PMC:4277126 / 53850-67981 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/4277126","sourcedb":"PMC","sourceid":"4277126","source_url":"http://www.ncbi.nlm.nih.gov/pmc/4277126","text":"Effects of LBPs on experimental glaucoma and I/R-induced retinal injury\nRetinal I/R injury is associated with many ocular diseases, including glaucoma, amaurosis, fugax, and diabetic retinopathy. Oxidative injury is one of the complications after retinal I/R injuries accompanied by retinal swelling, disrupted blood–retinal barrier (BRB), neuronal cell death, and glial cell activation.76 The role of BRB is to maintain the homeostatic condition of retinal microenvironment and exclude harmful substance getting into the retina. The outer barrier is formed by the retinal pigment epithelium, separating the outer retina from the choroid; and the inner BRB is formed by the tight junctions of the vascular endothelial cells and sheathed by the Muller cell processes. In many ocular diseases including ischemic retinal vein/artery occlusion and diabetic retinopathy, breakdown of the inner BRB increases retinal vascular permeability, resulting in retinal edema and cell death. Glaucoma, the leading cause of vision loss in the world, is associated with the loss of retinal ganglion cells (RGCs) and their axons. The secondary damage is considered to be the major cause of RGC loss in glaucoma. High intraocular pressure-induced retinal I/R is a commonly used model for retinal ischemic studies. This method produces global ischemia via the obstruction of both retinal and choroidal circulation, contributing to pathological features that are nearly identical to those observed in patients after a central retinal artery occlusion or ophthalmic artery occlusion. LBPs have shown protective effects against I/R-induced retinal injury in animal studies, and they protect RGCs, retinal vasculature, and BRB in animal models.77–85\n\nExperimental glaucoma: acute ocular hypertension\nAcute ocular hypertension (AOH) is a well-established animal model for producing retinal degeneration, which has been used to investigate the pathogenesis of RGC death and possible therapeutic interventions for neuroprotection. Several animal studies have shown the protective effects of LBPs against AOH-induced retinal injury.78,79\nMi et al79 evaluated the protective effect of LBPs on retinal I/R injury in male C57BL/6N mice. The mice were treated in unilateral eye for 1 hour by introducing 90 mmHg ocular pressure to induce AOH. The animals were administered with 1 mg/kg LBPs daily from 7 days before the I/R insult till sacrifice at either day 4 or day 7 post-insult. The neuroprotective effects of LBPs on RGCs and BRB were assessed. In control AOH retina, loss of RGCs, thinning of inner retinal layer thickness, increased immunoglobulin G (IgG) leakage, broken tight junctions, and decreased density of retinal blood vessels were observed. However, in LBP-treated AOH retina, there was less loss of RGCs with thinning of inner retinal layer thickness, IgG leakage, more continued structure of tight junctions associated with higher level of occludin protein, and the recovery of the blood vessel density when compared with vehicle-treated AOH retina.79 Moreover, LBPs provide neuroprotection by downregulating advanced glycation end products and their receptors, endothelin-1, and amyloid-β (Aβ) in the retina, as well as their related signaling pathways, which was related to inhibiting vascular damages and the neuronal degeneration in AOH insults. These data suggest that LBPs could prevent damage to RGCs from AOH-induced ischemic injury and that LBPs may be a potential treatment for vascular-related retinopathy.\nHe et al78 further explored the mechanisms for LBP-mediated protective effects on AOH-induced retinal injury in eight-week-old male Sprague–Dawley rats. The left eye of rats was subject to increased intraocular pressure of 130 mmHg for 60 minutes using a physiological saline reservoir to induce AOH. Successful achievement of retinal ischemia was confirmed by the collapse of the central retinal artery and the whitening of the iris during the elevation of intraocular pressure. About 1 mg/kg/day LBPs was administered by gavage for 7 days before AOH procedure. The protective effects of LBPs were evaluated by quantifying ganglion cell and amacrine cell survival and by measuring cellular apoptosis in the retinal layers. In addition, the expression of heme oxygenase-1 (HO-1) was examined using Western blotting and immunofluorescence analyses. The redox-sensitive transcription nuclear factor erythroid 2-related factor (Nrf2) in cytosol and nucleus was measured using immunofluorescent staining. HO-1 is the rate-limiting enzyme that catalyzes the degradation of heme into biliverdin, carbon monoxide, and iron, and is one of the phase II detoxifying enzymes and antioxidants that are closely regulated by Nrf2. Increased apoptosis and decreased number of viable cells were observed in the ganglion cell layer (GCL) and inner nuclear layer (INL) in the I/R retina, which were reversed by LBP treatment.78 In LBP-pretreated rats, the rate of RGC loss was delayed and more than 50% of RGCs remained viable in the retina 7 days after the ischemic insult. When compared with the vehicle-treated I/R retina, the LBP-treated I/R retina had an increase in the number of choline acetyltransferase-positive retinal amacrine cells. The retinal level of radical oxygen species (ROS) was decreased by LBP pretreatment in I/R mice. Similar to the specific Nrf2 activator, sulforaphane, LBP pretreatment significantly increased the number of RGCs with nuclear translocation of Nrf2 in I/R retina.78 Retinal HO-1 expression determined by immunofluorescent staining and immunoblotting was also upregulated by LBPs. Inhibition of HO-1 activity by zinc protoporphyrin at 20 mg/kg abolished LBP-induced protective effects in the retina after I/R.78 The data demonstrate that LBPs elicit retino- and neuro-protective effects via the activation of Nrf2 and upregulation of HO-1 expression.\n\nExperimental glaucoma: chronic ocular hypertension\nLBPs have shown potent neuroprotective effects by reducing the loss of RGCs in chronic ocular hypertension (COH) models.82–84 Chan et al82 investigated whether oral administration of LBPs protected RGCs against COH in Sprague–Dawley rats. COH in rats was induced by laser photocoagulation of episcleral and limbal veins. LBPs significantly decreased the loss of RGCs, although elevated intraocular pressure was not significantly altered. Around 70% of RGC death in COH rats was retarded with a short-term feeding of LBPs and this neuroprotective effect was maintained for up to 4 weeks.82 Rats treated with 1 mg/kg LBPs almost abolished COH-induced loss of RGCs. These results show the therapeutic benefits of L. barbarum against neurodegeneration in the retina of rat COH model.\nIt is believed that the neuroprotective effect of LBPs in COH rats is partly due to modulating the activation of microglia, as manipulating the activation state of microglia is beneficial for neuron protection. This effect has been observed by Chiu et al83 who used multiphoton confocal microscopy to investigate morphological changes of microglia in whole-mounted retinas of COH rats. Retinas under COH displayed slightly activated microglia. Administration of 1–100 mg/kg LBPs elicited moderately activated microglia in the inner retina with ramified appearance but thicker and focally enlarged processes. When activation of microglia was reduced by intravitreal injection of macrophage/microglia inhibitory factor, the neuroprotective effect of 10 mg/kg LBP was decreased.83 There is evidence from a proteomic study84 that the prosurvival effect of LBPs on rat RGCs in COH may be mediated by an increase in upregulation of βB2 crystalline, which is a neuroprotective agent.\n\nRetinal degeneration\nIn outer retina, LBPs have been shown to decrease apoptosis in photoreceptors of rd1 mice with photoreceptor degeneration.85 Mice homozygous for the rd1 mutation have an early onset severe retinal degeneration due to a murine viral insert and a second nonsense mutation in exon 7 of the Pde6b gene in all mouse strains with the rd1 mutation. LBP treatment increased GPx activity and GSH levels and decreased cysteine concentrations in rd1 retinas.85 These data suggest that the prosurvival effects of LBPs on photoreceptors in rd1 mouse retina are mainly via reduction of oxidative stress.\n\nMiddle cerebral artery occlusion-induced ischemic retinal injury\nLi et al77 investigated the effects of intragastric LBP pretreatment by gavage on the retinal injuries induced by middle cerebral artery occlusion (MCAO) in C57BL/6N male mice. Prior to induction of MCAO, mice were treated orally with 1 mg/kg LBPs once a day for 1 week. Retinal ischemia was maintained for 2 hours, after which the filament was pulled out to allow reperfusion for 22 hours. Viable cells in GCL of the central and peripheral retina were counted and retinal swelling was evaluated by measuring the inner retinal thickness from the inner limiting membrane to INL. Expression levels of glial fibrillary acidic protein (GFAP), aquaporin-4 (AQP4), poly(ADP-ribose) (PAR), and nitrotyrosine (NT) in mouse retina were determined by immunohistochemistry. The integrity of BRB was assessed by measuring IgG extravasation. The study showed that the number of viable cells in GCL in the central and the peripheral retina was significantly higher in the LBP-treated I/R mice compared with that in the vehicle-treated I/R mice.77 There was a decrease in inner retinal thickness of the central retina in the LBP-treated I/R mice when compared with the vehicle-treated I/R mice. Fewer apoptotic cells were found in GCL and INL of the LBP-treated I/R retina when compared with that of the vehicle-treated I/R retina. Protein kinase C-alpha expression (a marker for rod bipolar cells) in the LBP-treated I/R retina was more when compared with that in the vehicle-treated I/R retina.77 The expression of calretinin by amacrine cells was higher in LBP-treated I/R retina compared with that of the vehicle-treated I/R retina. There were more neuronal NO synthase-expressing amacrine cells found in the LBP-treated I/R retina compared with the vehicle-treated I/R retina. Disruption of BRB leads to swelling of astrocytes and Muller cells processes associated with the activation of GFAP and AQP4 under ischemic conditions. The immunoreactivity of GFAP in astrocytes in GCL was reduced in LBP-treated I/R retina compared with that of the vehicle-treated I/R retina. The immunoreactivity of AQP4 expressed in the astrocytes of inner limiting membrane and INL was significantly lower in LBP-treated I/R retina compared with the vehicle-treated I/R retina. LBP treatment also reduced the number of retinal blood vessels with IgG leakage, nuclear translocation of PAR expression, and NT expression.77 The breakdown of DNA strands activates the nuclear enzyme poly(ADP-ribose) polymerase (PARP) to produce PAR. Free radical formation facilitates NO production, which reacts with superoxide to from peroxynitrite, a strong oxidant that leads to nitration of tyrosine residues of cells to form NT. These results show that pretreatment of mice with LBPs effectively protected the retina from RGC apoptosis, retinal swelling, glial cell activation, BRB disruption, and oxidative stress.\n\nComplete or partial optic nerve transaction\nThe partial optic nerve transection (PONT) model allows good separation of secondary degeneration from the directly injured RGCs. Li et al80 investigated the protective effects of LBPs on RGCs in Sprague–Dawley rats subject to complete or partial optic nerve transection (CONT or PONT). Rats were administered with 1 mg/kg/day LBPs for 7 days before surgery until sacrificed at different time points. The expression levels of several proteins related to inflammation, oxidative stress, and Jun N-terminal kinases (JNK)/c-Jun pathway were determined using Western blotting assay. LBPs did not delay primary degeneration of RGCs after either CONT or PONT, but delayed secondary degeneration of RGCs after PONT.80 These results demonstrate that LBPs decrease secondary degeneration of RGCs by inhibiting oxidative stress and the JNK/c-Jun pathway and by transiently increasing the expression of insulin-like growth factor-1 (IGF-1).\nChu et al also investigated the retinal protective effects of LBPs in rat PONT model when the multifocal electroretinograms (mfERGs) were recorded in Sprague–Dawley rats.81 The mfERG allows for recording multiple local retinal responses within a short time period, and it is widely used in glaucoma investigation in animal and human studies. The rats were administered 1 mg/kg LBP via a nasogastric tube every day until euthanization. The PONT surgery was performed at day 7 after start of LBP dosing. As with the primate mfERG response, the waveform in rats contains a trough (N1) at around 25 milliseconds, followed by a major positive component (P1) at around 55 milliseconds, and a photopic negative response (PhNR) that can be observed at around 75 milliseconds.81 The topographical mfERG response demonstrated a stronger retinal function along the visual streak with a peak in the nasal field in both conditions with and without PONT. After administering 1 mg/kg LBP a week prior to PONT surgery, the rats showed increased N1 responses, P1 responses, and PhNRs, especially in the inferior retina when compared with the control group. The N1 amplitudes were significantly increased at week 4 after PONT except in the superior regions.81 The P1 amplitude in the far superior region showed a significant reduction 1 week after PONT, but then returned to the normal range. P1 amplitudes remained normal in other regions after PONT but were significantly increased in the inferior retina 4 weeks after PONT. The PhNR amplitude reduced significantly in the superior retina 1 week after PONT and then gradually returned to the normal range. The PhNR amplitude in the inferior retina appeared to be increased after PONT with prolonged feeding with LBPs, but this effect was not statistically significant. These results show that LBPs reduce the deterioration of retinal function after PONT through unknown 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