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Article ; Online: Acriflavine, a HIF-1 inhibitor, preserves vision in an experimental autoimmune encephalomyelitis model of optic neuritis.

Anders, Jeffrey J / Elwood, Benjamin W / Kardon, Randy H / Gramlich, Oliver W

2023 Volume 14, Page(s) 1271118

Abstract: Introduction: Optic neuritis (ON) is often an early sign of multiple sclerosis (MS), and recent studies show a link between HIF-1 pathway activation and inflammation. This study aimed to determine if inhibition of the HIF-1 pathway using the HIF-1a ... ...

Abstract	Introduction: Optic neuritis (ON) is often an early sign of multiple sclerosis (MS), and recent studies show a link between HIF-1 pathway activation and inflammation. This study aimed to determine if inhibition of the HIF-1 pathway using the HIF-1a antagonist acriflavine (ACF) can reduce clinical progression and rescue the ocular phenotype in an experimental autoimmune encephalomyelitis (EAE) ON model. Methods: EAE-related ON was induced in 60 female C57BL/6J mice by immunization with MOG33-55, and 20 EAE mice received daily systemic injections of ACF at 5 mg/kg. Changes in the visual function and structure of ACF-treated EAE mice were compared to those of placebo-injected EAE mice and naïve control mice. Results: ACF treatment improved motor-sensory impairment along with preserving visual acuity and optic nerve function. Analysis of retinal ganglion cell complex alsoshowed preserved thickness correlating with increased survival of retinal ganglion cells and their axons. Optic nerve cell infiltration and magnitude of demyelination were decreased in ACF-treated EAE mice. Subsequent in vitro studies revealed improvements not only attributed to the inhibition of HIF-1 butalso to previously unappreciated interaction with the eIF2a/ATF4 axis in the unfolded protein response pathway. Discussion: This study suggests that ACF treatment is effective in an animal model of MS via its pleiotropic effects on the inhibition of HIF-1 and UPR signaling, and it may be a viable approach to promote rehabilitation in MS.
MeSH term(s)	Female ; Animals ; Mice ; Encephalomyelitis, Autoimmune, Experimental/drug therapy ; Encephalomyelitis, Autoimmune, Experimental/metabolism ; Acriflavine/pharmacology ; Acriflavine/therapeutic use ; Acriflavine/metabolism ; Mice, Inbred C57BL ; Optic Neuritis/drug therapy ; Retinal Ganglion Cells/metabolism ; Multiple Sclerosis/metabolism
Chemical Substances	Acriflavine (1T3A50395T)
Language	English
Publishing date	2023-10-23
Publishing country	Switzerland
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2023.1271118
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Display of Data.

Ledolter, Johannes / Gramlich, Oliver W / Kardon, Randy H

Investigative ophthalmology & visual science

2020 Volume 61, Issue 6, Page(s) 25

MeSH term(s)	Animals ; Biomedical Research/statistics & numerical data ; Humans ; Ophthalmology ; Retinal Diseases/diagnosis ; User-Computer Interface
Language	English
Publishing date	2020-06-10
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	391794-0
ISSN	1552-5783 ; 0146-0404
ISSN (online)	1552-5783
ISSN	0146-0404
DOI	10.1167/iovs.61.6.25
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Article ; Online: Parametric Statistical Inference for Comparing Means and Variances.

Ledolter, Johannes / Gramlich, Oliver W / Kardon, Randy H

Investigative ophthalmology & visual science

2020 Volume 61, Issue 8, Page(s) 25

Abstract: Purpose: The purpose of this tutorial is to provide visual scientists with various approaches for comparing two or more groups of data using parametric statistical tests, which require that the distribution of data within each group is normal (Gaussian). ...

Abstract	Purpose: The purpose of this tutorial is to provide visual scientists with various approaches for comparing two or more groups of data using parametric statistical tests, which require that the distribution of data within each group is normal (Gaussian). Non-parametric tests are used for inference when the sample data are not normally distributed or the sample is too small to assess its true distribution. Methods: Methods are reviewed using retinal thickness, as measured by optical coherence tomography (OCT), as an example for comparing two or more group means. The following parametric statistical approaches are presented for different situations: two-sample t-test, Analysis of Variance (ANOVA), paired t-test, and the analysis of repeated measures data using a linear mixed-effects model approach. Results: Analyzing differences between means using various approaches is demonstrated, and follow-up procedures to analyze pairwise differences between means when there are more than two comparison groups are discussed. The assumption of equal variance between groups and methods to test for equal variances are examined. Examples of repeated measures analysis for right and left eyes on subjects, across spatial segments within the same eye (e.g. quadrants of each retina), and over time are given. Conclusions: This tutorial outlines parametric inference tests for comparing means of two or more groups and discusses how to interpret the output from statistical software packages. Critical assumptions made by the tests and ways of checking these assumptions are discussed. Efficient study designs increase the likelihood of detecting differences between groups if such differences exist. Situations commonly encountered by vision scientists involve repeated measures from the same subject over time, measurements on both right and left eyes from the same subject, and measurements from different locations within the same eye. Repeated measurements are usually correlated, and the statistical analysis needs to account for the correlation. Doing this the right way helps to ensure rigor so that the results can be repeated and validated.
MeSH term(s)	Analysis of Variance ; Biometry/methods ; Diagnostic Techniques, Ophthalmological ; Humans ; Normal Distribution ; Ophthalmology/methods ; Reproducibility of Results ; Retina/diagnostic imaging ; Statistics as Topic/methods ; Statistics as Topic/standards ; Tomography, Optical Coherence/methods ; Tomography, Optical Coherence/statistics & numerical data
Language	English
Publishing date	2020-07-21
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	391794-0
ISSN	1552-5783 ; 0146-0404
ISSN (online)	1552-5783
ISSN	0146-0404
DOI	10.1167/iovs.61.8.25
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Article ; Online: Immune Responses in the Glaucomatous Retina: Regulation and Dynamics.

Shestopalov, Valery I / Spurlock, Markus / Gramlich, Oliver W / Kuehn, Markus H

Cells

2021 Volume 10, Issue 8

Abstract: Glaucoma is a multifactorial disease resulting in progressive vision loss due to retinal ganglion cell (RGC) dysfunction and death. Early events in the pathobiology of the disease include oxidative, metabolic, or mechanical stress that acts upon RGC, ... ...

Abstract	Glaucoma is a multifactorial disease resulting in progressive vision loss due to retinal ganglion cell (RGC) dysfunction and death. Early events in the pathobiology of the disease include oxidative, metabolic, or mechanical stress that acts upon RGC, causing these to rapidly release danger signals, including extracellular ATP, resulting in micro- and macroglial activation and neuroinflammation. Danger signaling also leads to the formation of inflammasomes in the retina that enable maturation of proinflammatory cytokines such IL-1β and IL-18. Chronic neuroinflammation can have directly damaging effects on RGC, but it also creates a proinflammatory environment and compromises the immune privilege of the retina. In particular, continuous synthesis of proinflammatory mediators such as TNFα, IL-1β, and anaphylatoxins weakens the blood-retina barrier and recruits or activates T-cells. Recent data have demonstrated that adaptive immune responses strongly exacerbate RGC loss in animal models of the disease as T-cells appear to target heat shock proteins displayed on the surface of stressed RGC to cause their apoptotic death. It is possible that dysregulation of these immune responses contributes to the continued loss of RGC in some patients.
MeSH term(s)	Adenosine Triphosphate/metabolism ; Cytokines/metabolism ; Glaucoma/immunology ; Glaucoma/metabolism ; Glaucoma/pathology ; Humans ; Immunity, Innate ; Inflammasomes/metabolism ; Retinal Ganglion Cells/metabolism ; Signal Transduction
Chemical Substances	Cytokines ; Inflammasomes ; Adenosine Triphosphate (8L70Q75FXE)
Language	English
Publishing date	2021-08-03
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	2661518-6
ISSN	2073-4409 ; 2073-4409
ISSN (online)	2073-4409
ISSN	2073-4409
DOI	10.3390/cells10081973
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Article ; Online: Systemic Treatment with Pioglitazone Reverses Vision Loss in Preclinical Glaucoma Models.

Zeng, Huilan / Dumitrescu, Alina V / Wadkins, David / Elwood, Benjamin W / Gramlich, Oliver W / Kuehn, Markus H

Biomolecules

2022 Volume 12, Issue 2

Abstract: Neuroinflammation significantly contributes to the pathophysiology of several neurodegenerative diseases. This is also the case in glaucoma and may be a reason why many patients suffer from progressive vision loss despite maximal reduction in intraocular ...

Abstract	Neuroinflammation significantly contributes to the pathophysiology of several neurodegenerative diseases. This is also the case in glaucoma and may be a reason why many patients suffer from progressive vision loss despite maximal reduction in intraocular pressure. Pioglitazone is an agonist of the peroxisome proliferator-activated receptor gamma (PPARγ) whose pleiotrophic activities include modulation of cellular energy metabolism and reduction in inflammation. In this study we employed the DBA2/J mouse model of glaucoma with chronically elevated intraocular pressure to investigate whether oral low-dose pioglitazone treatment preserves retinal ganglion cell (RGC) survival. We then used an inducible glaucoma model in C57BL/6J mice to determine visual function, pattern electroretinographs, and tracking of optokinetic reflex. Our findings demonstrate that pioglitazone treatment does significantly protect RGCs and prevents axonal degeneration in the glaucomatous retina. Furthermore, treatment preserves and partially reverses vision loss in spite of continuously elevated intraocular pressure. These data suggest that pioglitazone may provide treatment benefits for those glaucoma patients experiencing continued vision loss.
MeSH term(s)	Animals ; Glaucoma/metabolism ; Humans ; Intraocular Pressure ; Mice ; Mice, Inbred C57BL ; Pioglitazone/pharmacology ; Pioglitazone/therapeutic use ; Retinal Ganglion Cells/metabolism
Chemical Substances	Pioglitazone (X4OV71U42S)
Language	English
Publishing date	2022-02-09
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2701262-1
ISSN	2218-273X ; 2218-273X
ISSN (online)	2218-273X
ISSN	2218-273X
DOI	10.3390/biom12020281
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Article ; Online: Mouse model of radiation retinopathy reveals vascular and neuronal injury.

Liu, Emily / Tamplin, Michelle R / Rosius, Jurnie / Tedeschi, Thomas R / Gramlich, Oliver W / Kardon, Randy H / Grumbach, Isabella M

Experimental eye research

2023 Volume 238, Page(s) 109729

Abstract: Purpose: To characterize the neuronal and vascular pathology in vivo and in vitro in a mouse model of radiation retinopathy.: Methods: C57Bl/6J mice underwent cranial irradiation with 12 Gy and in vivo imaging by optical coherence tomography and of ... ...

Abstract	Purpose: To characterize the neuronal and vascular pathology in vivo and in vitro in a mouse model of radiation retinopathy. Methods: C57Bl/6J mice underwent cranial irradiation with 12 Gy and in vivo imaging by optical coherence tomography and of relative blood flow velocity by laser speckle flowgraphy for up to 3-6 months after irradiation. Retinal architecture, vascular density and leakage and apoptosis were analyzed by histology and immunohistochemistry before irradiation or at 10, 30, 240, and 365 days after treatment. Results: The vascular density decreased in the plexiform layers starting at 30 days after irradiation. No impairment in retinal flow velocity was seen. Subtle perivascular leakage was present at 10 days, in particular in the outer plexiform layer. This corresponded to increased width of this layer. However, no significant change in the retinal thickness was detected by OCT-B scans. At 365 days after irradiation, the nuclear density was significantly reduced compared to baseline. Apoptosis was detected at 30 days and less prominent at 365 days. Conclusions: By histology, vascular leakage at 10 days was followed by increased neuronal apoptosis and loss of neuronal and vascular density. However, in vivo imaging approaches that are commonly used in human patients did not detect pathology in mice.
MeSH term(s)	Humans ; Mice ; Animals ; Fluorescein Angiography ; Retina ; Retinal Vessels/pathology ; Neurons ; Disease Models, Animal ; Radiation Injuries/pathology ; Retinal Diseases/etiology ; Retinal Diseases/pathology ; Tomography, Optical Coherence/methods
Language	English
Publishing date	2023-12-03
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't
ZDB-ID	80122-7
ISSN	1096-0007 ; 0014-4835
ISSN (online)	1096-0007
ISSN	0014-4835
DOI	10.1016/j.exer.2023.109729
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Article ; Online: Early Functional Impairment in Experimental Glaucoma Is Accompanied by Disruption of the GABAergic System and Inceptive Neuroinflammation.

Gramlich, Oliver W / Godwin, Cheyanne R / Wadkins, David / Elwood, Benjamin W / Kuehn, Markus H

International journal of molecular sciences

2021 Volume 22, Issue 14

Abstract: Glaucoma is a leading cause of irreversible blindness worldwide, and increased intraocular pressure (IOP) is a major risk factor. We aimed to determine if early functional and molecular differences in the glaucomatous retina manifest before significant ... ...

Abstract	Glaucoma is a leading cause of irreversible blindness worldwide, and increased intraocular pressure (IOP) is a major risk factor. We aimed to determine if early functional and molecular differences in the glaucomatous retina manifest before significant retinal ganglion cell (RGC) loss is apparent. Adenoviral vectors expressing a pathogenic form of myocilin (Ad5.MYOC) were used to induce IOP elevation in C57BL/6 mice. IOP and pattern electroretinograms (pERG) were recorded, and retinas were prepared for RNA sequencing, immunohistochemistry, or to determine RGC loss. Ocular injection of Ad5.MYOC leads to reliable IOP elevation, resulting in significant loss of RGC after nine weeks. A significant decrease in the pERG amplitude was evident in eyes three weeks after IOP elevation. Retinal gene expression analysis revealed increased expression for 291 genes related to complement cascade, inflammation, and antigen presentation in hypertensive eyes. Decreased expression was found for 378 genes associated with the γ-aminobutyric acid (GABA)ergic and glutamatergic systems and axon guidance. These data suggest that early functional changes in RGC might be due to reduced GABA
MeSH term(s)	Animals ; Cytoskeletal Proteins/genetics ; Cytoskeletal Proteins/metabolism ; Disease Models, Animal ; Eye Proteins/genetics ; Eye Proteins/metabolism ; Female ; GABAergic Neurons/metabolism ; GABAergic Neurons/pathology ; Gene Expression Regulation ; Glaucoma/etiology ; Glaucoma/metabolism ; Glaucoma/pathology ; Glycoproteins/genetics ; Glycoproteins/metabolism ; Inflammation/metabolism ; Inflammation/pathology ; Intraocular Pressure ; Male ; Mice ; Mice, Inbred C57BL ; Retinal Ganglion Cells/metabolism ; Retinal Ganglion Cells/pathology ; gamma-Aminobutyric Acid/metabolism
Chemical Substances	Cytoskeletal Proteins ; Eye Proteins ; Glycoproteins ; trabecular meshwork-induced glucocorticoid response protein ; gamma-Aminobutyric Acid (56-12-2)
Language	English
Publishing date	2021-07-15
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms22147581
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Article ; Online: Targeting Cholesterol Homeostasis Improves Recovery in Experimental Optic Neuritis.

Godwin, Cheyanne R / Anders, Jeffrey J / Cheng, Lin / Elwood, Benjamin W / Kardon, Randy H / Gramlich, Oliver W

Biomolecules

2022 Volume 12, Issue 10

Abstract: Acute optic neuritis (ON) is a common cause of vision loss and is often associated with multiple sclerosis (MS). Cholesterol recycling has been identified as a key limiting factor in recovery after demyelination events. Thus, the purpose of our study was ...

Abstract	Acute optic neuritis (ON) is a common cause of vision loss and is often associated with multiple sclerosis (MS). Cholesterol recycling has been identified as a key limiting factor in recovery after demyelination events. Thus, the purpose of our study was to determine if the augmentation of cholesterol transport by gentisic acid (GA) benefits retinal ganglion cell (RGC) development and myelination in organoid systems and enables the recovery of the ocular phenotype upon systemic GA treatment in a MOG-induced experimental autoimmune encephalomyelitis (EAE) ON model. The retinal organoids treated with GA demonstrate an accelerated maturation when compared to the conventionally derived organoids, which was evidenced by the improved organization of Brn3a-GFP<sup>+</sup>RGC and increased synaptogenesis. A GA supplementation in brain organoids leads to a 10-fold increase in NG2 and Olig2 expression. Weekly GA injections of EAE mice significantly lessened motor-sensory impairment, protected amplitudes in pattern electroretinogram recordings, and preserved visual acuity over the study period of 56 days. Furthermore, GA-treated EAE mice revealed diminished GCL/IPL complex thinning when compared to the untreated EAE mice. An optic nerve histopathology revealed less severe grades of demyelination in the GA-treated EAE cohort and fewer infiltrating cells were observed. Interventions to improve cholesterol homeostasis may be a viable approach to promoting the rehabilitation of MS patients.
MeSH term(s)	Mice ; Animals ; Optic Neuritis/drug therapy ; Optic Neuritis/etiology ; Optic Neuritis/pathology ; Encephalomyelitis, Autoimmune, Experimental/drug therapy ; Encephalomyelitis, Autoimmune, Experimental/pathology ; Retinal Ganglion Cells/metabolism ; Optic Nerve ; Multiple Sclerosis/pathology ; Homeostasis ; Mice, Inbred C57BL
Language	English
Publishing date	2022-10-07
Publishing country	Switzerland
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2701262-1
ISSN	2218-273X ; 2218-273X
ISSN (online)	2218-273X
ISSN	2218-273X
DOI	10.3390/biom12101437
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Article ; Online: Immune responses in mice after blast-mediated traumatic brain injury TBI autonomously contribute to retinal ganglion cell dysfunction and death.

Harper, Matthew M / Gramlich, Oliver W / Elwood, Benjamin W / Boehme, Nickolas A / Dutca, Laura M / Kuehn, Markus H

Experimental eye research

2022 Volume 225, Page(s) 109272

Abstract: Purpose: The purpose of this study was to examine the role of the immune system and its influence on chronic retinal ganglion cell (RGC) dysfunction following blast-mediated traumatic brain injury (bTBI).: Methods: C57BL/6J and B6.129S7-Rag1: ... ...

Abstract	Purpose: The purpose of this study was to examine the role of the immune system and its influence on chronic retinal ganglion cell (RGC) dysfunction following blast-mediated traumatic brain injury (bTBI). Methods: C57BL/6J and B6.129S7-Rag1 Results: Analysis of the PERG showed a decreased amplitude two months post-AT that persisted for the duration of the study in AT-TBI mice. We also observed a significant decrease in the retinal thickness of AT-TBI mice two months post-AT compared to sham, but not at four or six months post-AT. The OMR response was significantly decreased in AT-TBI mice 5- and 6-months post-AT. BRN3A staining showed a loss of RGCs in AT-TBI and AT-Rag Conclusion: These results suggest that the immune system contributes to chronic RGC dysfunction following bTBI.
MeSH term(s)	Mice ; Animals ; Retinal Ganglion Cells/pathology ; Mice, Inbred C57BL ; Disease Models, Animal ; Brain Injuries, Traumatic/complications ; Immunity
Language	English
Publishing date	2022-10-06
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	80122-7
ISSN	1096-0007 ; 0014-4835
ISSN (online)	1096-0007
ISSN	0014-4835
DOI	10.1016/j.exer.2022.109272
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Article ; Online: T and B Lymphocyte Deficiency in Rag1-/- Mice Reduces Retinal Ganglion Cell Loss in Experimental Glaucoma.

Gramlich, Oliver W / Godwin, Cheyanne R / Heuss, Neal D / Gregerson, Dale S / Kuehn, Markus H

Investigative ophthalmology & visual science

2020 Volume 61, Issue 14, Page(s) 18

Abstract: Purpose: We previously demonstrated that passive transfer of lymphocytes from glaucomatous mice induces retinal ganglion cell (RGC) damage in recipient animals, suggesting a role for immune responses in the multifactorial pathophysiology of glaucoma. ... ...

Abstract	Purpose: We previously demonstrated that passive transfer of lymphocytes from glaucomatous mice induces retinal ganglion cell (RGC) damage in recipient animals, suggesting a role for immune responses in the multifactorial pathophysiology of glaucoma. Here we evaluate whether absence of an adaptive immune response reduces RGC loss in glaucoma. Methods: Elevated intraocular pressure (IOP) was induced in one eye of C57BL/6J (B6) or T- and B-cell-deficient Rag1-/- knockout mice. After 16 weeks RGC density was determined in both the induced and the normotensive contralateral eyes. Data were compared to mice having received injections of "empty" vector (controls). The number of extravascular CD3+ cells in the retinas was determined using FACS. Results: Retinas of eyes with elevated IOP contain significantly more extravasated CD3+ cells than control retinas (46.0 vs. 27.1, P = 0.025). After 16 weeks of elevated IOP the average RGC density in B6 mice decreased by 20.7% (P = 1.9 × 10-4). In contrast, RGC loss in Rag1-/- eyes with elevated IOP was significantly lower (10.3%, P = 0.006 vs. B6). RGC loss was also observed in the contralateral eyes of B6 mice, despite the absence of elevated IOP in those eyes (10.1%; P = 0.008). In RAG1-/- loss in the contralateral eyes was minimal (3.1%) and significantly below that detected in B6 (P = 0.02). Conclusions: Our findings demonstrate that T Rag1-/- mice are significantly protected from glaucomatous RGC loss. In this model, lymphocyte activity contributes to approximately half of all RGC loss in eyes with elevated IOP and to essentially all loss observed in normotensive contralateral eyes.
MeSH term(s)	Animals ; B-Lymphocytes/immunology ; B-Lymphocytes/pathology ; Cell Count ; Disease Models, Animal ; Female ; Flow Cytometry ; Glaucoma/immunology ; Glaucoma/pathology ; Homeodomain Proteins/physiology ; Intraocular Pressure ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Retinal Ganglion Cells/pathology ; T-Lymphocytes/immunology ; T-Lymphocytes/pathology
Chemical Substances	Homeodomain Proteins ; RAG-1 protein (128559-51-3)
Language	English
Publishing date	2020-12-08
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	391794-0
ISSN	1552-5783 ; 0146-0404
ISSN (online)	1552-5783
ISSN	0146-0404
DOI	10.1167/iovs.61.14.18
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