", "Sensory systems", "Visual system", "Endocrinology", "Diabetic endocrinology", "Metabolic disorders", "Diabetes mellitus", "Type 1 diabetes", "ophthalmology", "Retinal disorders", "Model organisms", "Animal models", "Mouse models", "synaptic", "diabetic", "retinal", "neuropathy"], "article_id"=>1033057, "categories"=>["Biological Sciences"], "users"=>["Jose R. Hombrebueno", "Mei Chen", "Rosana G. Penalva", "Heping Xu"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0097970.s001", "https://dx.doi.org/10.1371/journal.pone.0097970.s002"], "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Loss_of_Synaptic_Connectivity_Particularly_in_Second_Order_Neurons_Is_a_Key_Feature_of_Diabetic_Retinal_Neuropathy_in_the_Ins2_Akita_Mouse/1033057", "title"=>"Loss of Synaptic Connectivity, Particularly in Second Order Neurons Is a Key Feature of Diabetic Retinal Neuropathy in the Ins2<sup>Akita</sup> Mouse", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-05-21 02:59:48"}

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Relative Metric

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