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NG2-Glia Cause Diabetic Blood-Brain Barrier Disruption by Secreting MMP-9
Xiaolong Li, Yan Cai, Zhu Zhong, Maolin Li, Dong Huang, Zhifei Qiao, Hongli Zhou, Zuo Zhang, Jiyin Zhou
Received September 25, 2023  Accepted February 22, 2024  Published online July 23, 2024  
DOI: https://doi.org/10.4093/dmj.2023.0342    [Epub ahead of print]
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AbstractAbstract PDFPubReader   ePub   
Background
Disorders of the blood-brain barrier (BBB) arising from diabetes mellitus are closely related to diabetic encephalopathy. Previous research has suggested that neuron-glia antigen 2 (NG2)-glia plays a key role in maintaining the integrity of the BBB. However, the mechanism by which NG2-glia regulates the diabetic BBB remains unclear.
Methods
Type 2 diabetes mellitus (T2DM) db/db mice and db/m mice were used. Evans-Blue BBB permeability tests and transmission electron microscopy techniques were applied. Tight junction proteins were assessed by immunofluorescence and transmission electron microscopy. NG2-glia number and signaling pathways were evaluated by immunofluorescence. Detection of matrix metalloproteinase-9 (MMP-9) in serum was performed using enzyme-linked immunosorbent assay (ELISA).
Results
In T2DM db/db mice, BBB permeability in the hippocampus significantly increased from 16 weeks of age, and the structure of tight junction proteins changed. The number of NG2-glia in the hippocampus of db/db mice increased around microvessels from 12 weeks of age. Concurrently, the expression of MMP-9 increased in the hippocampus with no change in serum. Sixteen- week-old db/db mice showed activation of the Wnt/β-catenin signaling in hippocampal NG2-glia. Treatment with XAV-939 improved structural and functional changes in the hippocampal BBB and reduced MMP-9 secretion by hippocampal NG2-glia in db/db mice. It was also found that the upregulation of β-catenin protein in NG2-glia in the hippocampus of 16-week-old db/db mice was significantly alleviated by treatment with XAV-939.
Conclusion
The results indicate that NG2-glia can lead to structural and functional disruption of the diabetic BBB by activating Wnt/β-catenin signaling, upregulating MMP-9, and degrading tight junction proteins.
Reviews
Pathophysiology
Glial and Vascular Cell Regulation of the Blood-Brain Barrier in Diabetes
Xiaolong Li, Yan Cai, Zuo Zhang, Jiyin Zhou
Diabetes Metab J. 2022;46(2):222-238.   Published online March 18, 2022
DOI: https://doi.org/10.4093/dmj.2021.0146
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  • 21 Web of Science
  • 22 Crossref
AbstractAbstract PDFPubReader   ePub   
As a structural barrier, the blood-brain barrier (BBB) is located at the interface between the brain parenchyma and blood, and modulates communication between the brain and blood microenvironment to maintain homeostasis. The BBB is composed of endothelial cells, basement membrane, pericytes, and astrocytic end feet. BBB impairment is a distinguishing and pathogenic factor in diabetic encephalopathy. Diabetes causes leakage of the BBB through downregulation of tight junction proteins, resulting in impaired functioning of endothelial cells, pericytes, astrocytes, microglia, nerve/glial antigen 2-glia, and oligodendrocytes. However, the temporal regulation, mechanisms of molecular and signaling pathways, and consequences of BBB impairment in diabetes are not well understood. Consequently, the efficacy of therapies diabetes targeting BBB leakage still lags behind the requirements. This review summarizes the recent research on the effects of diabetes on BBB composition and the potential roles of glial and vascular cells as therapeutic targets for BBB disruption in diabetic encephalopathy.

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Complications
Pathophysiology of Diabetic Retinopathy: The Old and the New
Sentaro Kusuhara, Yoko Fukushima, Shuntaro Ogura, Naomi Inoue, Akiyoshi Uemura
Diabetes Metab J. 2018;42(5):364-376.   Published online October 22, 2018
DOI: https://doi.org/10.4093/dmj.2018.0182
  • 22,410 View
  • 877 Download
  • 124 Web of Science
  • 125 Crossref
AbstractAbstract PDFPubReader   

Vision loss in diabetic retinopathy (DR) is ascribed primarily to retinal vascular abnormalities—including hyperpermeability, hypoperfusion, and neoangiogenesis—that eventually lead to anatomical and functional alterations in retinal neurons and glial cells. Recent advances in retinal imaging systems using optical coherence tomography technologies and pharmacological treatments using anti-vascular endothelial growth factor drugs and corticosteroids have revolutionized the clinical management of DR. However, the cellular and molecular mechanisms underlying the pathophysiology of DR are not fully determined, largely because hyperglycemic animal models only reproduce limited aspects of subclinical and early DR. Conversely, non-diabetic mouse models that represent the hallmark vascular disorders in DR, such as pericyte deficiency and retinal ischemia, have provided clues toward an understanding of the sequential events that are responsible for vision-impairing conditions. In this review, we summarize the clinical manifestations and treatment modalities of DR, discuss current and emerging concepts with regard to the pathophysiology of DR, and introduce perspectives on the development of new drugs, emphasizing the breakdown of the blood-retina barrier and retinal neovascularization.

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Original Article
Study on the Methylglyoxal-induced Apoptosis in Bovine Retinal Pericytes.
Jaetaek Kim, Seok Hong Lee, Jang Won Son, Jeong An Lee, Yeon Sahng Oh, Soon Hyun Shinn
Korean Diabetes J. 2004;28(3):199-207.   Published online June 1, 2004
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AbstractAbstract PDF
BACKGROUND
One of the histopathological hallmarks of early diabetic retinopathy is the loss of pericytes. Evidences suggest that this pericyte loss in vivo is mediated by apoptosis. However, the underlying cause of pericyte apoptosis is not fully understood. This study investigated the influence of methylglyoxal(MGO), a reactive alpha-dicarbonyl compound of glucose metabolism, on the apoptotic cell death in retinal pericytes. METHODS: Primary cultures of retinal pericytes were prepared from isolated bovine retinal microvessels. The cells were incubated under normoglycemic conditions after treatment with 200-800muM methylglyoxal for 6 hours. The cell viability was assessed using the MTT assay. The apoptosis and intracellular reactive oxygen species(ROS) generation were measured using an ELISA kit and flow cytometry, respectively. The NF-kappaB activation was detected by immunocytochemistry. RESULTS: MGO produced a progressive cytotoxic effect on the retinal pericytes. An analysis of the internucleosomal DNA fragmentation by ELISA showed that MGO(200 to 800muM) induced apoptosis in a concentration-dependent manner. ROS were generated earlier and the antioxidant, N-acetyl cysteine, inhibited the MGO-induced apoptosis. The NF-kappaB activation and increased caspase-3 activity were detected. The apoptosis was also inhibited by the caspase-3 inhibitor, Z-DEVD-fmk, or the NF-kappaB inhibitor, pyrrolidine dithiocarbamate. CONCLUSION: These results suggest that the elevated MGO levels observed in diabetes may cause apoptosis in the retinal pericytes through an oxidative stress mechanism, and suggests that the nuclear activation of NF-kappaB is involved in the apoptotic process.

Diabetes Metab J : Diabetes & Metabolism Journal
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