Idebenone Protects against Retinal Damage and Loss of Vision in a Mouse Model of Leber’s Hereditary Optic Neuropathy
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{"title"=>"Idebenone Protects against Retinal Damage and Loss of Vision in a Mouse Model of Leber's Hereditary Optic Neuropathy", "type"=>"journal", "authors"=>[{"first_name"=>"Fabrice D.", "last_name"=>"Heitz", "scopus_author_id"=>"56909654700"}, {"first_name"=>"Michael", "last_name"=>"Erb", "scopus_author_id"=>"57196563244"}, {"first_name"=>"Corinne", "last_name"=>"Anklin", "scopus_author_id"=>"26424571700"}, {"first_name"=>"Dimitri", "last_name"=>"Robay", "scopus_author_id"=>"8614503800"}, {"first_name"=>"Vincent", "last_name"=>"Pernet", "scopus_author_id"=>"8935985300"}, {"first_name"=>"Nuri", "last_name"=>"Gueven", "scopus_author_id"=>"6603624676"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "sgr"=>"84866511200", "scopus"=>"2-s2.0-84866511200", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pui"=>"365684215", "doi"=>"10.1371/journal.pone.0045182", "pmid"=>"23028832"}, "id"=>"e62016c2-1554-3100-9048-ca7bf5905a93", "abstract"=>"Leber's hereditary optic neuropathy (LHON) is an inherited disease caused by mutations in complex I of the mitochondrial respiratory chain. The disease is characterized by loss of central vision due to retinal ganglion cell (RGC) dysfunction and optic nerve atrophy. Despite progress towards a better understanding of the disease, no therapeutic treatment is currently approved for this devastating disease. Idebenone, a short-chain benzoquinone, has shown promising evidence of efficacy in protecting vision loss and in accelerating recovery of visual acuity in patients with LHON. It was therefore of interest to study suitable LHON models in vitro and in vivo to identify anatomical correlates for this protective activity. At nanomolar concentrations, idebenone protected the rodent RGC cell line RGC-5 against complex I dysfunction in vitro. Consistent with the reported dosing and observed effects in LHON patients, we describe that in mice, idebenone penetrated into the eye at concentrations equivalent to those which protected RGC-5 cells from complex I dysfunction in vitro. Consequently, we next investigated the protective effect of idebenone in a mouse model of LHON, whereby mitochondrial complex I dysfunction was caused by exposure to rotenone. In this model, idebenone protected against the loss of retinal ganglion cells, reduction in retinal thickness and gliosis. Furthermore, consistent with this protection of retinal integrity, idebenone restored the functional loss of vision in this disease model. These results support the pharmacological activity of idebenone and indicate that idebenone holds potential as an effective treatment for vision loss in LHON patients.", "link"=>"http://www.mendeley.com/research/idebenone-protects-against-retinal-damage-loss-vision-mouse-model-lebers-hereditary-optic-neuropathy", "reader_count"=>40, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>12, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>2, "Student > Master"=>3, "Other"=>3, "Student > Bachelor"=>8}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>12, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>2, "Student > Master"=>3, "Other"=>3, "Student > Bachelor"=>8}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>3, "Medicine and Dentistry"=>14, "Agricultural and Biological Sciences"=>12, "Neuroscience"=>4, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>5}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>14}, "Neuroscience"=>{"Neuroscience"=>4}, "Chemistry"=>{"Chemistry"=>5}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>12}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "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"=>{"United States"=>1, "United Kingdom"=>1, "Spain"=>1, "India"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/575879"], "description"=>"<p>Visual acuity was evaluated by counting the number of head movements at a velocity of 3 rpm 7 days prior injection (day -7) and 1 to 70 days after injection (day 1, 7, 21, 35, 70) of rotenone (5 mM). Mice were treated with dietary idebenone 2000 mg/kg or vehicle for the time of the experiment. (A) Schematic representation of the experimental setup. After vehicle (DMSO) injection, head movements in both directions of drum rotation (clockwise: CW; counterclockwise CCW) remain intact. Injection of rotenone into the left eye however, affects only the CW responses (dashed arrow) whereas CCW responses remain unaffected. (B) Quantification of clockwise (CW) head movement (number of head movements/2 min) following vehicle treatment and rotenone injection (vehicle + rotenone, n = 10 animals), and idebenone 2000 mg/kg treatment and rotenone injection (IDE 2000+ rotenone, n = 11 animals). Data are expressed as mean ± SEM. Statistical significance relative to vehicle + rotenone group: p≤0.05 (*); (C) Percentage of mice showing clockwise (CW) head movements for each treatment group 70 days after injection. Responder: group of mice showing head movements; Non-responder: group of mice without head movements.</p>", "links"=>[], "tags"=>["time-dependently", "restores", "rotenone-induced"], "article_id"=>246371, "categories"=>["Neuroscience", "Biochemistry", "Medicine", "Pharmacology", "Genetics"], "users"=>["Fabrice D. Heitz", "Michael Erb", "Corinne Anklin", "Dimitri Robay", "Vincent Pernet", "Nuri Gueven"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0045182.g008", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Idebenone_time_dependently_restores_rotenone_induced_loss_of_vision_/246371", "title"=>"Idebenone time-dependently restores rotenone-induced loss of vision.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-18 01:46:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/575110"], "description"=>"<p>Distribution of NQO1 in the mouse retina co-stained with rabbit anti-NQO1 and mouse monoclonal anti-Brn3a primary antibodies. Anti-rabbit Alexa 488-conjugated and anti-mouse Alexa 495-conjugated secondary antibodies were used for fluorescent visualization of NQO1 (green) and RGCs (red) in the retina. The white rectangle in (A) depicts the region of interest shown at high magnification in (B). The different retinal cell layers are shown by nuclear staining using DAPI (blue). Scale bars represent 30 µm. (OS: outer segment, IS: inner segment, ONL: outer nuclear layer, OPL: outer plexiform layer, INL: inner nuclear layer, IPL: inner plexiform layer, GCL: ganglion cell layer (incl. nerve fiber layer).</p>", "links"=>[], "tags"=>["rgcs"], "article_id"=>245605, "categories"=>["Neuroscience", "Biochemistry", "Medicine", "Pharmacology", "Genetics"], "users"=>["Fabrice D. Heitz", "Michael Erb", "Corinne Anklin", "Dimitri Robay", "Vincent Pernet", "Nuri Gueven"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0045182.g002", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_NQO1_expression_in_RGCs_and_the_inner_segment_of_photoreceptors_/245605", "title"=>"NQO1 expression in RGCs and the inner segment of photoreceptors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-18 01:33:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/574892"], "description"=>"<p>(A) Scheme of the experimental design. RGC-5 cells were pre-incubated with idebenone or vehicle (DMSO) for 1 or 2 days before the complex I inhibitor rotenone was applied to the cells for 6 hours. Cell viability was then measured after 1 day post-incubation with idebenone or vehicle. (B) Treatment with rotenone caused a 59% reduction in cell viability in vehicle-treated RGC-5 cells. (C) Idebenone pre-treatment for 1 (white bars) and 2 days (black bars) significantly rescued cell viability (expressed as % rescue). Data are expressed as mean ± SD (n = 6 wells per group). Statistical significance relative to vehicle group: p≤0.05 (*), p≤0.001 (***).</p>", "links"=>[], "tags"=>["idebenone", "inhibition", "rgc-5", "cells"], "article_id"=>245382, "categories"=>["Neuroscience", "Biochemistry", "Medicine", "Pharmacology", "Genetics"], "users"=>["Fabrice D. Heitz", "Michael Erb", "Corinne Anklin", "Dimitri Robay", "Vincent Pernet", "Nuri Gueven"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0045182.g001", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Protective_effect_of_idebenone_against_complex_I_inhibition_in_RGC_5_cells_in_vitro_/245382", "title"=>"Protective effect of idebenone against complex I inhibition in RGC-5 cells <i>in vitro</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-18 01:29:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/575787"], "description"=>"<p>For analysis of gliosis 7 days after intravitreal injection of rotenone or DMSO (Sham), mice were treated with dietary idebenone (IDE 200, 400 and 2000 mg/kg body weight) or vehicle. (A) Images of retinal slices stained with anti-GFAP primary antibody to visualize Müller glial cell projections (white arrows). White arrowheads indicate outer plexiform layer and also illustrate rotenone induced reduction in retinal thickness (i.e. distance between white arrow heads and ganglion cell layer at the top of the images). Scale bar = 15 µm. (B) Quantification of gliosis (GFAP signal based on relative fluorescence units, RFU) following idebenone treatment and rotenone injection (n = 3 to 7 per group). Data are expressed as mean ± SEM.</p>", "links"=>[], "tags"=>["protects", "rotenone-induced"], "article_id"=>246281, "categories"=>["Neuroscience", "Biochemistry", "Medicine", "Pharmacology", "Genetics"], "users"=>["Fabrice D. Heitz", "Michael Erb", "Corinne Anklin", "Dimitri Robay", "Vincent Pernet", "Nuri Gueven"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0045182.g007", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Idebenone_protects_against_rotenone_induced_gliosis_/246281", "title"=>"Idebenone protects against rotenone-induced gliosis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-18 01:44:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/575988"], "description"=>"<p>Histological data are expressed as % of Sham (DMSO) controls ± SEM. Numbers of retinal ganglion cells (RGC number) is based on RGCs/mm 7 days post-injection applicable to all groups; retinal thickness (µm) 7 days post-injection; gliosis is based on relative fluorescence units (RFU) of GFAP-specific immunostaining 7 days post-injection. Sham (DMSO): sham-injected with DMSO; vehicle: vehicle treated; rotenone: rotenone-injected; IDE200: idebenone treated (200 mg/kg); IDE400: idebenone treated (400 mg/kg); IDE2000: idebenone treated (2000 mg/kg). Statistical significance relative to vehicle + rotenone group: p≤0.05 (*), p≤0.01 (**), p≤0.001 (***); based on raw numbers; n = number of retinas per group.</p>", "links"=>[], "tags"=>["idebenone", "endpoints"], "article_id"=>246480, "categories"=>["Neuroscience", "Biochemistry", "Medicine", "Pharmacology", "Genetics"], "users"=>["Fabrice D. Heitz", "Michael Erb", "Corinne Anklin", "Dimitri Robay", "Vincent Pernet", "Nuri Gueven"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0045182.t001", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dose_effect_of_idebenone_treatment_on_multiple_endpoints_in_an_in_vivo_mouse_model_for_LHON_/246480", "title"=>"Dose-effect of idebenone treatment on multiple endpoints in an <i>in vivo</i> mouse model for LHON.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-09-18 01:48:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/575668"], "description"=>"<p>For analysis of retinal thickness 7 days after intravitreal injection of rotenone or DMSO (Sham), mice were treated with dietary idebenone (IDE 200, 400 and 2000 mg/kg body weight) or vehicle. (A) Images of retinal slices stained with anti-beta 3 tubulin primary antibodies to visualize inner and outer retinal layers. The arrows indicate retinal thickness measured from the pigment epithelium to the nerve fiber layer. Scale bar = 30 µm. (B) Quantification of total retinal thickness (µm) following idebenone treatment and rotenone injection (n = 6 to 10 per group). Data are expressed as mean ± SEM.</p>", "links"=>[], "tags"=>["protects", "rotenone-induced", "retinal"], "article_id"=>246161, "categories"=>["Neuroscience", "Biochemistry", "Medicine", "Pharmacology", "Genetics"], "users"=>["Fabrice D. Heitz", "Michael Erb", "Corinne Anklin", "Dimitri Robay", "Vincent Pernet", "Nuri Gueven"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0045182.g006", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Idebenone_protects_against_rotenone_induced_decrease_in_retinal_thickness_/246161", "title"=>"Idebenone protects against rotenone-induced decrease in retinal thickness.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-18 01:42:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/575249"], "description"=>"<p>Concentrations of idebenone in aqueous humor (open circle) and vitreous humor (filled triangle) following once daily administration of idebenone in the diet for 21 days (A) and following single oral administration of idebenone at 60 mg/kg (B) were determined. Concentrations of idebenone in the eye fluids are expressed as ng/ml (left y axis) and nM (right y axis). For (A), sampling time was more than 8h after last dose of idebenone, the values therefore represent trough levels.</p>", "links"=>[], "tags"=>["idebenone"], "article_id"=>245748, "categories"=>["Neuroscience", "Biochemistry", "Medicine", "Pharmacology", "Genetics"], "users"=>["Fabrice D. Heitz", "Michael Erb", "Corinne Anklin", "Dimitri Robay", "Vincent Pernet", "Nuri Gueven"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0045182.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pharmacokinetic_analysis_of_idebenone_in_eye_fluids_/245748", "title"=>"Pharmacokinetic analysis of idebenone in eye fluids.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-18 01:35:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/575415"], "description"=>"<p>(A) Image of a normal retinal section showing RGCs (red) and Müller glial cell projections (green) using anti-Brn3a and anti-GFAP primary antibodies respectively. The different retinal cell layers are shown by nuclear staining using DAPI (blue). (Scale bar = 25 µm). (B) To investigate the efficacy of idebenone in protecting against complex I deficiency in the retina <i>in vivo</i>, we performed intravitreal injection of rotenone (15 mM) in mice pre-treated for 21 days with idebenone or vehicle in diet. Retinal ganglion cell number, retinal thickness and reactive gliosis were evaluated based on histological analysis of retinal sections 7 days after rotenone challenge.</p>", "links"=>[], "tags"=>["idebenone", "lhon"], "article_id"=>245910, "categories"=>["Neuroscience", "Biochemistry", "Medicine", "Pharmacology", "Genetics"], "users"=>["Fabrice D. Heitz", "Michael Erb", "Corinne Anklin", "Dimitri Robay", "Vincent Pernet", "Nuri Gueven"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0045182.g004", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Experimental_approach_to_study_the_protective_effect_of_idebenone_in_a_LHON_mouse_model_/245910", "title"=>"Experimental approach to study the protective effect of idebenone in a LHON mouse model.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-18 01:38:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/304932", "https://ndownloader.figshare.com/files/305002", "https://ndownloader.figshare.com/files/305075", "https://ndownloader.figshare.com/files/305141", "https://ndownloader.figshare.com/files/305191", "https://ndownloader.figshare.com/files/305247", "https://ndownloader.figshare.com/files/305295"], "description"=>"<div><p>Leber’s hereditary optic neuropathy (LHON) is an inherited disease caused by mutations in complex I of the mitochondrial respiratory chain. The disease is characterized by loss of central vision due to retinal ganglion cell (RGC) dysfunction and optic nerve atrophy. Despite progress towards a better understanding of the disease, no therapeutic treatment is currently approved for this devastating disease. Idebenone, a short-chain benzoquinone, has shown promising evidence of efficacy in protecting vision loss and in accelerating recovery of visual acuity in patients with LHON. It was therefore of interest to study suitable LHON models <em>in vitro</em> and <em>in vivo</em> to identify anatomical correlates for this protective activity. At nanomolar concentrations, idebenone protected the rodent RGC cell line RGC-5 against complex I dysfunction <em>in vitro.</em> Consistent with the reported dosing and observed effects in LHON patients, we describe that in mice, idebenone penetrated into the eye at concentrations equivalent to those which protected RGC-5 cells from complex I dysfunction <em>in vitro</em>. Consequently, we next investigated the protective effect of idebenone in a mouse model of LHON, whereby mitochondrial complex I dysfunction was caused by exposure to rotenone. In this model, idebenone protected against the loss of retinal ganglion cells, reduction in retinal thickness and gliosis. Furthermore, consistent with this protection of retinal integrity, idebenone restored the functional loss of vision in this disease model. These results support the pharmacological activity of idebenone and indicate that idebenone holds potential as an effective treatment for vision loss in LHON patients.</p> </div>", "links"=>[], "tags"=>["idebenone", "protects", "retinal", "hereditary", "optic", "neuropathy"], "article_id"=>120151, "categories"=>["Neuroscience", "Biochemistry", "Medicine", "Pharmacology", "Genetics"], "users"=>["Fabrice D. Heitz", "Michael Erb", "Corinne Anklin", "Dimitri Robay", "Vincent Pernet", "Nuri Gueven"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0045182.s001", "https://dx.doi.org/10.1371/journal.pone.0045182.s002", "https://dx.doi.org/10.1371/journal.pone.0045182.s003", "https://dx.doi.org/10.1371/journal.pone.0045182.s004", "https://dx.doi.org/10.1371/journal.pone.0045182.s005", "https://dx.doi.org/10.1371/journal.pone.0045182.s006", "https://dx.doi.org/10.1371/journal.pone.0045182.s007"], "stats"=>{"downloads"=>33, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Idebenone_Protects_against_Retinal_Damage_and_Loss_of_Vision_in_a_Mouse_Model_of_Leber_s_Hereditary_Optic_Neuropathy/120151", "title"=>"Idebenone Protects against Retinal Damage and Loss of Vision in a Mouse Model of Leber’s Hereditary Optic Neuropathy", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-09-18 00:02:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/575578"], "description"=>"<p>Mice were treated with dietary idebenone (IDE 200, 400 and 2000 mg/kg body weight) or vehicle. (A) Images of retinal slices stained with anti-Brn3a primary antibody to visualize RGCs. Scale bar = 25 µm. (B) Quantification of RGCs (RGC number/mm) following idebenone treatment and rotenone injection (n = 6 to 10 per group). Data expressed as mean ± SEM.</p>", "links"=>[], "tags"=>["prevents", "rotenone-induced", "rgc", "rgcs", "retina", "days", "intravitreal", "injection", "rotenone", "dmso"], "article_id"=>246057, "categories"=>["Neuroscience", "Biochemistry", "Medicine", "Pharmacology", "Genetics"], "users"=>["Fabrice D. Heitz", "Michael Erb", "Corinne Anklin", "Dimitri Robay", "Vincent Pernet", "Nuri Gueven"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0045182.g005", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Idebenone_prevents_rotenone_induced_RGC_death_Analysis_of_RGCs_in_the_mouse_retina_7_days_after_intravitreal_injection_of_rotenone_or_DMSO_Sham_/246057", "title"=>"Idebenone prevents rotenone-induced RGC death. Analysis of RGCs in the mouse retina 7 days after intravitreal injection of rotenone or DMSO (Sham).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-18 01:40:57"}

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Relative Metric

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