Susceptibility to Neurodegeneration in a Glaucoma Is Modified by Bax Gene Dosage
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{"title"=>"Susceptibility to neurodegeneration in a glaucoma is modified by bax gene dosage", "type"=>"journal", "authors"=>[{"first_name"=>"Richard T.", "last_name"=>"Libby", "scopus_author_id"=>"7006498298"}, {"first_name"=>"Yan", "last_name"=>"Li", "scopus_author_id"=>"55785116100"}, {"first_name"=>"Olga V.", "last_name"=>"Savinova", "scopus_author_id"=>"57189497544"}, {"first_name"=>"Joseph", "last_name"=>"Barter", "scopus_author_id"=>"23388622900"}, {"first_name"=>"Richard S.", "last_name"=>"Smith", "scopus_author_id"=>"7410287965"}, {"first_name"=>"Robert W.", "last_name"=>"Nickells", "scopus_author_id"=>"7003624797"}, {"first_name"=>"Simon W.M.", "last_name"=>"John", "scopus_author_id"=>"7202388904"}], "year"=>2005, "source"=>"PLoS Genetics", "identifiers"=>{"sgr"=>"77955614345", "doi"=>"10.1371/journal.pgen.0010004", "pui"=>"359358558", "pmid"=>"16103918", "scopus"=>"2-s2.0-77955614345", "issn"=>"15537390", "isbn"=>"1553-7390 (Print)"}, "id"=>"e42d907c-03bd-3cf7-951f-95cade5b6fc7", "abstract"=>"In glaucoma, harmful intraocular pressure often contributes to retinal ganglion cell death. It is not clear, however, if intraocular pressure directly insults the retinal ganglion cell axon, the soma, or both. The pathways that mediate pressure-induced retinal ganglion cell death are poorly defined, and no molecules are known to be required. DBA/2J mice deficient in the proapoptotic molecule BCL2-associated X protein (BAX) were used to investigate the roles of BAX-mediated cell death pathways in glaucoma. Both Bax+/- and Bax-/- mice were protected from retinal ganglion cell death. In contrast, axonal degeneration was not prevented in either Bax+/- or Bax-/- mice. While BAX deficiency did not prevent axonal degeneration, it did slow axonal loss. Additionally, we compared the effects of BAX deficiency on the glaucoma to its effects on retinal ganglion cell death due to two insults that are proposed to participate in glaucoma. As in the glaucoma, BAX deficiency protected retinal ganglion cells after axon injury by optic nerve crush. However, it did not protect retinal ganglion cells from N-methyl-D-aspartate (NMDA)-induced excitotoxicity. BAX is required for retinal ganglion cell death in an inherited glaucoma; however, it is not required for retinal ganglion cell axon degeneration. This indicates that distinct somal and axonal degeneration pathways are active in this glaucoma. Finally, our data support a role for optic nerve injury but not for NMDA receptor-mediated excitotoxicity in this glaucoma. These findings indicate a need to understand axon-specific degeneration pathways in glaucoma, and they suggest that distinct somal and axonal degeneration pathways may need to be targeted to save vision.", "link"=>"http://www.mendeley.com/research/susceptibility-neurodegeneration-glaucoma-modified-bax-gene-dosage", "reader_count"=>54, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>2, "Researcher"=>13, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>24, "Student > Postgraduate"=>2, "Student > Master"=>6, "Student > Bachelor"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>2, "Researcher"=>13, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>24, "Student > Postgraduate"=>2, "Student > Master"=>6, "Student > Bachelor"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>7, "Agricultural and Biological Sciences"=>26, "Medicine and Dentistry"=>7, "Neuroscience"=>8, "Veterinary Science and Veterinary Medicine"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>7}, "Neuroscience"=>{"Neuroscience"=>8}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>26}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}, "Unspecified"=>{"Unspecified"=>4}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"United States"=>1, "United Kingdom"=>1, "Malaysia"=>1, "Australia"=>1}, "group_count"=>3}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/962783"], "description"=>"<p>To assess the possibility that <i>Bax</i> deficiency may delay axon degeneration by lessening the glaucomatous insult to which RGCs are exposed, we analyzed IOP at key ages of IOP elevation. (A) The average IOP for each genotype (± SEM) and (B) the actual IOP values recorded. <i>Bax</i> deficiency did not prevent IOP elevation. At both 9 mo and 10.5 mo, the average IOP of both <i>Bax</i><sup>+/−</sup> and <i>Bax</i><sup>−/−</sup> mice was significantly elevated compared to preglaucomatous DBA/2J mice (<i>p</i> < 0.001). The width of the horizontal line (black in [A], gray in [B]) represents the mean IOP ± SEM of a group of wild-type preglaucomatous DBA/2J mice that were 3 mo old. The degree of IOP elevation, however, was altered in <i>Bax</i><sup>−/−</sup> mice. In both 9- and 10.5-mo-old <i>Bax</i><sup>−/−</sup> mice, the average IOP was less than that of <i>Bax</i><sup>+/+</sup> and <i>Bax</i><sup>+/−</sup> mice. This reduction in IOP elevation was significant at 10.5 mo (<i>p</i> < 0.01). The IOP of <i>Bax</i><sup>+/−</sup> mice did not differ from wild type at either 9 or 10.5 mo (<i>p</i> > 0.82). By 12 mo, there was no difference in IOP between mice of any genotype (<i>p</i> > 0.25).</p>", "links"=>[], "tags"=>["deficiency", "iop"], "article_id"=>632753, "categories"=>["Genetics", "Neuroscience", "Cell Biology", "Medicine"], "users"=>["Richard T Libby", "Yan Li", "Olga V Savinova", "Joseph Barter", "Richard S Smith", "Robert W Nickells", "Simon W.M John"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.0010004.g004", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Complete_Bax_Deficiency_Has_a_Protective_Effect_against_IOP_Elevation_/632753", "title"=>"Complete <i>Bax</i> Deficiency Has a Protective Effect against IOP Elevation", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 09:06:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/962555"], "description"=>"<div><p>To assess the effects of <i>Bax</i> deficiency on optic nerve degeneration, we analyzed PPD-stained optic nerve cross sections from <i>Bax</i><sup>+/+</sup> and <i>Bax</i><sup>−/−</sup> mice (<i>n</i> > 49 for each genotype; see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.0010004#s4\" target=\"_blank\">Materials and Methods</a>).</p>\n <p>(A and B) Before the DBA/2J glaucoma damages RGCs, the optic nerves of both <i>Bax</i><sup>+/+</sup> (A) and <i>Bax</i><sup>−/−</sup> mice (B) had a normal organization. The axons appeared healthy with a clear axoplasm and darkly stained myelin sheath.</p>\n <p>(C and D) BAX deficiency did not prevent glaucomatous optic nerve damage. Severe degeneration involving extensive to complete axon loss and scarring occurred in both <i>Bax</i><sup>+/+</sup> (C) and <i>Bax</i><sup>−/−</sup> mice (D). The majority of mice of both genotypes had this severe degree of damage by 12 mo of age. These experiments show that BAX is not required for glaucomatous axon degeneration. Scale bar, 50 μm.</p></div>", "links"=>[], "tags"=>["glaucomatous", "optic"], "article_id"=>632533, "categories"=>["Genetics", "Neuroscience", "Cell Biology", "Medicine"], "users"=>["Richard T Libby", "Yan Li", "Olga V Savinova", "Joseph Barter", "Richard S Smith", "Robert W Nickells", "Simon W.M John"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.0010004.g002", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_BAX_Is_Not_Required_for_Glaucomatous_Optic_Nerve_Degeneration_/632533", "title"=>"BAX Is Not Required for Glaucomatous Optic Nerve Degeneration", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 09:05:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/962896"], "description"=>"<p>BAX deficiency did not prevent glaucomatous axon degeneration. Nevertheless, the beneficial effect on RGC survival raised the possibility that it may have a protective effect on the axon and delay optic nerve damage. To assess this, three investigators masked to genotype determined the severity of optic nerve damage for mice of each <i>Bax</i> genotype at each age (<i>n</i> = 49–71 per genotype at each age; see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.0010004#s4\" target=\"_blank\">Materials and Methods</a>). At 10.5 mo, both <i>Bax</i><sup>+/−</sup> and <i>Bax</i><sup>−/−</sup> mice had significantly less optic nerve damage than <i>Bax<sup>+/+</sup></i> mice. Mild damage was evident in 53% of <i>Bax</i><sup>−/−</sup> and 44% of <i>Bax</i><sup>+/−</sup> optic nerves, compared to only 20% of <i>Bax</i><sup>+/+</sup> (<i>p</i> < 0.001 for both <i>Bax</i><sup>+/−</sup> and <i>Bax</i><sup>−/−</sup> compared to <i>Bax</i><sup>+/+</sup>; Chi<sup>2</sup> test). With disease progression to 12 mo of age, the distribution of optic nerve damage became indistinguishable among mice of different <i>Bax</i> genotypes (<i>p</i> > 0.10). Quantitative assessment of a random subset of nerves assigned each damage level (more than eight of each) demonstrates that the number of axons that remain in optic nerves having each damage level are clearly different (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.0010004#s4\" target=\"_blank\">Materials and Methods</a>).</p>", "links"=>[], "tags"=>["optic", "degeneration", "delayed"], "article_id"=>632857, "categories"=>["Genetics", "Neuroscience", "Cell Biology", "Medicine"], "users"=>["Richard T Libby", "Yan Li", "Olga V Savinova", "Joseph Barter", "Richard S Smith", "Robert W Nickells", "Simon W.M John"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.0010004.g005", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Glaucomatous_Optic_Nerve_Degeneration_Is_Delayed_in_Bax_Deficient_Mice_/632857", "title"=>"Glaucomatous Optic Nerve Degeneration Is Delayed in <i>Bax</i>-Deficient Mice", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 09:07:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/962673"], "description"=>"<div><p>To determine the effects of BAX deficiency on RGC death in glaucoma, we analyzed RGC layer cells at stages with and without glaucomatous optic nerve damage (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.0010004#s4\" target=\"_blank\">Materials and Methods</a>). All shown images are from a similar region of the superior, peripheral retina.</p>\n <p>(A and B) In both <i>Bax<sup>+/+</sup></i> (A) and <i>Bax</i><sup>−/−</sup> (B) mice without glaucomatous optic nerve damage, the retinas appear healthy. The retinas of both genotypes are similar except that <i>Bax</i><sup>−/−</sup> mice have extra RGCs (since BAX is important in normal developmental RGC death [<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.0010004#pgen-0010004-b39\" target=\"_blank\">39</a>]).</p>\n <p>(C and D) In contrast, an obvious difference was evident between the retinas of <i>Bax</i><sup>+/+</sup> and <i>Bax</i><sup>−/−</sup> mice that had all suffered severe glaucomatous damage with 95% or more axon degeneration. As expected, for <i>Bax</i><sup>+/+</sup> retinas (C) from eyes with 95% or more optic nerve axon loss, there was a noticeable decrease in RGC layer cells (compare [C] to [A]). In contrast, retinas from <i>Bax</i><sup>−/−</sup> mice with correspondingly damaged optic nerves (D) had suffered no obvious loss of RGC layer cells (compare [D] to [B]). This suggests that BAX is required for RGC death in DBA/2J glaucoma. As is well established for both RGCs and other neurons, <i>Bax</i><sup>−/−</sup> RGCs that survive without axons have a shrunken morphology [<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.0010004#pgen-0010004-b38\" target=\"_blank\">38</a>,<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.0010004#pgen-0010004-b82\" target=\"_blank\">82</a>]. This is clearly evident in the <i>Bax</i><sup>−/−</sup> glaucomatous mice (D).</p>\n <p>(E) RGC layer cell counts for eyes with 95% or more axon degeneration confirmed that BAX is necessary for RGC death in this glaucoma. To allow comparison between genotypes, the percent of surviving cells is shown (% soma in mice with 95% or more axon loss compared to mice of the same genotype without glaucomatous damage). At 12 mo of age, <i>Bax</i><sup>+/+</sup> mice had 61.4% ± 3.8% of their RGC layer cells remaining, <i>Bax</i><sup>−/−</sup> mice had no appreciable cell loss (101% ± 5.3%). The RGC layer cells of <i>Bax</i><sup>+/−</sup> mice were also protected (89.2% ± 5.7%). The <i>p</i> values comparing differences in cell counts between nonglaucomatous and very severely glaucomatous (≥ 95% axon loss) eyes of the same genotype were: <i>Bax</i><sup>+/+</sup>, <i>p</i> < 0.001; <i>Bax</i><sup>+/−</sup>, <i>p</i> = 0.207; <i>Bax</i><sup>−/−</sup>, <i>p</i> = 0.426. No cell loss was seen in <i>Bax</i><sup>−/−</sup> mice even out to 18 mo (94.8% ± 4.4% cells surviving, <i>p</i> = 0.524 compared to nonglaucomatous <i>Bax</i><sup>−/−</sup> mice). These findings show that BAX gene dosage has an important effect on the susceptibility of RGCs to glaucomatous death. Scale bar, 50 μm.</p></div>", "links"=>[], "tags"=>["deficiency", "prevents", "glaucomatous", "rgc"], "article_id"=>632649, "categories"=>["Genetics", "Neuroscience", "Cell Biology", "Medicine"], "users"=>["Richard T Libby", "Yan Li", "Olga V Savinova", "Joseph Barter", "Richard S Smith", "Robert W Nickells", "Simon W.M John"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.0010004.g003", "stats"=>{"downloads"=>2, "page_views"=>26, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bax_Deficiency_Prevents_Glaucomatous_RGC_Death_/632649", "title"=>"<i>Bax</i> Deficiency Prevents Glaucomatous RGC Death", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 09:06:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/962418"], "description"=>"<div><p>(A–C) A double-labeling assay that identifies fragmented DNA using fluorescently labeled dUTP (A) and detects chromatin condensation by binding of the dye YOYO-1 (B) was used to assess the presence of these hallmarks of apoptosis in glaucomatous DBA/2J eyes at 10–11 mo of age (a time when many RGCs die). A cell in the retinal ganglion cell layer (GCL, arrowhead) has both of these features of apoptosis as indicated by double labeling (C). INL, inner nuclear layer.</p>\n <p>(D–F) Electron microscopy provided further evidence for apoptosis. (D) An example of a healthy RGC. (E) Chromatin condensation (a hallmark of apoptosis) along the inner surface of the nuclear envelope in a ganglion cell (arrows). The internal limiting membrane of the retina is indicated by arrowheads. (F) An apoptotic body in the ganglion cell layer (arrows) containing a nuclear fragment with prominent condensed chromatin (asterisk) and other cell remnants.</p>\n <p>(G) A TUNEL assay (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.0010004#s4\" target=\"_blank\">Materials and Methods</a>) was used to assess the prevalence of cell death at different ages. TUNEL labeling was not detected at 7 mo (an age prior to glaucomatous cell death) and peaked at 10–13 mo, when most RGCs die. No TUNEL-positive cells were detected in nonglaucomatous, age-matched control mice. These results support an important role of apoptosis in RGC death in spontaneous glaucoma. Scale bar, 1 μm.</p></div>", "links"=>[], "tags"=>["rgcs"], "article_id"=>632396, "categories"=>["Genetics", "Neuroscience", "Cell Biology", "Medicine"], "users"=>["Richard T Libby", "Yan Li", "Olga V Savinova", "Joseph Barter", "Richard S Smith", "Robert W Nickells", "Simon W.M John"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.0010004.g001", "stats"=>{"downloads"=>2, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dying_RGCs_Have_Characteristic_Features_of_Apoptosis_/632396", "title"=>"Dying RGCs Have Characteristic Features of Apoptosis", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 09:04:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/963003"], "description"=>"<p>To help distinguish between the likely roles of mechanical axon insult and excitotoxicity in cell death induction in spontaneous glaucoma, we subjected preglaucomatous DBA/2J mice of each <i>Bax</i> genotype to either controlled optic nerve crush or NMDA-mediated excitotoxicity. For controlled crush and NMDA, the percent RGC survival in the manipulated eye compared to the contralateral control eye is shown. For ease of comparison, the data for glaucomatous damage are the same as shown in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.0010004#pgen-0010004-g003\" target=\"_blank\">Figure 3</a>. In contrast to the spontaneous glaucoma, NMDA-mediated RGC death is not dependent on BAX, as evident by the complete lack of protection from death in <i>Bax</i><sup>−/−</sup> mice. As for the spontaneous glaucoma, RGC death induced by controlled optic nerve crush was completely dependent on BAX and prevented in both <i>Bax</i><sup>+/−</sup> and <i>Bax</i><sup>−/−</sup> mice. Overall, the effects of BAX in the face of spontaneous glaucoma and controlled crush were remarkably similar.</p>", "links"=>[], "tags"=>["axon", "bax-dependent", "rgc"], "article_id"=>632957, "categories"=>["Genetics", "Neuroscience", "Cell Biology", "Medicine"], "users"=>["Richard T Libby", "Yan Li", "Olga V Savinova", "Joseph Barter", "Richard S Smith", "Robert W Nickells", "Simon W.M John"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.0010004.g006", "stats"=>{"downloads"=>2, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mechanical_Axon_Insult_but_Not_Excitotoxicity_Induces_BAX_Dependent_RGC_Death_/632957", "title"=>"Mechanical Axon Insult, but Not Excitotoxicity, Induces BAX-Dependent RGC Death", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 09:08:20"}

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